Research Article Incidence of Keratinophilic Fungi from...

8
Research Article Incidence of Keratinophilic Fungi from Selected Soils of Vidarbha Region of Maharashtra State, India Sunil Kumar Deshmukh and Shilpa Amit Verekar Department of Natural Products, Piramal Enterprises Limited, 1 Nirlon Complex, Off Western Express Highway, Near NSE Complex, Goregaon (East), Mumbai 400 063, India Correspondence should be addressed to Sunil Kumar Deshmukh; sunild2811@rediffmail.com Received 14 July 2014; Accepted 5 October 2014; Published 10 November 2014 Academic Editor: Daniel Elad Copyright © 2014 S. K. Deshmukh and S. A. Verekar. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. One hundred and fiſty samples were collected from eleven districts of Vidarbha region of Maharashtra state and screened for the presence of keratinophilic fungi using hair baiting technique for isolation. Seventy-one isolates were recovered and identified. e cultures were identified using macro- and micromorphological features. eir identification was also confirmed by the BLAST search of sequences of the ITS1-5.8S-ITS2 rDNA region against the NCBI/Genbank data and compared with deposited sequences for identification purpose. irteen species of eight genera were isolated, namely, Auxarthron conjugatum (2.00%), Chrysosporium indicum (14.00%), Chrysosporium evolceanui (2.66%), Chrysosporium tropicum (4.66%), Chrysosporium zonatum (1.33%), Chrysosporium state of Ctenomyces serratus (3.33%), Gymnascella dankaliensis (1.33%), Gymnascella hyalinospora (0.66%), Gymnoascoideus petalosporus (0.66%), Microsporum gypseum complex (9.33%), Trichophyton mentagrophytes (2.00%), T. terrestre (3.33%), and Uncinocarpus queenslandicus (2.00%). is study indicates that the soils of Vidarbha region of Maharashtra may be significant reservoirs of certain keratinophilic fungi. 1. Introduction Keratinophilic fungi are an ecologically important group of fungi that decompose one of the most abundant and highly stable animal proteins on earth-keratin which they utilize as a nutrient substrate for growth. e distribution of these fungi depends on different factors, one of which, of vital impor- tance, is human and/or animal presence [1]. Some of these fungi are well-known dermatophytes and are known to cause superficial cutaneous infections (dermatophytoses) of kera- tinized tissues (skin, hair, and nails) of humans and animals. Mycotic infection is reported throughout the world, and it is extremely contagious [2]. e occurrence of dermatophytes in soil was reported for the first time by Vanbreuseghem [3] using the hair bait technique. Since then studies on the isola- tion of keratinophilic fungi from soil have been investigated throughout the world [47]. Vidarbha is the eastern region of Maharashtra state which lies between 17 57 –21 46 N latitude and 75 57 –80 59 E longitude. e temperature of Vidarbha ranges from a minimum of 12–25 C to a maximum of 30–48 C with relative humidity varying from 10–15% to 60–95%. Tropical climate and topology of Vidarbha region of Maharashtra make this region a potentially interesting area to study the distribution of these fungi. We therefore undertook this study and report the results obtained. 2. Materials and Methods 2.1. Collection and Processing of Soil Samples. One hundred and fiſty samples were collected from various sites of eleven districts, namely, Akola, Amravati, Bhandara, Buldhana, Chandrapur, Gadchiroli, Gondia, Nagpur, Wardha, Yavatmal, and Washim from Vidhabha region of Maharashtra during June 2009–May 2010 (Figures 1 and 2 and Table 1). e sam- ples were collected from the superficial layer of soil at a depth not exceeding 3–5 cm with a plastic spoon in sterile poly- ethylene bags, brought to the laboratory and stored at 15 C for a maximum of two weeks if not processed promptly. e samples were collected from forest land, cultivated land, road side, public gardens, poultry farm, cattle farm, garbage, and Hindawi Publishing Corporation Journal of Mycology Volume 2014, Article ID 148970, 7 pages http://dx.doi.org/10.1155/2014/148970

Transcript of Research Article Incidence of Keratinophilic Fungi from...

Page 1: Research Article Incidence of Keratinophilic Fungi from ...downloads.hindawi.com/archive/2014/148970.pdf · respectively, as described by White et al. [ ]. Ampli cation was performed

Research ArticleIncidence of Keratinophilic Fungi from Selected Soils ofVidarbha Region of Maharashtra State India

Sunil Kumar Deshmukh and Shilpa Amit Verekar

Department of Natural Products Piramal Enterprises Limited 1 Nirlon Complex Off Western Express Highway Near NSE ComplexGoregaon (East) Mumbai 400 063 India

Correspondence should be addressed to Sunil Kumar Deshmukh sunild2811rediffmailcom

Received 14 July 2014 Accepted 5 October 2014 Published 10 November 2014

Academic Editor Daniel Elad

Copyright copy 2014 S K Deshmukh and S A Verekar This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

One hundred and fifty samples were collected from eleven districts of Vidarbha region of Maharashtra state and screened for thepresence of keratinophilic fungi using hair baiting technique for isolation Seventy-one isolates were recovered and identifiedThe cultures were identified using macro- and micromorphological features Their identification was also confirmed by theBLAST search of sequences of the ITS1-58S-ITS2 rDNA region against the NCBIGenbank data and compared with depositedsequences for identification purpose Thirteen species of eight genera were isolated namely Auxarthron conjugatum (200)Chrysosporium indicum (1400) Chrysosporium evolceanui (266) Chrysosporium tropicum (466) Chrysosporium zonatum(133) Chrysosporium state of Ctenomyces serratus (333) Gymnascella dankaliensis (133) Gymnascella hyalinospora (066)Gymnoascoideus petalosporus (066)Microsporum gypseum complex (933) Trichophyton mentagrophytes (200) T terrestre(333) and Uncinocarpus queenslandicus (200) This study indicates that the soils of Vidarbha region of Maharashtra may besignificant reservoirs of certain keratinophilic fungi

1 Introduction

Keratinophilic fungi are an ecologically important group offungi that decompose one of the most abundant and highlystable animal proteins on earth-keratin which they utilize asa nutrient substrate for growthThedistribution of these fungidepends on different factors one of which of vital impor-tance is human andor animal presence [1] Some of thesefungi are well-known dermatophytes and are known to causesuperficial cutaneous infections (dermatophytoses) of kera-tinized tissues (skin hair and nails) of humans and animalsMycotic infection is reported throughout the world and it isextremely contagious [2] The occurrence of dermatophytesin soil was reported for the first time by Vanbreuseghem [3]using the hair bait technique Since then studies on the isola-tion of keratinophilic fungi from soil have been investigatedthroughout the world [4ndash7] Vidarbha is the eastern regionof Maharashtra state which lies between 17∘571015840ndash21∘461015840Nlatitude and 75∘571015840ndash80∘591015840E longitude The temperature ofVidarbha ranges from a minimum of 12ndash25∘C to a maximum

of 30ndash48∘C with relative humidity varying from 10ndash15 to60ndash95 Tropical climate and topology of Vidarbha region ofMaharashtramake this region a potentially interesting area tostudy the distribution of these fungi We therefore undertookthis study and report the results obtained

2 Materials and Methods

21 Collection and Processing of Soil Samples One hundredand fifty samples were collected from various sites of elevendistricts namely Akola Amravati Bhandara BuldhanaChandrapur Gadchiroli Gondia NagpurWardha Yavatmaland Washim from Vidhabha region of Maharashtra duringJune 2009ndashMay 2010 (Figures 1 and 2 and Table 1) The sam-ples were collected from the superficial layer of soil at a depthnot exceeding 3ndash5 cm with a plastic spoon in sterile poly-ethylene bags brought to the laboratory and stored at 15∘Cfor a maximum of two weeks if not processed promptly Thesamples were collected from forest land cultivated land roadside public gardens poultry farm cattle farm garbage and

Hindawi Publishing CorporationJournal of MycologyVolume 2014 Article ID 148970 7 pageshttpdxdoiorg1011552014148970

2 Journal of Mycology

India

0 200 400(xm)

N

Figure 1 Location of the State of Maharashtra in India

lake side For isolation hair bait technique of Vanbreuseghem[3] was used Sterile Petri dishes were half filled with the soilsamples andmoistened with water and baited with keratin byburying sterile human hairs in the soil Human hairs from a25-years-old male were used The hairs were washed severaltimes first with detergent (hair shampoo) followed by waterand thenwith diethyl ether and finally autoclaved at 121∘C for15minThe dishes were incubated at room temperature (28∘Cplusmn 2) and examined daily after 5 days for fungal growth for 4weeks

22 Isolation and Identification of Keratinophilic Fungi Afterobserving the growth under a stereoscopic binocular micro-scope it was cultured on slopesplates of Sabouraudrsquos dextroseagar supplemented with chloramphenicol (50mgL) andcycloheximide (500mgL) Cultures were incubated at roomtemperature for five to ten days following which the cultureswere microscopically checked for purity and subcultured toget pure cultures These fungi were identified based on thevarious available monographs using macro- and micromor-phological features of these cultures [8ndash12]

23 Molecular Identification of Keratinophilic Fungi Molec-ular characteristics of the cultures were studied by determi-nation of their DNA sequences of the ITS1-58S-ITS2 regionGenomic DNA was extracted by the Miniprep protocol ofLee and Taylor [13] The ITS1-58S-ITS2 rDNA was amplifiedusing ITS1 and ITS4 as the forward and reverse primersrespectively as described by White et al [14] Amplificationwas performed in 100120583L reaction volumes containing 10xbuffer 10 120583L MgCl

2(25mM) 2 120583L dNTP (10mM) 2 120583L ITS1

Table 1 Distribution of soil samples examined of Vidarbha regionof Maharashtra (India)

DistrictsNumber ofsamplesexamined

Number ofpositive samples positive

Akola 24 11 4583Amravati 20 9 4500Bhandara 15 8 5333Buldhana 15 7 4666Chandrapur 5 2 4000Gadchiroli 5 2 4000Gondia 6 4 6666Nagpur 15 7 4666Wardha 15 5 3333Yavatmal 15 8 5333Washim 15 8 5333Total 150 71 4733

primer (20 pm) 2120583L ITS4 primer (20 pm) 2120583L Taq Poly-merase (25U) 1120583L DNA Sample (5 120583gmL) 3120583L and MilliQ Water 78120583L The PCR reaction was carried out using aThermal Cycler (MJ research PTC 200) with conditions asfollows denaturation for five minutes at 94∘C 34 cycles of(30 sec at 94∘C 30 sec at 55∘C and 1min at 72∘C) extensionfor four minutes at 72∘C and storage at 4∘C Negative controlswere used in each set of reactions The final products wereanalyzed by electrophoresis on 12 agarose (Sigma) ThePCR products were purified using Qiagen Gel extraction kit(CAT number 28704) and the PCR products of expected sizewere sequenced using ITS1 and ITS4 primers in an AppliedBiosystem 3730 DNA analyzer at GenOmbiotech PuneIndia

24 Phylogenetic Analysis Similarity analysis of the nucleoti-des was performed by BLAST searches against sequencesavailable in GenBank [15] For phylogenetic tree construc-tion multiple sequences were obtained from GenBank andthe alignments were performed using MEGA6 [16]

3 Results and Discussion

The results of the isolations are presented in Table 2 Theyreveal that out of 150 samples only 71 yielded keratinophilicfungi that can be categorized in thirteen species of eightgenera namely Auxarthron conjugatum (200) Chrysospo-rium indicum (1400) Chrysosporium evolceanui (266)Chrysosporium tropicum (466) Chrysosporium zonatum(133) Chrysosporium state of Ctenomyces serratus (333)Gymnascella dankaliensis (133) Gymnascella hyalinospora(066) Gymnoascoideus petalosporus (066) Microspo-rum gypseum complex (933) Trichophyton mentagrophytes(200) T terrestre (333) and Uncinocarpus queenslandi-cus (200)

Journal of Mycology 3

Table2Distrib

utionof

keratin

ophilic

fung

iindifferent

typeso

fsoilsof

Vidarbha

region

ofMaharashtra

Source

ofsoilsamples

Forest

land

Cultivated

land

Road

side

Public

gardens

Poultry

farm

Cattle

farm

Garbage

Lake

side

Total

distr

ibution

Num

bero

fsam

ples

exam

ined

2020

2025

1520

2010

150

Num

bero

fpositive

samples

611

913

711

95

71Distrib

ution(

)30

5545

5246

66

5545

504733

1Au

xarthron

conjugatum

(Kuehn

)OrrampKu

ehn

mdashmdash

1mdash

mdash1

mdash1

3200

2Ch

rysosporium

indicum

(Randh

awaamp

Sand

hu)G

arg

22

35

24

21

211400

3Ch

rysosporium

evolceanui

(Randh

awaamp

Sand

hu)G

arg

mdash1

1mdash

mdashmdash

11

4266

4Ch

rysosporium

tropicum

Carm

ichael

mdash1

12

mdash1

11

7466

5Ch

rysosporium

zonatum

Al-M

usallam

ampTan

mdash1

mdashmdash

mdash1

mdashmdash

213

3

6Ch

rysosporium

stateof

Ctenom

ycesserratus

Eidam

13

1mdash

mdashmdash

mdashmdash

5333

7Gy

mnoascella

dankalien

sis1

mdashmdash

mdashmdash

mdash1

mdash2

133

8Gy

mna

scellahyalinospora

(Kuehn

etal)Cu

rrah

mdashmdash

mdash1

mdashmdash

mdashmdash

1066

9Gy

mnoascoideusp

etalosporusOrrR

oyampGho

shmdash

mdashmdash

1mdash

mdashmdash

mdash1

066

10Microsporum

gypseum

(EB

odin)G

uiartamp

Grig

oraki

11

mdash3

33

21

1493

311

Trich

ophytonmentagrophytes(CPRo

bin)

Sabo

ur

mdashmdash

1mdash

11

mdashmdash

3200

12Trich

ophytonterrestre

DurieampFrey

1mdash

1mdash

1mdash

2mdash

5333

13Un

cinocarpu

squeensla

ndicu

s(Ap

inisampRe

es)S

igler

mdash2

mdash1

mdashmdash

mdashmdash

3200

Total

611

913

711

95

71

4 Journal of Mycology

Akola

Buldhana

Amravati NagpurWardha

Yawatmal ChandrapurWashim

Gadchiroli

GondhiaBhandara

Figure 2 Sites of collection of soil samples in Vidarbha region of Maharashtra

All thirteen strains yielded unique PCR amplificationThe sequences of the ITS1-58S-ITS2 rDNA region for thethirteen strains were from 527 bp to 631 bp Chrysosporiumstate of Ctenomyces serratus and Trichophyton mentagro-phytes were the smallest and the largest respectively Theother species showed a product size of approximately 600 bpThere was considerable difference in the sequence data of thethirteen strains analyzed The data were also compared withsequences deposited in the NCBIGenbank for identificationpurposes and a tree was constructed with the nearest typeof strain sequences based on rRNA gene sequences (ITSregion) using the Maximum Composite Likelihood Method(Figure 3) The Phylogenetic tree indicates different clus-ters for each isolate showing their sequence variation Thesequences obtained show greater than 96 similarity to thereference sequences available in NCBI Genbank database

Chrysosporium indicum (1400) was the most prevalentspecies and this is in agreement with the finding of previousworkers [17ndash20] Its high percentage of distribution clearlyindicates that it is well adapted to warmer condition of India[21]Microsporumgypseum complexwas foundnext toC ind-icum in distribution (933) and has been reported from vari-ous parts of IndiaWe also encounteredArthroderma sp threetimes in association with theMicrosporum gypseum complexwhichwasmade upof the two teleomorph statesArthrodermaincurvata and A gypsea but A fulva was altogether absentHowevermating experiments were not conducted to confirmits specific identity It was reported from Indian soils by Deyand Kakoti [22] It was further isolated from various partsof India [21 23ndash27] Chrysosporium tropicum was next toMgypseum comprising of 466 in distribution It is a cosmo-politan species and has been reported from various parts ofIndia [17 18 27 28]

The other species of Chrysosporium isolated were Chry-sosporium evolceanui (266) Chrysosporium zonatum(133) and Chrysosporium state of Ctenomyces serratus(333) Chrysosporium evolceanuiwas reported from Indiansoils as Trichophyton evolceanui by Randhawa and Sandhu[17] then Garg [21] placed it in the genus Chrysosporium asC evolceanui It is reported from Indian soils [26 29 30]Various workers have isolated Chrysosporium zonatum fromIndian soil [31 32] Chrysosporium state of Ctenomyces serra-tus was recorded in 333 of samples and this has beenreported from various parts of India [17ndash19 21]

Other species of keratinophilic fungi isolated wereGymnascella dankaliensis (133) Gymnascella hyalinospora(066) Gymnoascoideus petalosporus (066) Auxarth-ron conjugatum (200) and Uncinocarpus queenslandicus(200)G dankailensis is reported from Indian soils [29 33]Gymnascella hyalinospora was reported from Indian soils bySingh and Kushwaha [32] and Deshmukh [34] Gymnoascoi-deus petalosporus was previously recorded from Chilka Lakesoil [35] soils from Vedanthangal Water Bird Sanctuary [20]and soils of Orissa [33] Auxarthron conjugatum is reportedfrom Indian soils by Deshmukh and Verekar [20] Jain andAgrawal [36] andDeshmukh andAgrawal [37] Anamorphicstate of Uncinocarpus queenslandicus ie Chrysosporium que-enslandicumwas reported from Indian soil [18 24 26 38 39]

The other species of dermatophytes recovered were Tri-chophyton mentagrophytes (200) and T terrestre (333)Trichophyton mentagrophytes has been reported from Indiansoils [26 34 40ndash42] and is known to cause diseases in manand animals [43 44] T terrestre has been reported fromIndian soils by various workers [26 45ndash47]

The prevalence of these fungi in the soils of region ofVidarbha is of importance for their pathogenic potential

Journal of Mycology 5

AJ439446 C indicum

AJ005368 C evolceanui

AB219229 C zonatum

EF568044 C tropicum

C zonatum Vidarbha isolate

U queenslandicus

AB861842 U queenslandicus

T terrestre

EF631622 T terrestre

T mentagrophytes

HQ223449 T mentagrophytes

C serratus

AJ877222 C serratus

M gypseum

JQ390554 M gypseum

G dankaliensis

AY304514 G dankaliensis

G hyalinospora

HM991271 G hyalinospora

G petalosporus

HM991270 G petalosporus

100

100

100

100

100

100

100

100

100

100

98

99

84

92

46

98

80

68

46

63

64

000002004006008

C tropicum

C indicum Vidarbha isolate

C evolceanui Vidarbha isolate

HM036583 Auxarthron conjugatum

Auxarthron conjugatum

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Figure 3 Phylogenetic tree based on ITS1-58S-ITS4 region sequences for isolated 13 keratinophilic fungi with reference strains Numbers atthe respective nodes are percentage of 1000 bootstrap replicates Bar indicates genetic distance due to sequence variation

and has been confirmed in several investigations in differentparts of the world For example Chrysosporium zonatumwasreported to cause disseminated infection in a patient withchronic granulomatous disease [48] In Japan C zonatumstrains were isolated from bronchial lavage from a female inChiba and from a male in Kyushu Both patients presentedpulmonary cavity sites [49] Chrysosporium tropicum wasreported from comb lesion in two different breeds of chickenin India [50]There are reports of disseminated infections dueto C queenslandicum in garter snakes [51] Gymnascella dan-kaliensis was reported from superficial infections in humanbeings [52] and Iwen et al [53] isolatedGymnascella hyalinos-pora from invasive pulmonary infection in a patient with

acute myelogenous leukemia Similarly Lyskova [54] isolatedChrysosporium queenslandicum C sulfureum C tropicumMalbranchea pulchella and Myriodontium keratinophilumfrom infections of the skin and nails of patients in the Mora-vian-Silesian Region (Czech Republic)Thus these fungimaybe regarded as opportunistic pathogens

There are some reports of occurrence of keratinophilicfungi from various parts of Maharashtra [40 47 55 56]but to best of our knowledge this is the first comprehensivereport on incidence of keratinophilic fungi from Vidarbharegion These findings are in agreement with the findings ofprevious work on keratinophilic fungi It appears from thisstudy that a rich variety of keratinophilic fungal flora exists

6 Journal of Mycology

in Vidarbha region of Maharashtra which may be attributedto the climatic and environmental conditions such as the soiltype vegetation fauna and human habitations Garg et al[57] emphasized that the climate and perhaps other environ-mental factors are important in determining the distributionof keratinophilic fungi in ecological habitats

Our findings confirm the presence of keratinophilic andrelated dermatophytes in the soils of Vidarbha region Theseareas potentially have a high risk for causing cutaneous fungalinfections in humans and animals and could be considered asa source of these infections

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] S K Deshmukh and S A Verekar ldquoThe occurrence of dermato-phytes and other keratinophilic fungi from the soils of Hima-chal Pradesh (India)rdquo Czech Mycology vol 58 no 1-2 pp 117ndash124 2006

[2] M T Hedayati A Mohseni-Bandpi and S Moradi ldquoA surveyon the pathogenic fungi in soil samples of potted plants fromSari hospitals Iranrdquo Journal of Hospital Infection vol 58 no 1pp 59ndash62 2004

[3] R Vanbreuseghem ldquoTechnique biologique pour lisolement desdermatophytes du solrdquo Annales de la Societe Belge de MedecineTropicale vol 32 pp 173ndash178 1952

[4] S M Zaki Y Mikami A A Karam El-Din and Y A YoussefldquoKeratinophilic fungi recovered from muddy soil in Cairovicinities Egyptrdquo Mycopathologia vol 160 no 3 pp 245ndash2512005

[5] S K Deshmukh and S A Verekar ldquoKeratinophilic fungi fromthe vicinity of meteorite crater soils of Lonar (India)rdquo Myco-pathologia vol 162 no 4 pp 303ndash306 2006

[6] H C Gugnani S Sharma and K Wright ldquoA preliminary studyon the occurrence of keratinophilic fungi in soils of JamaicardquoRevista do Instituto de Medicina Tropical de Sao Paulo vol 56no 3 pp 231ndash234 2014

[7] K Pakshir M Rahimi Ghiasi K Zomorodian and A R Ghar-avi ldquoIsolation and molecular identification of keratinophilicfungi from public parks soil in Shiraz Iranrdquo BioMed ResearchInternational vol 2013 Article ID 619576 5 pages 2013

[8] L Sigler and J W Carmichael ldquoTaxonomy ofMalbranchea andsome other hyphomycetes with arthroconidiardquoMycotaxon vol4 pp 349ndash488 1976

[9] C A N Van Oorschot ldquoA revision of Chrysosporium and alliedgenerardquo Studies in Mycology vol 20 pp 1ndash89 1980

[10] R S Currah ldquoTaxonomy of the Onygenales ArthrodermaceaeGymnoascaceae Myxotrichaceae and Onygenaceaerdquo Myco-taxon vol 24 pp 1ndash216 1985

[11] J A von Arx ldquoThe ascomycetes genus Gymnoascusrdquo Persooniavol 13 pp 173ndash183 1986

[12] J Cano and J Gurrao ldquoThe genus Aphanoascusrdquo MycologicalResearch vol 94 pp 355ndash377 1990

[13] S B Lee and J W Taylor ldquoIsolation of DNA from fungalmycelium and single cellsrdquo in Protocols A Guide toMethods andApplications M A Innis H D Gelfand J J Sninsky and T

J White Eds pp 282ndash287 Academic Press San Diego CalifUSA 1990

[14] T J White T Bruns S Lee and J Taylor ldquoAmplification anddirect sequencing of fungal ribosomal RNA genes for phyloge-neticsrdquo in PCR Protocols A Guide to Methods and ApplicationsA Innis D H Gelfand J J Sninsky and T J White Eds pp315ndash322 Academic Press San Diego Calif USA 1990

[15] S F AltschulW GishWMiller EWMyers and D J LipmanldquoBasic local alignment search toolrdquo Journal ofMolecular Biologyvol 215 no 3 pp 403ndash410 1990

[16] K Tamura G Stecher D Peterson A Filipski and S KumarldquoMEGA6molecular evolutionary genetics analysis version 60rdquoMolecular Biology and Evolution vol 30 no 12 pp 2725ndash27292013

[17] H S Randhawa and R S Sandhu ldquoA survey of soil inhabit-ing dermatophytes and related keratinophilic fungi of IndiardquoSabouraudia Journal of Medical and Veterinary Mycology vol4 no 2 pp 71ndash79 1965

[18] S K Deshmukh and S C Agrawal ldquoPrevalence of dermato-phytes and other keratinophilic fungi in soils of MadhyaPradesh (India)rdquoMykosen vol 26 no 11 pp 574ndash577 1983

[19] S K Deshmukh and S A Verekar ldquoPrevalence of Keratinophil-ic fungi in ldquoUsarrdquo Soils of Uttar Pradesh Indiardquo MicrobiologyResearch vol 2 no 2 p e15 2011

[20] S K Deshmukh and S A Verekar ldquoIncidence of keratinophilicfungi from the soils of Vedanthangal Water Bird Sanctuary(India)rdquoMycoses vol 54 no 6 pp 487ndash490 2011

[21] A K Garg ldquoIsolation of dermatophytes and other keratinophil-ic fungi from soils in Indiardquo Sabouraudia Journal ofMedical andVeterinary Mycology vol 4 no 4 pp 259ndash264 1966

[22] N C Dey and L M Kakoti ldquoMicrosporum gypseum in IndiardquoJournal of the IndianMedical Association vol 25 no 5 pp 160ndash164 1955

[23] R K S Kushwaha and S C Agarwal ldquoSome keratinophilicfungi and related dermatophytes from soilsrdquo Proceedings of theIndian National Science Academy vol 42 no B pp 102ndash1101976

[24] C J Singh B G Singh and B S Singh ldquoKeratinophilic fungiof Ghana birds sanctuary Bharatpur (Rajasthan)rdquo Advances inPlant Sciences vol 7 pp 280ndash291 1994

[25] G M Vidyasagar N Hosmani and D Shivkumar ldquoKer-atinophilic fungi isolated from hospital dust and soils of publicplaces at Gulbarga Indiardquo Mycopathologia vol 159 no 1 pp13ndash21 2005

[26] I Singh A Mishra and R K S Kushwaha ldquoDermatophytesrelated keratinophilic and opportunistic fungi in indoor dust ofhouses and hospitalsrdquo Indian Journal of Medical Microbiologyvol 27 no 3 pp 242ndash246 2009

[27] N Jain and M Sharma ldquoDistribution of dermatophytes andother related fungi in Jaipur city with particular reference tosoil pHrdquoMycoses vol 54 no 1 pp 52ndash58 2011

[28] JW Carmichael ldquoChrysosporium and some other aleuriosporichyphomycetesrdquo Canadian Journal of Botany vol 40 pp 1137ndash1173 1962

[29] S A Verekar and S K Deshmukh ldquoIncidence of keratinophilicfungi from caves around Mumbai Maharastra (India)rdquo Journalof Basic and Applied Mycology vol 5 pp 62ndash64 2006

[30] I Singh R K S Kushwaha andP Parihar ldquoKeratinophilic fungiin soil of potted plants of indoor environments inKanpur Indiaand their proteolytic abilityrdquoMycoscience vol 50 no 4 pp 303ndash307 2009

Journal of Mycology 7

[31] S Katiyar and R K S Kushwaha ldquoHuman hair colonizing fungiin water sediments of IndiardquoMycopathologia vol 152 no 2 pp81ndash84 2001

[32] I Singh and R K S Kushwaha ldquoDermatophytes and relatedkeratinophilic fungi in soil of parks and agricultural fields ofUttar Pradesh Indiardquo Indian Journal of Dermatology vol 55 no3 pp 306ndash308 2010

[33] B Sur and G R Ghosh ldquoKeratinophilic fungi from OrissaIndia I isolation from soilsrdquo Sabouraudia Journal ofMedical andVeterinary Mycology vol 18 no 4 pp 269ndash274 1980

[34] S K Deshmukh ldquoIncidence of keratinophilic fungi fromselected soils of Kerala state (India)rdquo Mycopathologia vol 156no 3 pp 177ndash181 2003

[35] G R Ghosh and S Bhatt ldquoKeratinophilic Fungi from ChilkaLake-side Soil Orissa (India)rdquo Indian Journal of Microbiologyvol 40 no 4 pp 247ndash254 2000

[36] P C Jain and S C Agrawal ldquoSome additions to IndianMalbrancheardquo Kavaka vol 7 pp 69ndash72 1979

[37] S K Deshmukh and S C Agrawal ldquoIsolation of dermatophytesand other keratinophilic fungi from soils of Jammu IndiardquoMycoses vol 46 no 5-6 pp 226ndash228 2003

[38] S Kaul and G Sumbali ldquoKeratinolysis by poultry farm soilfungirdquoMycopathologia vol 139 no 3 pp 137ndash140 1997

[39] P Saxena A Kumar and J N Shrivastava ldquoDiversity ofkeratinophilic mycoflora in the soil of Agra (India)rdquo FoliaMicrobiologica vol 49 no 4 pp 430ndash434 2004

[40] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from the vicinity of salt pan soils of MumbaiIndiardquoMycopathologia vol 157 no 3 pp 265ndash267 2004

[41] H C Gugnani A Paliwal-Joshi H Rahman et al ldquoOccurrenceof pathogenic fungi in soil of burrows of rats and of other sitesin bamboo plantations in India and NepalrdquoMycoses vol 50 no6 pp 507ndash511 2007

[42] M Sharma and M Sharma ldquoIncidence of dermatophytes andother keratinophilic fungi in the schools and college playgroundsoils of Jaipur Indiardquo African Journal of Microbiology Researchvol 4 no 24 pp 2647ndash2654 2010

[43] L N Mohapatra H C Gugnani and K Shivrajan ldquoNaturalinfection in laboratory animals due to Trichophyton mentagro-phytes in IndiardquoMycopathologia et Mycologia Applicata vol 24no 3 pp 275ndash280 1964

[44] C A Oyeka ldquoTrichophyton mentagrophytes a keratinophilicfungusrdquo in Biology of Dermatophytes and other KeratinophilicFungi R K S Kushwaha and J Guarro Eds pp 60ndash65 RevistaIberoamericana de Micologia Bilbao Spain 2000

[45] T N Verma B K Sinha and U L Das ldquoIsolation of ker-atinophilic fungi from soil in Bihar (India)rdquo Mykosen vol 25no 8 pp 449ndash452 1982

[46] S K Deshmukh ldquoIncidence of dermatophytes and other ker-atinophilic fungi in the glacier bank soils of the Kashmir valleyIndiardquoMycologist vol 16 no 4 pp 165ndash167 2002

[47] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from Karnala bird sanctuary Maharashtra(India)rdquo Journal of Basic and Applied Mycology vol 1 no 2 pp194ndash196 2002

[48] E Roilides L Sigler E Bibashi H Katsifa N Flaris andC Panteliadis ldquoDisseminated infection due to Chrysosporiumzonatum in a patient with chronic granulomatous disease andreview of non-aspergillus fungal infections in patients with thisdiseaserdquo Journal of ClinicalMicrobiology vol 37 no 1 pp 18ndash251999

[49] L Sigler A L Flis and JW Carmichael ldquoThe genusUncinocar-pus (Onygenaceae) and its synonym Brunneospora new con-cepts combinations and connections to anamorphs in Chrysos-porium and further evidence of relationship with Coccidioidesimmitisrdquo Canadian Journal of Botany vol 76 no 9 pp 1624ndash1636 1998

[50] S A Saidi S Bhatt J L Richard A Sikdar and G R GhoshldquoChrysosporium tropicum as a probable cause of mycosis ofpoultry in Indiardquo Mycopathologia vol 125 no 3 pp 143ndash1471994

[51] T Vissiennon K F Schuppel E Ullrich and A F KuijpersldquoCase report A disseminated infection due to Chrysosporiumqueenslandicum in a garter snake (Thamnophis)rdquoMycoses vol42 no 1-2 pp 107ndash110 1999

[52] G S de Hoog and J Guarro Atlas of Clinical Fungi Centraal-bureau voor Schimmelcultures Baarn The Netherlands 1995

[53] P C Iwen L Sigler S Tarantolo et al ldquoPulmonary infectioncaused by Gymnascella hyalinospora in a patient with acutemyelogenous leukemiardquo Journal of Clinical Microbiology vol38 no 1 pp 375ndash381 2000

[54] P Lyskova ldquoSaprotrophicmicroscopic fungi and dermatophytesaccompanying infections of the skin and nails of patients in theMoravian-Silesian Region (Czech Republic)rdquo Czech Mycologyvol 59 pp 125ndash137 2007

[55] A A Padhye S PMisra andM JThirumalachar ldquoOccurrenceof soil inhabiting dermatophytes and other keratinophilic fungifrom soils in Poonardquo Hindustan Antibiotics Bulletin vol 9 no2 pp 90ndash93 1966

[56] A A Padhye V H Pawar R S Sukapure and M J Thiru-malachar ldquoKeratinophilic fungi from marine soils of BombayIndia Irdquo Hindustan Antibiotics Bulletin vol 10 no 2 pp 138ndash141 1967

[57] A P Garg S Gandotra K G Mukerji and G J F Pugh ldquoEcol-ogy of keratinophilic fungirdquo Proceedings Plant Sciences vol 94no 2-3 pp 149ndash163 1985

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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International Journal of

Microbiology

Page 2: Research Article Incidence of Keratinophilic Fungi from ...downloads.hindawi.com/archive/2014/148970.pdf · respectively, as described by White et al. [ ]. Ampli cation was performed

2 Journal of Mycology

India

0 200 400(xm)

N

Figure 1 Location of the State of Maharashtra in India

lake side For isolation hair bait technique of Vanbreuseghem[3] was used Sterile Petri dishes were half filled with the soilsamples andmoistened with water and baited with keratin byburying sterile human hairs in the soil Human hairs from a25-years-old male were used The hairs were washed severaltimes first with detergent (hair shampoo) followed by waterand thenwith diethyl ether and finally autoclaved at 121∘C for15minThe dishes were incubated at room temperature (28∘Cplusmn 2) and examined daily after 5 days for fungal growth for 4weeks

22 Isolation and Identification of Keratinophilic Fungi Afterobserving the growth under a stereoscopic binocular micro-scope it was cultured on slopesplates of Sabouraudrsquos dextroseagar supplemented with chloramphenicol (50mgL) andcycloheximide (500mgL) Cultures were incubated at roomtemperature for five to ten days following which the cultureswere microscopically checked for purity and subcultured toget pure cultures These fungi were identified based on thevarious available monographs using macro- and micromor-phological features of these cultures [8ndash12]

23 Molecular Identification of Keratinophilic Fungi Molec-ular characteristics of the cultures were studied by determi-nation of their DNA sequences of the ITS1-58S-ITS2 regionGenomic DNA was extracted by the Miniprep protocol ofLee and Taylor [13] The ITS1-58S-ITS2 rDNA was amplifiedusing ITS1 and ITS4 as the forward and reverse primersrespectively as described by White et al [14] Amplificationwas performed in 100120583L reaction volumes containing 10xbuffer 10 120583L MgCl

2(25mM) 2 120583L dNTP (10mM) 2 120583L ITS1

Table 1 Distribution of soil samples examined of Vidarbha regionof Maharashtra (India)

DistrictsNumber ofsamplesexamined

Number ofpositive samples positive

Akola 24 11 4583Amravati 20 9 4500Bhandara 15 8 5333Buldhana 15 7 4666Chandrapur 5 2 4000Gadchiroli 5 2 4000Gondia 6 4 6666Nagpur 15 7 4666Wardha 15 5 3333Yavatmal 15 8 5333Washim 15 8 5333Total 150 71 4733

primer (20 pm) 2120583L ITS4 primer (20 pm) 2120583L Taq Poly-merase (25U) 1120583L DNA Sample (5 120583gmL) 3120583L and MilliQ Water 78120583L The PCR reaction was carried out using aThermal Cycler (MJ research PTC 200) with conditions asfollows denaturation for five minutes at 94∘C 34 cycles of(30 sec at 94∘C 30 sec at 55∘C and 1min at 72∘C) extensionfor four minutes at 72∘C and storage at 4∘C Negative controlswere used in each set of reactions The final products wereanalyzed by electrophoresis on 12 agarose (Sigma) ThePCR products were purified using Qiagen Gel extraction kit(CAT number 28704) and the PCR products of expected sizewere sequenced using ITS1 and ITS4 primers in an AppliedBiosystem 3730 DNA analyzer at GenOmbiotech PuneIndia

24 Phylogenetic Analysis Similarity analysis of the nucleoti-des was performed by BLAST searches against sequencesavailable in GenBank [15] For phylogenetic tree construc-tion multiple sequences were obtained from GenBank andthe alignments were performed using MEGA6 [16]

3 Results and Discussion

The results of the isolations are presented in Table 2 Theyreveal that out of 150 samples only 71 yielded keratinophilicfungi that can be categorized in thirteen species of eightgenera namely Auxarthron conjugatum (200) Chrysospo-rium indicum (1400) Chrysosporium evolceanui (266)Chrysosporium tropicum (466) Chrysosporium zonatum(133) Chrysosporium state of Ctenomyces serratus (333)Gymnascella dankaliensis (133) Gymnascella hyalinospora(066) Gymnoascoideus petalosporus (066) Microspo-rum gypseum complex (933) Trichophyton mentagrophytes(200) T terrestre (333) and Uncinocarpus queenslandi-cus (200)

Journal of Mycology 3

Table2Distrib

utionof

keratin

ophilic

fung

iindifferent

typeso

fsoilsof

Vidarbha

region

ofMaharashtra

Source

ofsoilsamples

Forest

land

Cultivated

land

Road

side

Public

gardens

Poultry

farm

Cattle

farm

Garbage

Lake

side

Total

distr

ibution

Num

bero

fsam

ples

exam

ined

2020

2025

1520

2010

150

Num

bero

fpositive

samples

611

913

711

95

71Distrib

ution(

)30

5545

5246

66

5545

504733

1Au

xarthron

conjugatum

(Kuehn

)OrrampKu

ehn

mdashmdash

1mdash

mdash1

mdash1

3200

2Ch

rysosporium

indicum

(Randh

awaamp

Sand

hu)G

arg

22

35

24

21

211400

3Ch

rysosporium

evolceanui

(Randh

awaamp

Sand

hu)G

arg

mdash1

1mdash

mdashmdash

11

4266

4Ch

rysosporium

tropicum

Carm

ichael

mdash1

12

mdash1

11

7466

5Ch

rysosporium

zonatum

Al-M

usallam

ampTan

mdash1

mdashmdash

mdash1

mdashmdash

213

3

6Ch

rysosporium

stateof

Ctenom

ycesserratus

Eidam

13

1mdash

mdashmdash

mdashmdash

5333

7Gy

mnoascella

dankalien

sis1

mdashmdash

mdashmdash

mdash1

mdash2

133

8Gy

mna

scellahyalinospora

(Kuehn

etal)Cu

rrah

mdashmdash

mdash1

mdashmdash

mdashmdash

1066

9Gy

mnoascoideusp

etalosporusOrrR

oyampGho

shmdash

mdashmdash

1mdash

mdashmdash

mdash1

066

10Microsporum

gypseum

(EB

odin)G

uiartamp

Grig

oraki

11

mdash3

33

21

1493

311

Trich

ophytonmentagrophytes(CPRo

bin)

Sabo

ur

mdashmdash

1mdash

11

mdashmdash

3200

12Trich

ophytonterrestre

DurieampFrey

1mdash

1mdash

1mdash

2mdash

5333

13Un

cinocarpu

squeensla

ndicu

s(Ap

inisampRe

es)S

igler

mdash2

mdash1

mdashmdash

mdashmdash

3200

Total

611

913

711

95

71

4 Journal of Mycology

Akola

Buldhana

Amravati NagpurWardha

Yawatmal ChandrapurWashim

Gadchiroli

GondhiaBhandara

Figure 2 Sites of collection of soil samples in Vidarbha region of Maharashtra

All thirteen strains yielded unique PCR amplificationThe sequences of the ITS1-58S-ITS2 rDNA region for thethirteen strains were from 527 bp to 631 bp Chrysosporiumstate of Ctenomyces serratus and Trichophyton mentagro-phytes were the smallest and the largest respectively Theother species showed a product size of approximately 600 bpThere was considerable difference in the sequence data of thethirteen strains analyzed The data were also compared withsequences deposited in the NCBIGenbank for identificationpurposes and a tree was constructed with the nearest typeof strain sequences based on rRNA gene sequences (ITSregion) using the Maximum Composite Likelihood Method(Figure 3) The Phylogenetic tree indicates different clus-ters for each isolate showing their sequence variation Thesequences obtained show greater than 96 similarity to thereference sequences available in NCBI Genbank database

Chrysosporium indicum (1400) was the most prevalentspecies and this is in agreement with the finding of previousworkers [17ndash20] Its high percentage of distribution clearlyindicates that it is well adapted to warmer condition of India[21]Microsporumgypseum complexwas foundnext toC ind-icum in distribution (933) and has been reported from vari-ous parts of IndiaWe also encounteredArthroderma sp threetimes in association with theMicrosporum gypseum complexwhichwasmade upof the two teleomorph statesArthrodermaincurvata and A gypsea but A fulva was altogether absentHowevermating experiments were not conducted to confirmits specific identity It was reported from Indian soils by Deyand Kakoti [22] It was further isolated from various partsof India [21 23ndash27] Chrysosporium tropicum was next toMgypseum comprising of 466 in distribution It is a cosmo-politan species and has been reported from various parts ofIndia [17 18 27 28]

The other species of Chrysosporium isolated were Chry-sosporium evolceanui (266) Chrysosporium zonatum(133) and Chrysosporium state of Ctenomyces serratus(333) Chrysosporium evolceanuiwas reported from Indiansoils as Trichophyton evolceanui by Randhawa and Sandhu[17] then Garg [21] placed it in the genus Chrysosporium asC evolceanui It is reported from Indian soils [26 29 30]Various workers have isolated Chrysosporium zonatum fromIndian soil [31 32] Chrysosporium state of Ctenomyces serra-tus was recorded in 333 of samples and this has beenreported from various parts of India [17ndash19 21]

Other species of keratinophilic fungi isolated wereGymnascella dankaliensis (133) Gymnascella hyalinospora(066) Gymnoascoideus petalosporus (066) Auxarth-ron conjugatum (200) and Uncinocarpus queenslandicus(200)G dankailensis is reported from Indian soils [29 33]Gymnascella hyalinospora was reported from Indian soils bySingh and Kushwaha [32] and Deshmukh [34] Gymnoascoi-deus petalosporus was previously recorded from Chilka Lakesoil [35] soils from Vedanthangal Water Bird Sanctuary [20]and soils of Orissa [33] Auxarthron conjugatum is reportedfrom Indian soils by Deshmukh and Verekar [20] Jain andAgrawal [36] andDeshmukh andAgrawal [37] Anamorphicstate of Uncinocarpus queenslandicus ie Chrysosporium que-enslandicumwas reported from Indian soil [18 24 26 38 39]

The other species of dermatophytes recovered were Tri-chophyton mentagrophytes (200) and T terrestre (333)Trichophyton mentagrophytes has been reported from Indiansoils [26 34 40ndash42] and is known to cause diseases in manand animals [43 44] T terrestre has been reported fromIndian soils by various workers [26 45ndash47]

The prevalence of these fungi in the soils of region ofVidarbha is of importance for their pathogenic potential

Journal of Mycology 5

AJ439446 C indicum

AJ005368 C evolceanui

AB219229 C zonatum

EF568044 C tropicum

C zonatum Vidarbha isolate

U queenslandicus

AB861842 U queenslandicus

T terrestre

EF631622 T terrestre

T mentagrophytes

HQ223449 T mentagrophytes

C serratus

AJ877222 C serratus

M gypseum

JQ390554 M gypseum

G dankaliensis

AY304514 G dankaliensis

G hyalinospora

HM991271 G hyalinospora

G petalosporus

HM991270 G petalosporus

100

100

100

100

100

100

100

100

100

100

98

99

84

92

46

98

80

68

46

63

64

000002004006008

C tropicum

C indicum Vidarbha isolate

C evolceanui Vidarbha isolate

HM036583 Auxarthron conjugatum

Auxarthron conjugatum

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Figure 3 Phylogenetic tree based on ITS1-58S-ITS4 region sequences for isolated 13 keratinophilic fungi with reference strains Numbers atthe respective nodes are percentage of 1000 bootstrap replicates Bar indicates genetic distance due to sequence variation

and has been confirmed in several investigations in differentparts of the world For example Chrysosporium zonatumwasreported to cause disseminated infection in a patient withchronic granulomatous disease [48] In Japan C zonatumstrains were isolated from bronchial lavage from a female inChiba and from a male in Kyushu Both patients presentedpulmonary cavity sites [49] Chrysosporium tropicum wasreported from comb lesion in two different breeds of chickenin India [50]There are reports of disseminated infections dueto C queenslandicum in garter snakes [51] Gymnascella dan-kaliensis was reported from superficial infections in humanbeings [52] and Iwen et al [53] isolatedGymnascella hyalinos-pora from invasive pulmonary infection in a patient with

acute myelogenous leukemia Similarly Lyskova [54] isolatedChrysosporium queenslandicum C sulfureum C tropicumMalbranchea pulchella and Myriodontium keratinophilumfrom infections of the skin and nails of patients in the Mora-vian-Silesian Region (Czech Republic)Thus these fungimaybe regarded as opportunistic pathogens

There are some reports of occurrence of keratinophilicfungi from various parts of Maharashtra [40 47 55 56]but to best of our knowledge this is the first comprehensivereport on incidence of keratinophilic fungi from Vidarbharegion These findings are in agreement with the findings ofprevious work on keratinophilic fungi It appears from thisstudy that a rich variety of keratinophilic fungal flora exists

6 Journal of Mycology

in Vidarbha region of Maharashtra which may be attributedto the climatic and environmental conditions such as the soiltype vegetation fauna and human habitations Garg et al[57] emphasized that the climate and perhaps other environ-mental factors are important in determining the distributionof keratinophilic fungi in ecological habitats

Our findings confirm the presence of keratinophilic andrelated dermatophytes in the soils of Vidarbha region Theseareas potentially have a high risk for causing cutaneous fungalinfections in humans and animals and could be considered asa source of these infections

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] S K Deshmukh and S A Verekar ldquoThe occurrence of dermato-phytes and other keratinophilic fungi from the soils of Hima-chal Pradesh (India)rdquo Czech Mycology vol 58 no 1-2 pp 117ndash124 2006

[2] M T Hedayati A Mohseni-Bandpi and S Moradi ldquoA surveyon the pathogenic fungi in soil samples of potted plants fromSari hospitals Iranrdquo Journal of Hospital Infection vol 58 no 1pp 59ndash62 2004

[3] R Vanbreuseghem ldquoTechnique biologique pour lisolement desdermatophytes du solrdquo Annales de la Societe Belge de MedecineTropicale vol 32 pp 173ndash178 1952

[4] S M Zaki Y Mikami A A Karam El-Din and Y A YoussefldquoKeratinophilic fungi recovered from muddy soil in Cairovicinities Egyptrdquo Mycopathologia vol 160 no 3 pp 245ndash2512005

[5] S K Deshmukh and S A Verekar ldquoKeratinophilic fungi fromthe vicinity of meteorite crater soils of Lonar (India)rdquo Myco-pathologia vol 162 no 4 pp 303ndash306 2006

[6] H C Gugnani S Sharma and K Wright ldquoA preliminary studyon the occurrence of keratinophilic fungi in soils of JamaicardquoRevista do Instituto de Medicina Tropical de Sao Paulo vol 56no 3 pp 231ndash234 2014

[7] K Pakshir M Rahimi Ghiasi K Zomorodian and A R Ghar-avi ldquoIsolation and molecular identification of keratinophilicfungi from public parks soil in Shiraz Iranrdquo BioMed ResearchInternational vol 2013 Article ID 619576 5 pages 2013

[8] L Sigler and J W Carmichael ldquoTaxonomy ofMalbranchea andsome other hyphomycetes with arthroconidiardquoMycotaxon vol4 pp 349ndash488 1976

[9] C A N Van Oorschot ldquoA revision of Chrysosporium and alliedgenerardquo Studies in Mycology vol 20 pp 1ndash89 1980

[10] R S Currah ldquoTaxonomy of the Onygenales ArthrodermaceaeGymnoascaceae Myxotrichaceae and Onygenaceaerdquo Myco-taxon vol 24 pp 1ndash216 1985

[11] J A von Arx ldquoThe ascomycetes genus Gymnoascusrdquo Persooniavol 13 pp 173ndash183 1986

[12] J Cano and J Gurrao ldquoThe genus Aphanoascusrdquo MycologicalResearch vol 94 pp 355ndash377 1990

[13] S B Lee and J W Taylor ldquoIsolation of DNA from fungalmycelium and single cellsrdquo in Protocols A Guide toMethods andApplications M A Innis H D Gelfand J J Sninsky and T

J White Eds pp 282ndash287 Academic Press San Diego CalifUSA 1990

[14] T J White T Bruns S Lee and J Taylor ldquoAmplification anddirect sequencing of fungal ribosomal RNA genes for phyloge-neticsrdquo in PCR Protocols A Guide to Methods and ApplicationsA Innis D H Gelfand J J Sninsky and T J White Eds pp315ndash322 Academic Press San Diego Calif USA 1990

[15] S F AltschulW GishWMiller EWMyers and D J LipmanldquoBasic local alignment search toolrdquo Journal ofMolecular Biologyvol 215 no 3 pp 403ndash410 1990

[16] K Tamura G Stecher D Peterson A Filipski and S KumarldquoMEGA6molecular evolutionary genetics analysis version 60rdquoMolecular Biology and Evolution vol 30 no 12 pp 2725ndash27292013

[17] H S Randhawa and R S Sandhu ldquoA survey of soil inhabit-ing dermatophytes and related keratinophilic fungi of IndiardquoSabouraudia Journal of Medical and Veterinary Mycology vol4 no 2 pp 71ndash79 1965

[18] S K Deshmukh and S C Agrawal ldquoPrevalence of dermato-phytes and other keratinophilic fungi in soils of MadhyaPradesh (India)rdquoMykosen vol 26 no 11 pp 574ndash577 1983

[19] S K Deshmukh and S A Verekar ldquoPrevalence of Keratinophil-ic fungi in ldquoUsarrdquo Soils of Uttar Pradesh Indiardquo MicrobiologyResearch vol 2 no 2 p e15 2011

[20] S K Deshmukh and S A Verekar ldquoIncidence of keratinophilicfungi from the soils of Vedanthangal Water Bird Sanctuary(India)rdquoMycoses vol 54 no 6 pp 487ndash490 2011

[21] A K Garg ldquoIsolation of dermatophytes and other keratinophil-ic fungi from soils in Indiardquo Sabouraudia Journal ofMedical andVeterinary Mycology vol 4 no 4 pp 259ndash264 1966

[22] N C Dey and L M Kakoti ldquoMicrosporum gypseum in IndiardquoJournal of the IndianMedical Association vol 25 no 5 pp 160ndash164 1955

[23] R K S Kushwaha and S C Agarwal ldquoSome keratinophilicfungi and related dermatophytes from soilsrdquo Proceedings of theIndian National Science Academy vol 42 no B pp 102ndash1101976

[24] C J Singh B G Singh and B S Singh ldquoKeratinophilic fungiof Ghana birds sanctuary Bharatpur (Rajasthan)rdquo Advances inPlant Sciences vol 7 pp 280ndash291 1994

[25] G M Vidyasagar N Hosmani and D Shivkumar ldquoKer-atinophilic fungi isolated from hospital dust and soils of publicplaces at Gulbarga Indiardquo Mycopathologia vol 159 no 1 pp13ndash21 2005

[26] I Singh A Mishra and R K S Kushwaha ldquoDermatophytesrelated keratinophilic and opportunistic fungi in indoor dust ofhouses and hospitalsrdquo Indian Journal of Medical Microbiologyvol 27 no 3 pp 242ndash246 2009

[27] N Jain and M Sharma ldquoDistribution of dermatophytes andother related fungi in Jaipur city with particular reference tosoil pHrdquoMycoses vol 54 no 1 pp 52ndash58 2011

[28] JW Carmichael ldquoChrysosporium and some other aleuriosporichyphomycetesrdquo Canadian Journal of Botany vol 40 pp 1137ndash1173 1962

[29] S A Verekar and S K Deshmukh ldquoIncidence of keratinophilicfungi from caves around Mumbai Maharastra (India)rdquo Journalof Basic and Applied Mycology vol 5 pp 62ndash64 2006

[30] I Singh R K S Kushwaha andP Parihar ldquoKeratinophilic fungiin soil of potted plants of indoor environments inKanpur Indiaand their proteolytic abilityrdquoMycoscience vol 50 no 4 pp 303ndash307 2009

Journal of Mycology 7

[31] S Katiyar and R K S Kushwaha ldquoHuman hair colonizing fungiin water sediments of IndiardquoMycopathologia vol 152 no 2 pp81ndash84 2001

[32] I Singh and R K S Kushwaha ldquoDermatophytes and relatedkeratinophilic fungi in soil of parks and agricultural fields ofUttar Pradesh Indiardquo Indian Journal of Dermatology vol 55 no3 pp 306ndash308 2010

[33] B Sur and G R Ghosh ldquoKeratinophilic fungi from OrissaIndia I isolation from soilsrdquo Sabouraudia Journal ofMedical andVeterinary Mycology vol 18 no 4 pp 269ndash274 1980

[34] S K Deshmukh ldquoIncidence of keratinophilic fungi fromselected soils of Kerala state (India)rdquo Mycopathologia vol 156no 3 pp 177ndash181 2003

[35] G R Ghosh and S Bhatt ldquoKeratinophilic Fungi from ChilkaLake-side Soil Orissa (India)rdquo Indian Journal of Microbiologyvol 40 no 4 pp 247ndash254 2000

[36] P C Jain and S C Agrawal ldquoSome additions to IndianMalbrancheardquo Kavaka vol 7 pp 69ndash72 1979

[37] S K Deshmukh and S C Agrawal ldquoIsolation of dermatophytesand other keratinophilic fungi from soils of Jammu IndiardquoMycoses vol 46 no 5-6 pp 226ndash228 2003

[38] S Kaul and G Sumbali ldquoKeratinolysis by poultry farm soilfungirdquoMycopathologia vol 139 no 3 pp 137ndash140 1997

[39] P Saxena A Kumar and J N Shrivastava ldquoDiversity ofkeratinophilic mycoflora in the soil of Agra (India)rdquo FoliaMicrobiologica vol 49 no 4 pp 430ndash434 2004

[40] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from the vicinity of salt pan soils of MumbaiIndiardquoMycopathologia vol 157 no 3 pp 265ndash267 2004

[41] H C Gugnani A Paliwal-Joshi H Rahman et al ldquoOccurrenceof pathogenic fungi in soil of burrows of rats and of other sitesin bamboo plantations in India and NepalrdquoMycoses vol 50 no6 pp 507ndash511 2007

[42] M Sharma and M Sharma ldquoIncidence of dermatophytes andother keratinophilic fungi in the schools and college playgroundsoils of Jaipur Indiardquo African Journal of Microbiology Researchvol 4 no 24 pp 2647ndash2654 2010

[43] L N Mohapatra H C Gugnani and K Shivrajan ldquoNaturalinfection in laboratory animals due to Trichophyton mentagro-phytes in IndiardquoMycopathologia et Mycologia Applicata vol 24no 3 pp 275ndash280 1964

[44] C A Oyeka ldquoTrichophyton mentagrophytes a keratinophilicfungusrdquo in Biology of Dermatophytes and other KeratinophilicFungi R K S Kushwaha and J Guarro Eds pp 60ndash65 RevistaIberoamericana de Micologia Bilbao Spain 2000

[45] T N Verma B K Sinha and U L Das ldquoIsolation of ker-atinophilic fungi from soil in Bihar (India)rdquo Mykosen vol 25no 8 pp 449ndash452 1982

[46] S K Deshmukh ldquoIncidence of dermatophytes and other ker-atinophilic fungi in the glacier bank soils of the Kashmir valleyIndiardquoMycologist vol 16 no 4 pp 165ndash167 2002

[47] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from Karnala bird sanctuary Maharashtra(India)rdquo Journal of Basic and Applied Mycology vol 1 no 2 pp194ndash196 2002

[48] E Roilides L Sigler E Bibashi H Katsifa N Flaris andC Panteliadis ldquoDisseminated infection due to Chrysosporiumzonatum in a patient with chronic granulomatous disease andreview of non-aspergillus fungal infections in patients with thisdiseaserdquo Journal of ClinicalMicrobiology vol 37 no 1 pp 18ndash251999

[49] L Sigler A L Flis and JW Carmichael ldquoThe genusUncinocar-pus (Onygenaceae) and its synonym Brunneospora new con-cepts combinations and connections to anamorphs in Chrysos-porium and further evidence of relationship with Coccidioidesimmitisrdquo Canadian Journal of Botany vol 76 no 9 pp 1624ndash1636 1998

[50] S A Saidi S Bhatt J L Richard A Sikdar and G R GhoshldquoChrysosporium tropicum as a probable cause of mycosis ofpoultry in Indiardquo Mycopathologia vol 125 no 3 pp 143ndash1471994

[51] T Vissiennon K F Schuppel E Ullrich and A F KuijpersldquoCase report A disseminated infection due to Chrysosporiumqueenslandicum in a garter snake (Thamnophis)rdquoMycoses vol42 no 1-2 pp 107ndash110 1999

[52] G S de Hoog and J Guarro Atlas of Clinical Fungi Centraal-bureau voor Schimmelcultures Baarn The Netherlands 1995

[53] P C Iwen L Sigler S Tarantolo et al ldquoPulmonary infectioncaused by Gymnascella hyalinospora in a patient with acutemyelogenous leukemiardquo Journal of Clinical Microbiology vol38 no 1 pp 375ndash381 2000

[54] P Lyskova ldquoSaprotrophicmicroscopic fungi and dermatophytesaccompanying infections of the skin and nails of patients in theMoravian-Silesian Region (Czech Republic)rdquo Czech Mycologyvol 59 pp 125ndash137 2007

[55] A A Padhye S PMisra andM JThirumalachar ldquoOccurrenceof soil inhabiting dermatophytes and other keratinophilic fungifrom soils in Poonardquo Hindustan Antibiotics Bulletin vol 9 no2 pp 90ndash93 1966

[56] A A Padhye V H Pawar R S Sukapure and M J Thiru-malachar ldquoKeratinophilic fungi from marine soils of BombayIndia Irdquo Hindustan Antibiotics Bulletin vol 10 no 2 pp 138ndash141 1967

[57] A P Garg S Gandotra K G Mukerji and G J F Pugh ldquoEcol-ogy of keratinophilic fungirdquo Proceedings Plant Sciences vol 94no 2-3 pp 149ndash163 1985

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Page 3: Research Article Incidence of Keratinophilic Fungi from ...downloads.hindawi.com/archive/2014/148970.pdf · respectively, as described by White et al. [ ]. Ampli cation was performed

Journal of Mycology 3

Table2Distrib

utionof

keratin

ophilic

fung

iindifferent

typeso

fsoilsof

Vidarbha

region

ofMaharashtra

Source

ofsoilsamples

Forest

land

Cultivated

land

Road

side

Public

gardens

Poultry

farm

Cattle

farm

Garbage

Lake

side

Total

distr

ibution

Num

bero

fsam

ples

exam

ined

2020

2025

1520

2010

150

Num

bero

fpositive

samples

611

913

711

95

71Distrib

ution(

)30

5545

5246

66

5545

504733

1Au

xarthron

conjugatum

(Kuehn

)OrrampKu

ehn

mdashmdash

1mdash

mdash1

mdash1

3200

2Ch

rysosporium

indicum

(Randh

awaamp

Sand

hu)G

arg

22

35

24

21

211400

3Ch

rysosporium

evolceanui

(Randh

awaamp

Sand

hu)G

arg

mdash1

1mdash

mdashmdash

11

4266

4Ch

rysosporium

tropicum

Carm

ichael

mdash1

12

mdash1

11

7466

5Ch

rysosporium

zonatum

Al-M

usallam

ampTan

mdash1

mdashmdash

mdash1

mdashmdash

213

3

6Ch

rysosporium

stateof

Ctenom

ycesserratus

Eidam

13

1mdash

mdashmdash

mdashmdash

5333

7Gy

mnoascella

dankalien

sis1

mdashmdash

mdashmdash

mdash1

mdash2

133

8Gy

mna

scellahyalinospora

(Kuehn

etal)Cu

rrah

mdashmdash

mdash1

mdashmdash

mdashmdash

1066

9Gy

mnoascoideusp

etalosporusOrrR

oyampGho

shmdash

mdashmdash

1mdash

mdashmdash

mdash1

066

10Microsporum

gypseum

(EB

odin)G

uiartamp

Grig

oraki

11

mdash3

33

21

1493

311

Trich

ophytonmentagrophytes(CPRo

bin)

Sabo

ur

mdashmdash

1mdash

11

mdashmdash

3200

12Trich

ophytonterrestre

DurieampFrey

1mdash

1mdash

1mdash

2mdash

5333

13Un

cinocarpu

squeensla

ndicu

s(Ap

inisampRe

es)S

igler

mdash2

mdash1

mdashmdash

mdashmdash

3200

Total

611

913

711

95

71

4 Journal of Mycology

Akola

Buldhana

Amravati NagpurWardha

Yawatmal ChandrapurWashim

Gadchiroli

GondhiaBhandara

Figure 2 Sites of collection of soil samples in Vidarbha region of Maharashtra

All thirteen strains yielded unique PCR amplificationThe sequences of the ITS1-58S-ITS2 rDNA region for thethirteen strains were from 527 bp to 631 bp Chrysosporiumstate of Ctenomyces serratus and Trichophyton mentagro-phytes were the smallest and the largest respectively Theother species showed a product size of approximately 600 bpThere was considerable difference in the sequence data of thethirteen strains analyzed The data were also compared withsequences deposited in the NCBIGenbank for identificationpurposes and a tree was constructed with the nearest typeof strain sequences based on rRNA gene sequences (ITSregion) using the Maximum Composite Likelihood Method(Figure 3) The Phylogenetic tree indicates different clus-ters for each isolate showing their sequence variation Thesequences obtained show greater than 96 similarity to thereference sequences available in NCBI Genbank database

Chrysosporium indicum (1400) was the most prevalentspecies and this is in agreement with the finding of previousworkers [17ndash20] Its high percentage of distribution clearlyindicates that it is well adapted to warmer condition of India[21]Microsporumgypseum complexwas foundnext toC ind-icum in distribution (933) and has been reported from vari-ous parts of IndiaWe also encounteredArthroderma sp threetimes in association with theMicrosporum gypseum complexwhichwasmade upof the two teleomorph statesArthrodermaincurvata and A gypsea but A fulva was altogether absentHowevermating experiments were not conducted to confirmits specific identity It was reported from Indian soils by Deyand Kakoti [22] It was further isolated from various partsof India [21 23ndash27] Chrysosporium tropicum was next toMgypseum comprising of 466 in distribution It is a cosmo-politan species and has been reported from various parts ofIndia [17 18 27 28]

The other species of Chrysosporium isolated were Chry-sosporium evolceanui (266) Chrysosporium zonatum(133) and Chrysosporium state of Ctenomyces serratus(333) Chrysosporium evolceanuiwas reported from Indiansoils as Trichophyton evolceanui by Randhawa and Sandhu[17] then Garg [21] placed it in the genus Chrysosporium asC evolceanui It is reported from Indian soils [26 29 30]Various workers have isolated Chrysosporium zonatum fromIndian soil [31 32] Chrysosporium state of Ctenomyces serra-tus was recorded in 333 of samples and this has beenreported from various parts of India [17ndash19 21]

Other species of keratinophilic fungi isolated wereGymnascella dankaliensis (133) Gymnascella hyalinospora(066) Gymnoascoideus petalosporus (066) Auxarth-ron conjugatum (200) and Uncinocarpus queenslandicus(200)G dankailensis is reported from Indian soils [29 33]Gymnascella hyalinospora was reported from Indian soils bySingh and Kushwaha [32] and Deshmukh [34] Gymnoascoi-deus petalosporus was previously recorded from Chilka Lakesoil [35] soils from Vedanthangal Water Bird Sanctuary [20]and soils of Orissa [33] Auxarthron conjugatum is reportedfrom Indian soils by Deshmukh and Verekar [20] Jain andAgrawal [36] andDeshmukh andAgrawal [37] Anamorphicstate of Uncinocarpus queenslandicus ie Chrysosporium que-enslandicumwas reported from Indian soil [18 24 26 38 39]

The other species of dermatophytes recovered were Tri-chophyton mentagrophytes (200) and T terrestre (333)Trichophyton mentagrophytes has been reported from Indiansoils [26 34 40ndash42] and is known to cause diseases in manand animals [43 44] T terrestre has been reported fromIndian soils by various workers [26 45ndash47]

The prevalence of these fungi in the soils of region ofVidarbha is of importance for their pathogenic potential

Journal of Mycology 5

AJ439446 C indicum

AJ005368 C evolceanui

AB219229 C zonatum

EF568044 C tropicum

C zonatum Vidarbha isolate

U queenslandicus

AB861842 U queenslandicus

T terrestre

EF631622 T terrestre

T mentagrophytes

HQ223449 T mentagrophytes

C serratus

AJ877222 C serratus

M gypseum

JQ390554 M gypseum

G dankaliensis

AY304514 G dankaliensis

G hyalinospora

HM991271 G hyalinospora

G petalosporus

HM991270 G petalosporus

100

100

100

100

100

100

100

100

100

100

98

99

84

92

46

98

80

68

46

63

64

000002004006008

C tropicum

C indicum Vidarbha isolate

C evolceanui Vidarbha isolate

HM036583 Auxarthron conjugatum

Auxarthron conjugatum

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Figure 3 Phylogenetic tree based on ITS1-58S-ITS4 region sequences for isolated 13 keratinophilic fungi with reference strains Numbers atthe respective nodes are percentage of 1000 bootstrap replicates Bar indicates genetic distance due to sequence variation

and has been confirmed in several investigations in differentparts of the world For example Chrysosporium zonatumwasreported to cause disseminated infection in a patient withchronic granulomatous disease [48] In Japan C zonatumstrains were isolated from bronchial lavage from a female inChiba and from a male in Kyushu Both patients presentedpulmonary cavity sites [49] Chrysosporium tropicum wasreported from comb lesion in two different breeds of chickenin India [50]There are reports of disseminated infections dueto C queenslandicum in garter snakes [51] Gymnascella dan-kaliensis was reported from superficial infections in humanbeings [52] and Iwen et al [53] isolatedGymnascella hyalinos-pora from invasive pulmonary infection in a patient with

acute myelogenous leukemia Similarly Lyskova [54] isolatedChrysosporium queenslandicum C sulfureum C tropicumMalbranchea pulchella and Myriodontium keratinophilumfrom infections of the skin and nails of patients in the Mora-vian-Silesian Region (Czech Republic)Thus these fungimaybe regarded as opportunistic pathogens

There are some reports of occurrence of keratinophilicfungi from various parts of Maharashtra [40 47 55 56]but to best of our knowledge this is the first comprehensivereport on incidence of keratinophilic fungi from Vidarbharegion These findings are in agreement with the findings ofprevious work on keratinophilic fungi It appears from thisstudy that a rich variety of keratinophilic fungal flora exists

6 Journal of Mycology

in Vidarbha region of Maharashtra which may be attributedto the climatic and environmental conditions such as the soiltype vegetation fauna and human habitations Garg et al[57] emphasized that the climate and perhaps other environ-mental factors are important in determining the distributionof keratinophilic fungi in ecological habitats

Our findings confirm the presence of keratinophilic andrelated dermatophytes in the soils of Vidarbha region Theseareas potentially have a high risk for causing cutaneous fungalinfections in humans and animals and could be considered asa source of these infections

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] S K Deshmukh and S A Verekar ldquoThe occurrence of dermato-phytes and other keratinophilic fungi from the soils of Hima-chal Pradesh (India)rdquo Czech Mycology vol 58 no 1-2 pp 117ndash124 2006

[2] M T Hedayati A Mohseni-Bandpi and S Moradi ldquoA surveyon the pathogenic fungi in soil samples of potted plants fromSari hospitals Iranrdquo Journal of Hospital Infection vol 58 no 1pp 59ndash62 2004

[3] R Vanbreuseghem ldquoTechnique biologique pour lisolement desdermatophytes du solrdquo Annales de la Societe Belge de MedecineTropicale vol 32 pp 173ndash178 1952

[4] S M Zaki Y Mikami A A Karam El-Din and Y A YoussefldquoKeratinophilic fungi recovered from muddy soil in Cairovicinities Egyptrdquo Mycopathologia vol 160 no 3 pp 245ndash2512005

[5] S K Deshmukh and S A Verekar ldquoKeratinophilic fungi fromthe vicinity of meteorite crater soils of Lonar (India)rdquo Myco-pathologia vol 162 no 4 pp 303ndash306 2006

[6] H C Gugnani S Sharma and K Wright ldquoA preliminary studyon the occurrence of keratinophilic fungi in soils of JamaicardquoRevista do Instituto de Medicina Tropical de Sao Paulo vol 56no 3 pp 231ndash234 2014

[7] K Pakshir M Rahimi Ghiasi K Zomorodian and A R Ghar-avi ldquoIsolation and molecular identification of keratinophilicfungi from public parks soil in Shiraz Iranrdquo BioMed ResearchInternational vol 2013 Article ID 619576 5 pages 2013

[8] L Sigler and J W Carmichael ldquoTaxonomy ofMalbranchea andsome other hyphomycetes with arthroconidiardquoMycotaxon vol4 pp 349ndash488 1976

[9] C A N Van Oorschot ldquoA revision of Chrysosporium and alliedgenerardquo Studies in Mycology vol 20 pp 1ndash89 1980

[10] R S Currah ldquoTaxonomy of the Onygenales ArthrodermaceaeGymnoascaceae Myxotrichaceae and Onygenaceaerdquo Myco-taxon vol 24 pp 1ndash216 1985

[11] J A von Arx ldquoThe ascomycetes genus Gymnoascusrdquo Persooniavol 13 pp 173ndash183 1986

[12] J Cano and J Gurrao ldquoThe genus Aphanoascusrdquo MycologicalResearch vol 94 pp 355ndash377 1990

[13] S B Lee and J W Taylor ldquoIsolation of DNA from fungalmycelium and single cellsrdquo in Protocols A Guide toMethods andApplications M A Innis H D Gelfand J J Sninsky and T

J White Eds pp 282ndash287 Academic Press San Diego CalifUSA 1990

[14] T J White T Bruns S Lee and J Taylor ldquoAmplification anddirect sequencing of fungal ribosomal RNA genes for phyloge-neticsrdquo in PCR Protocols A Guide to Methods and ApplicationsA Innis D H Gelfand J J Sninsky and T J White Eds pp315ndash322 Academic Press San Diego Calif USA 1990

[15] S F AltschulW GishWMiller EWMyers and D J LipmanldquoBasic local alignment search toolrdquo Journal ofMolecular Biologyvol 215 no 3 pp 403ndash410 1990

[16] K Tamura G Stecher D Peterson A Filipski and S KumarldquoMEGA6molecular evolutionary genetics analysis version 60rdquoMolecular Biology and Evolution vol 30 no 12 pp 2725ndash27292013

[17] H S Randhawa and R S Sandhu ldquoA survey of soil inhabit-ing dermatophytes and related keratinophilic fungi of IndiardquoSabouraudia Journal of Medical and Veterinary Mycology vol4 no 2 pp 71ndash79 1965

[18] S K Deshmukh and S C Agrawal ldquoPrevalence of dermato-phytes and other keratinophilic fungi in soils of MadhyaPradesh (India)rdquoMykosen vol 26 no 11 pp 574ndash577 1983

[19] S K Deshmukh and S A Verekar ldquoPrevalence of Keratinophil-ic fungi in ldquoUsarrdquo Soils of Uttar Pradesh Indiardquo MicrobiologyResearch vol 2 no 2 p e15 2011

[20] S K Deshmukh and S A Verekar ldquoIncidence of keratinophilicfungi from the soils of Vedanthangal Water Bird Sanctuary(India)rdquoMycoses vol 54 no 6 pp 487ndash490 2011

[21] A K Garg ldquoIsolation of dermatophytes and other keratinophil-ic fungi from soils in Indiardquo Sabouraudia Journal ofMedical andVeterinary Mycology vol 4 no 4 pp 259ndash264 1966

[22] N C Dey and L M Kakoti ldquoMicrosporum gypseum in IndiardquoJournal of the IndianMedical Association vol 25 no 5 pp 160ndash164 1955

[23] R K S Kushwaha and S C Agarwal ldquoSome keratinophilicfungi and related dermatophytes from soilsrdquo Proceedings of theIndian National Science Academy vol 42 no B pp 102ndash1101976

[24] C J Singh B G Singh and B S Singh ldquoKeratinophilic fungiof Ghana birds sanctuary Bharatpur (Rajasthan)rdquo Advances inPlant Sciences vol 7 pp 280ndash291 1994

[25] G M Vidyasagar N Hosmani and D Shivkumar ldquoKer-atinophilic fungi isolated from hospital dust and soils of publicplaces at Gulbarga Indiardquo Mycopathologia vol 159 no 1 pp13ndash21 2005

[26] I Singh A Mishra and R K S Kushwaha ldquoDermatophytesrelated keratinophilic and opportunistic fungi in indoor dust ofhouses and hospitalsrdquo Indian Journal of Medical Microbiologyvol 27 no 3 pp 242ndash246 2009

[27] N Jain and M Sharma ldquoDistribution of dermatophytes andother related fungi in Jaipur city with particular reference tosoil pHrdquoMycoses vol 54 no 1 pp 52ndash58 2011

[28] JW Carmichael ldquoChrysosporium and some other aleuriosporichyphomycetesrdquo Canadian Journal of Botany vol 40 pp 1137ndash1173 1962

[29] S A Verekar and S K Deshmukh ldquoIncidence of keratinophilicfungi from caves around Mumbai Maharastra (India)rdquo Journalof Basic and Applied Mycology vol 5 pp 62ndash64 2006

[30] I Singh R K S Kushwaha andP Parihar ldquoKeratinophilic fungiin soil of potted plants of indoor environments inKanpur Indiaand their proteolytic abilityrdquoMycoscience vol 50 no 4 pp 303ndash307 2009

Journal of Mycology 7

[31] S Katiyar and R K S Kushwaha ldquoHuman hair colonizing fungiin water sediments of IndiardquoMycopathologia vol 152 no 2 pp81ndash84 2001

[32] I Singh and R K S Kushwaha ldquoDermatophytes and relatedkeratinophilic fungi in soil of parks and agricultural fields ofUttar Pradesh Indiardquo Indian Journal of Dermatology vol 55 no3 pp 306ndash308 2010

[33] B Sur and G R Ghosh ldquoKeratinophilic fungi from OrissaIndia I isolation from soilsrdquo Sabouraudia Journal ofMedical andVeterinary Mycology vol 18 no 4 pp 269ndash274 1980

[34] S K Deshmukh ldquoIncidence of keratinophilic fungi fromselected soils of Kerala state (India)rdquo Mycopathologia vol 156no 3 pp 177ndash181 2003

[35] G R Ghosh and S Bhatt ldquoKeratinophilic Fungi from ChilkaLake-side Soil Orissa (India)rdquo Indian Journal of Microbiologyvol 40 no 4 pp 247ndash254 2000

[36] P C Jain and S C Agrawal ldquoSome additions to IndianMalbrancheardquo Kavaka vol 7 pp 69ndash72 1979

[37] S K Deshmukh and S C Agrawal ldquoIsolation of dermatophytesand other keratinophilic fungi from soils of Jammu IndiardquoMycoses vol 46 no 5-6 pp 226ndash228 2003

[38] S Kaul and G Sumbali ldquoKeratinolysis by poultry farm soilfungirdquoMycopathologia vol 139 no 3 pp 137ndash140 1997

[39] P Saxena A Kumar and J N Shrivastava ldquoDiversity ofkeratinophilic mycoflora in the soil of Agra (India)rdquo FoliaMicrobiologica vol 49 no 4 pp 430ndash434 2004

[40] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from the vicinity of salt pan soils of MumbaiIndiardquoMycopathologia vol 157 no 3 pp 265ndash267 2004

[41] H C Gugnani A Paliwal-Joshi H Rahman et al ldquoOccurrenceof pathogenic fungi in soil of burrows of rats and of other sitesin bamboo plantations in India and NepalrdquoMycoses vol 50 no6 pp 507ndash511 2007

[42] M Sharma and M Sharma ldquoIncidence of dermatophytes andother keratinophilic fungi in the schools and college playgroundsoils of Jaipur Indiardquo African Journal of Microbiology Researchvol 4 no 24 pp 2647ndash2654 2010

[43] L N Mohapatra H C Gugnani and K Shivrajan ldquoNaturalinfection in laboratory animals due to Trichophyton mentagro-phytes in IndiardquoMycopathologia et Mycologia Applicata vol 24no 3 pp 275ndash280 1964

[44] C A Oyeka ldquoTrichophyton mentagrophytes a keratinophilicfungusrdquo in Biology of Dermatophytes and other KeratinophilicFungi R K S Kushwaha and J Guarro Eds pp 60ndash65 RevistaIberoamericana de Micologia Bilbao Spain 2000

[45] T N Verma B K Sinha and U L Das ldquoIsolation of ker-atinophilic fungi from soil in Bihar (India)rdquo Mykosen vol 25no 8 pp 449ndash452 1982

[46] S K Deshmukh ldquoIncidence of dermatophytes and other ker-atinophilic fungi in the glacier bank soils of the Kashmir valleyIndiardquoMycologist vol 16 no 4 pp 165ndash167 2002

[47] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from Karnala bird sanctuary Maharashtra(India)rdquo Journal of Basic and Applied Mycology vol 1 no 2 pp194ndash196 2002

[48] E Roilides L Sigler E Bibashi H Katsifa N Flaris andC Panteliadis ldquoDisseminated infection due to Chrysosporiumzonatum in a patient with chronic granulomatous disease andreview of non-aspergillus fungal infections in patients with thisdiseaserdquo Journal of ClinicalMicrobiology vol 37 no 1 pp 18ndash251999

[49] L Sigler A L Flis and JW Carmichael ldquoThe genusUncinocar-pus (Onygenaceae) and its synonym Brunneospora new con-cepts combinations and connections to anamorphs in Chrysos-porium and further evidence of relationship with Coccidioidesimmitisrdquo Canadian Journal of Botany vol 76 no 9 pp 1624ndash1636 1998

[50] S A Saidi S Bhatt J L Richard A Sikdar and G R GhoshldquoChrysosporium tropicum as a probable cause of mycosis ofpoultry in Indiardquo Mycopathologia vol 125 no 3 pp 143ndash1471994

[51] T Vissiennon K F Schuppel E Ullrich and A F KuijpersldquoCase report A disseminated infection due to Chrysosporiumqueenslandicum in a garter snake (Thamnophis)rdquoMycoses vol42 no 1-2 pp 107ndash110 1999

[52] G S de Hoog and J Guarro Atlas of Clinical Fungi Centraal-bureau voor Schimmelcultures Baarn The Netherlands 1995

[53] P C Iwen L Sigler S Tarantolo et al ldquoPulmonary infectioncaused by Gymnascella hyalinospora in a patient with acutemyelogenous leukemiardquo Journal of Clinical Microbiology vol38 no 1 pp 375ndash381 2000

[54] P Lyskova ldquoSaprotrophicmicroscopic fungi and dermatophytesaccompanying infections of the skin and nails of patients in theMoravian-Silesian Region (Czech Republic)rdquo Czech Mycologyvol 59 pp 125ndash137 2007

[55] A A Padhye S PMisra andM JThirumalachar ldquoOccurrenceof soil inhabiting dermatophytes and other keratinophilic fungifrom soils in Poonardquo Hindustan Antibiotics Bulletin vol 9 no2 pp 90ndash93 1966

[56] A A Padhye V H Pawar R S Sukapure and M J Thiru-malachar ldquoKeratinophilic fungi from marine soils of BombayIndia Irdquo Hindustan Antibiotics Bulletin vol 10 no 2 pp 138ndash141 1967

[57] A P Garg S Gandotra K G Mukerji and G J F Pugh ldquoEcol-ogy of keratinophilic fungirdquo Proceedings Plant Sciences vol 94no 2-3 pp 149ndash163 1985

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Page 4: Research Article Incidence of Keratinophilic Fungi from ...downloads.hindawi.com/archive/2014/148970.pdf · respectively, as described by White et al. [ ]. Ampli cation was performed

4 Journal of Mycology

Akola

Buldhana

Amravati NagpurWardha

Yawatmal ChandrapurWashim

Gadchiroli

GondhiaBhandara

Figure 2 Sites of collection of soil samples in Vidarbha region of Maharashtra

All thirteen strains yielded unique PCR amplificationThe sequences of the ITS1-58S-ITS2 rDNA region for thethirteen strains were from 527 bp to 631 bp Chrysosporiumstate of Ctenomyces serratus and Trichophyton mentagro-phytes were the smallest and the largest respectively Theother species showed a product size of approximately 600 bpThere was considerable difference in the sequence data of thethirteen strains analyzed The data were also compared withsequences deposited in the NCBIGenbank for identificationpurposes and a tree was constructed with the nearest typeof strain sequences based on rRNA gene sequences (ITSregion) using the Maximum Composite Likelihood Method(Figure 3) The Phylogenetic tree indicates different clus-ters for each isolate showing their sequence variation Thesequences obtained show greater than 96 similarity to thereference sequences available in NCBI Genbank database

Chrysosporium indicum (1400) was the most prevalentspecies and this is in agreement with the finding of previousworkers [17ndash20] Its high percentage of distribution clearlyindicates that it is well adapted to warmer condition of India[21]Microsporumgypseum complexwas foundnext toC ind-icum in distribution (933) and has been reported from vari-ous parts of IndiaWe also encounteredArthroderma sp threetimes in association with theMicrosporum gypseum complexwhichwasmade upof the two teleomorph statesArthrodermaincurvata and A gypsea but A fulva was altogether absentHowevermating experiments were not conducted to confirmits specific identity It was reported from Indian soils by Deyand Kakoti [22] It was further isolated from various partsof India [21 23ndash27] Chrysosporium tropicum was next toMgypseum comprising of 466 in distribution It is a cosmo-politan species and has been reported from various parts ofIndia [17 18 27 28]

The other species of Chrysosporium isolated were Chry-sosporium evolceanui (266) Chrysosporium zonatum(133) and Chrysosporium state of Ctenomyces serratus(333) Chrysosporium evolceanuiwas reported from Indiansoils as Trichophyton evolceanui by Randhawa and Sandhu[17] then Garg [21] placed it in the genus Chrysosporium asC evolceanui It is reported from Indian soils [26 29 30]Various workers have isolated Chrysosporium zonatum fromIndian soil [31 32] Chrysosporium state of Ctenomyces serra-tus was recorded in 333 of samples and this has beenreported from various parts of India [17ndash19 21]

Other species of keratinophilic fungi isolated wereGymnascella dankaliensis (133) Gymnascella hyalinospora(066) Gymnoascoideus petalosporus (066) Auxarth-ron conjugatum (200) and Uncinocarpus queenslandicus(200)G dankailensis is reported from Indian soils [29 33]Gymnascella hyalinospora was reported from Indian soils bySingh and Kushwaha [32] and Deshmukh [34] Gymnoascoi-deus petalosporus was previously recorded from Chilka Lakesoil [35] soils from Vedanthangal Water Bird Sanctuary [20]and soils of Orissa [33] Auxarthron conjugatum is reportedfrom Indian soils by Deshmukh and Verekar [20] Jain andAgrawal [36] andDeshmukh andAgrawal [37] Anamorphicstate of Uncinocarpus queenslandicus ie Chrysosporium que-enslandicumwas reported from Indian soil [18 24 26 38 39]

The other species of dermatophytes recovered were Tri-chophyton mentagrophytes (200) and T terrestre (333)Trichophyton mentagrophytes has been reported from Indiansoils [26 34 40ndash42] and is known to cause diseases in manand animals [43 44] T terrestre has been reported fromIndian soils by various workers [26 45ndash47]

The prevalence of these fungi in the soils of region ofVidarbha is of importance for their pathogenic potential

Journal of Mycology 5

AJ439446 C indicum

AJ005368 C evolceanui

AB219229 C zonatum

EF568044 C tropicum

C zonatum Vidarbha isolate

U queenslandicus

AB861842 U queenslandicus

T terrestre

EF631622 T terrestre

T mentagrophytes

HQ223449 T mentagrophytes

C serratus

AJ877222 C serratus

M gypseum

JQ390554 M gypseum

G dankaliensis

AY304514 G dankaliensis

G hyalinospora

HM991271 G hyalinospora

G petalosporus

HM991270 G petalosporus

100

100

100

100

100

100

100

100

100

100

98

99

84

92

46

98

80

68

46

63

64

000002004006008

C tropicum

C indicum Vidarbha isolate

C evolceanui Vidarbha isolate

HM036583 Auxarthron conjugatum

Auxarthron conjugatum

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Figure 3 Phylogenetic tree based on ITS1-58S-ITS4 region sequences for isolated 13 keratinophilic fungi with reference strains Numbers atthe respective nodes are percentage of 1000 bootstrap replicates Bar indicates genetic distance due to sequence variation

and has been confirmed in several investigations in differentparts of the world For example Chrysosporium zonatumwasreported to cause disseminated infection in a patient withchronic granulomatous disease [48] In Japan C zonatumstrains were isolated from bronchial lavage from a female inChiba and from a male in Kyushu Both patients presentedpulmonary cavity sites [49] Chrysosporium tropicum wasreported from comb lesion in two different breeds of chickenin India [50]There are reports of disseminated infections dueto C queenslandicum in garter snakes [51] Gymnascella dan-kaliensis was reported from superficial infections in humanbeings [52] and Iwen et al [53] isolatedGymnascella hyalinos-pora from invasive pulmonary infection in a patient with

acute myelogenous leukemia Similarly Lyskova [54] isolatedChrysosporium queenslandicum C sulfureum C tropicumMalbranchea pulchella and Myriodontium keratinophilumfrom infections of the skin and nails of patients in the Mora-vian-Silesian Region (Czech Republic)Thus these fungimaybe regarded as opportunistic pathogens

There are some reports of occurrence of keratinophilicfungi from various parts of Maharashtra [40 47 55 56]but to best of our knowledge this is the first comprehensivereport on incidence of keratinophilic fungi from Vidarbharegion These findings are in agreement with the findings ofprevious work on keratinophilic fungi It appears from thisstudy that a rich variety of keratinophilic fungal flora exists

6 Journal of Mycology

in Vidarbha region of Maharashtra which may be attributedto the climatic and environmental conditions such as the soiltype vegetation fauna and human habitations Garg et al[57] emphasized that the climate and perhaps other environ-mental factors are important in determining the distributionof keratinophilic fungi in ecological habitats

Our findings confirm the presence of keratinophilic andrelated dermatophytes in the soils of Vidarbha region Theseareas potentially have a high risk for causing cutaneous fungalinfections in humans and animals and could be considered asa source of these infections

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] S K Deshmukh and S A Verekar ldquoThe occurrence of dermato-phytes and other keratinophilic fungi from the soils of Hima-chal Pradesh (India)rdquo Czech Mycology vol 58 no 1-2 pp 117ndash124 2006

[2] M T Hedayati A Mohseni-Bandpi and S Moradi ldquoA surveyon the pathogenic fungi in soil samples of potted plants fromSari hospitals Iranrdquo Journal of Hospital Infection vol 58 no 1pp 59ndash62 2004

[3] R Vanbreuseghem ldquoTechnique biologique pour lisolement desdermatophytes du solrdquo Annales de la Societe Belge de MedecineTropicale vol 32 pp 173ndash178 1952

[4] S M Zaki Y Mikami A A Karam El-Din and Y A YoussefldquoKeratinophilic fungi recovered from muddy soil in Cairovicinities Egyptrdquo Mycopathologia vol 160 no 3 pp 245ndash2512005

[5] S K Deshmukh and S A Verekar ldquoKeratinophilic fungi fromthe vicinity of meteorite crater soils of Lonar (India)rdquo Myco-pathologia vol 162 no 4 pp 303ndash306 2006

[6] H C Gugnani S Sharma and K Wright ldquoA preliminary studyon the occurrence of keratinophilic fungi in soils of JamaicardquoRevista do Instituto de Medicina Tropical de Sao Paulo vol 56no 3 pp 231ndash234 2014

[7] K Pakshir M Rahimi Ghiasi K Zomorodian and A R Ghar-avi ldquoIsolation and molecular identification of keratinophilicfungi from public parks soil in Shiraz Iranrdquo BioMed ResearchInternational vol 2013 Article ID 619576 5 pages 2013

[8] L Sigler and J W Carmichael ldquoTaxonomy ofMalbranchea andsome other hyphomycetes with arthroconidiardquoMycotaxon vol4 pp 349ndash488 1976

[9] C A N Van Oorschot ldquoA revision of Chrysosporium and alliedgenerardquo Studies in Mycology vol 20 pp 1ndash89 1980

[10] R S Currah ldquoTaxonomy of the Onygenales ArthrodermaceaeGymnoascaceae Myxotrichaceae and Onygenaceaerdquo Myco-taxon vol 24 pp 1ndash216 1985

[11] J A von Arx ldquoThe ascomycetes genus Gymnoascusrdquo Persooniavol 13 pp 173ndash183 1986

[12] J Cano and J Gurrao ldquoThe genus Aphanoascusrdquo MycologicalResearch vol 94 pp 355ndash377 1990

[13] S B Lee and J W Taylor ldquoIsolation of DNA from fungalmycelium and single cellsrdquo in Protocols A Guide toMethods andApplications M A Innis H D Gelfand J J Sninsky and T

J White Eds pp 282ndash287 Academic Press San Diego CalifUSA 1990

[14] T J White T Bruns S Lee and J Taylor ldquoAmplification anddirect sequencing of fungal ribosomal RNA genes for phyloge-neticsrdquo in PCR Protocols A Guide to Methods and ApplicationsA Innis D H Gelfand J J Sninsky and T J White Eds pp315ndash322 Academic Press San Diego Calif USA 1990

[15] S F AltschulW GishWMiller EWMyers and D J LipmanldquoBasic local alignment search toolrdquo Journal ofMolecular Biologyvol 215 no 3 pp 403ndash410 1990

[16] K Tamura G Stecher D Peterson A Filipski and S KumarldquoMEGA6molecular evolutionary genetics analysis version 60rdquoMolecular Biology and Evolution vol 30 no 12 pp 2725ndash27292013

[17] H S Randhawa and R S Sandhu ldquoA survey of soil inhabit-ing dermatophytes and related keratinophilic fungi of IndiardquoSabouraudia Journal of Medical and Veterinary Mycology vol4 no 2 pp 71ndash79 1965

[18] S K Deshmukh and S C Agrawal ldquoPrevalence of dermato-phytes and other keratinophilic fungi in soils of MadhyaPradesh (India)rdquoMykosen vol 26 no 11 pp 574ndash577 1983

[19] S K Deshmukh and S A Verekar ldquoPrevalence of Keratinophil-ic fungi in ldquoUsarrdquo Soils of Uttar Pradesh Indiardquo MicrobiologyResearch vol 2 no 2 p e15 2011

[20] S K Deshmukh and S A Verekar ldquoIncidence of keratinophilicfungi from the soils of Vedanthangal Water Bird Sanctuary(India)rdquoMycoses vol 54 no 6 pp 487ndash490 2011

[21] A K Garg ldquoIsolation of dermatophytes and other keratinophil-ic fungi from soils in Indiardquo Sabouraudia Journal ofMedical andVeterinary Mycology vol 4 no 4 pp 259ndash264 1966

[22] N C Dey and L M Kakoti ldquoMicrosporum gypseum in IndiardquoJournal of the IndianMedical Association vol 25 no 5 pp 160ndash164 1955

[23] R K S Kushwaha and S C Agarwal ldquoSome keratinophilicfungi and related dermatophytes from soilsrdquo Proceedings of theIndian National Science Academy vol 42 no B pp 102ndash1101976

[24] C J Singh B G Singh and B S Singh ldquoKeratinophilic fungiof Ghana birds sanctuary Bharatpur (Rajasthan)rdquo Advances inPlant Sciences vol 7 pp 280ndash291 1994

[25] G M Vidyasagar N Hosmani and D Shivkumar ldquoKer-atinophilic fungi isolated from hospital dust and soils of publicplaces at Gulbarga Indiardquo Mycopathologia vol 159 no 1 pp13ndash21 2005

[26] I Singh A Mishra and R K S Kushwaha ldquoDermatophytesrelated keratinophilic and opportunistic fungi in indoor dust ofhouses and hospitalsrdquo Indian Journal of Medical Microbiologyvol 27 no 3 pp 242ndash246 2009

[27] N Jain and M Sharma ldquoDistribution of dermatophytes andother related fungi in Jaipur city with particular reference tosoil pHrdquoMycoses vol 54 no 1 pp 52ndash58 2011

[28] JW Carmichael ldquoChrysosporium and some other aleuriosporichyphomycetesrdquo Canadian Journal of Botany vol 40 pp 1137ndash1173 1962

[29] S A Verekar and S K Deshmukh ldquoIncidence of keratinophilicfungi from caves around Mumbai Maharastra (India)rdquo Journalof Basic and Applied Mycology vol 5 pp 62ndash64 2006

[30] I Singh R K S Kushwaha andP Parihar ldquoKeratinophilic fungiin soil of potted plants of indoor environments inKanpur Indiaand their proteolytic abilityrdquoMycoscience vol 50 no 4 pp 303ndash307 2009

Journal of Mycology 7

[31] S Katiyar and R K S Kushwaha ldquoHuman hair colonizing fungiin water sediments of IndiardquoMycopathologia vol 152 no 2 pp81ndash84 2001

[32] I Singh and R K S Kushwaha ldquoDermatophytes and relatedkeratinophilic fungi in soil of parks and agricultural fields ofUttar Pradesh Indiardquo Indian Journal of Dermatology vol 55 no3 pp 306ndash308 2010

[33] B Sur and G R Ghosh ldquoKeratinophilic fungi from OrissaIndia I isolation from soilsrdquo Sabouraudia Journal ofMedical andVeterinary Mycology vol 18 no 4 pp 269ndash274 1980

[34] S K Deshmukh ldquoIncidence of keratinophilic fungi fromselected soils of Kerala state (India)rdquo Mycopathologia vol 156no 3 pp 177ndash181 2003

[35] G R Ghosh and S Bhatt ldquoKeratinophilic Fungi from ChilkaLake-side Soil Orissa (India)rdquo Indian Journal of Microbiologyvol 40 no 4 pp 247ndash254 2000

[36] P C Jain and S C Agrawal ldquoSome additions to IndianMalbrancheardquo Kavaka vol 7 pp 69ndash72 1979

[37] S K Deshmukh and S C Agrawal ldquoIsolation of dermatophytesand other keratinophilic fungi from soils of Jammu IndiardquoMycoses vol 46 no 5-6 pp 226ndash228 2003

[38] S Kaul and G Sumbali ldquoKeratinolysis by poultry farm soilfungirdquoMycopathologia vol 139 no 3 pp 137ndash140 1997

[39] P Saxena A Kumar and J N Shrivastava ldquoDiversity ofkeratinophilic mycoflora in the soil of Agra (India)rdquo FoliaMicrobiologica vol 49 no 4 pp 430ndash434 2004

[40] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from the vicinity of salt pan soils of MumbaiIndiardquoMycopathologia vol 157 no 3 pp 265ndash267 2004

[41] H C Gugnani A Paliwal-Joshi H Rahman et al ldquoOccurrenceof pathogenic fungi in soil of burrows of rats and of other sitesin bamboo plantations in India and NepalrdquoMycoses vol 50 no6 pp 507ndash511 2007

[42] M Sharma and M Sharma ldquoIncidence of dermatophytes andother keratinophilic fungi in the schools and college playgroundsoils of Jaipur Indiardquo African Journal of Microbiology Researchvol 4 no 24 pp 2647ndash2654 2010

[43] L N Mohapatra H C Gugnani and K Shivrajan ldquoNaturalinfection in laboratory animals due to Trichophyton mentagro-phytes in IndiardquoMycopathologia et Mycologia Applicata vol 24no 3 pp 275ndash280 1964

[44] C A Oyeka ldquoTrichophyton mentagrophytes a keratinophilicfungusrdquo in Biology of Dermatophytes and other KeratinophilicFungi R K S Kushwaha and J Guarro Eds pp 60ndash65 RevistaIberoamericana de Micologia Bilbao Spain 2000

[45] T N Verma B K Sinha and U L Das ldquoIsolation of ker-atinophilic fungi from soil in Bihar (India)rdquo Mykosen vol 25no 8 pp 449ndash452 1982

[46] S K Deshmukh ldquoIncidence of dermatophytes and other ker-atinophilic fungi in the glacier bank soils of the Kashmir valleyIndiardquoMycologist vol 16 no 4 pp 165ndash167 2002

[47] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from Karnala bird sanctuary Maharashtra(India)rdquo Journal of Basic and Applied Mycology vol 1 no 2 pp194ndash196 2002

[48] E Roilides L Sigler E Bibashi H Katsifa N Flaris andC Panteliadis ldquoDisseminated infection due to Chrysosporiumzonatum in a patient with chronic granulomatous disease andreview of non-aspergillus fungal infections in patients with thisdiseaserdquo Journal of ClinicalMicrobiology vol 37 no 1 pp 18ndash251999

[49] L Sigler A L Flis and JW Carmichael ldquoThe genusUncinocar-pus (Onygenaceae) and its synonym Brunneospora new con-cepts combinations and connections to anamorphs in Chrysos-porium and further evidence of relationship with Coccidioidesimmitisrdquo Canadian Journal of Botany vol 76 no 9 pp 1624ndash1636 1998

[50] S A Saidi S Bhatt J L Richard A Sikdar and G R GhoshldquoChrysosporium tropicum as a probable cause of mycosis ofpoultry in Indiardquo Mycopathologia vol 125 no 3 pp 143ndash1471994

[51] T Vissiennon K F Schuppel E Ullrich and A F KuijpersldquoCase report A disseminated infection due to Chrysosporiumqueenslandicum in a garter snake (Thamnophis)rdquoMycoses vol42 no 1-2 pp 107ndash110 1999

[52] G S de Hoog and J Guarro Atlas of Clinical Fungi Centraal-bureau voor Schimmelcultures Baarn The Netherlands 1995

[53] P C Iwen L Sigler S Tarantolo et al ldquoPulmonary infectioncaused by Gymnascella hyalinospora in a patient with acutemyelogenous leukemiardquo Journal of Clinical Microbiology vol38 no 1 pp 375ndash381 2000

[54] P Lyskova ldquoSaprotrophicmicroscopic fungi and dermatophytesaccompanying infections of the skin and nails of patients in theMoravian-Silesian Region (Czech Republic)rdquo Czech Mycologyvol 59 pp 125ndash137 2007

[55] A A Padhye S PMisra andM JThirumalachar ldquoOccurrenceof soil inhabiting dermatophytes and other keratinophilic fungifrom soils in Poonardquo Hindustan Antibiotics Bulletin vol 9 no2 pp 90ndash93 1966

[56] A A Padhye V H Pawar R S Sukapure and M J Thiru-malachar ldquoKeratinophilic fungi from marine soils of BombayIndia Irdquo Hindustan Antibiotics Bulletin vol 10 no 2 pp 138ndash141 1967

[57] A P Garg S Gandotra K G Mukerji and G J F Pugh ldquoEcol-ogy of keratinophilic fungirdquo Proceedings Plant Sciences vol 94no 2-3 pp 149ndash163 1985

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Page 5: Research Article Incidence of Keratinophilic Fungi from ...downloads.hindawi.com/archive/2014/148970.pdf · respectively, as described by White et al. [ ]. Ampli cation was performed

Journal of Mycology 5

AJ439446 C indicum

AJ005368 C evolceanui

AB219229 C zonatum

EF568044 C tropicum

C zonatum Vidarbha isolate

U queenslandicus

AB861842 U queenslandicus

T terrestre

EF631622 T terrestre

T mentagrophytes

HQ223449 T mentagrophytes

C serratus

AJ877222 C serratus

M gypseum

JQ390554 M gypseum

G dankaliensis

AY304514 G dankaliensis

G hyalinospora

HM991271 G hyalinospora

G petalosporus

HM991270 G petalosporus

100

100

100

100

100

100

100

100

100

100

98

99

84

92

46

98

80

68

46

63

64

000002004006008

C tropicum

C indicum Vidarbha isolate

C evolceanui Vidarbha isolate

HM036583 Auxarthron conjugatum

Auxarthron conjugatum

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Vidarbha isolate

Figure 3 Phylogenetic tree based on ITS1-58S-ITS4 region sequences for isolated 13 keratinophilic fungi with reference strains Numbers atthe respective nodes are percentage of 1000 bootstrap replicates Bar indicates genetic distance due to sequence variation

and has been confirmed in several investigations in differentparts of the world For example Chrysosporium zonatumwasreported to cause disseminated infection in a patient withchronic granulomatous disease [48] In Japan C zonatumstrains were isolated from bronchial lavage from a female inChiba and from a male in Kyushu Both patients presentedpulmonary cavity sites [49] Chrysosporium tropicum wasreported from comb lesion in two different breeds of chickenin India [50]There are reports of disseminated infections dueto C queenslandicum in garter snakes [51] Gymnascella dan-kaliensis was reported from superficial infections in humanbeings [52] and Iwen et al [53] isolatedGymnascella hyalinos-pora from invasive pulmonary infection in a patient with

acute myelogenous leukemia Similarly Lyskova [54] isolatedChrysosporium queenslandicum C sulfureum C tropicumMalbranchea pulchella and Myriodontium keratinophilumfrom infections of the skin and nails of patients in the Mora-vian-Silesian Region (Czech Republic)Thus these fungimaybe regarded as opportunistic pathogens

There are some reports of occurrence of keratinophilicfungi from various parts of Maharashtra [40 47 55 56]but to best of our knowledge this is the first comprehensivereport on incidence of keratinophilic fungi from Vidarbharegion These findings are in agreement with the findings ofprevious work on keratinophilic fungi It appears from thisstudy that a rich variety of keratinophilic fungal flora exists

6 Journal of Mycology

in Vidarbha region of Maharashtra which may be attributedto the climatic and environmental conditions such as the soiltype vegetation fauna and human habitations Garg et al[57] emphasized that the climate and perhaps other environ-mental factors are important in determining the distributionof keratinophilic fungi in ecological habitats

Our findings confirm the presence of keratinophilic andrelated dermatophytes in the soils of Vidarbha region Theseareas potentially have a high risk for causing cutaneous fungalinfections in humans and animals and could be considered asa source of these infections

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] S K Deshmukh and S A Verekar ldquoThe occurrence of dermato-phytes and other keratinophilic fungi from the soils of Hima-chal Pradesh (India)rdquo Czech Mycology vol 58 no 1-2 pp 117ndash124 2006

[2] M T Hedayati A Mohseni-Bandpi and S Moradi ldquoA surveyon the pathogenic fungi in soil samples of potted plants fromSari hospitals Iranrdquo Journal of Hospital Infection vol 58 no 1pp 59ndash62 2004

[3] R Vanbreuseghem ldquoTechnique biologique pour lisolement desdermatophytes du solrdquo Annales de la Societe Belge de MedecineTropicale vol 32 pp 173ndash178 1952

[4] S M Zaki Y Mikami A A Karam El-Din and Y A YoussefldquoKeratinophilic fungi recovered from muddy soil in Cairovicinities Egyptrdquo Mycopathologia vol 160 no 3 pp 245ndash2512005

[5] S K Deshmukh and S A Verekar ldquoKeratinophilic fungi fromthe vicinity of meteorite crater soils of Lonar (India)rdquo Myco-pathologia vol 162 no 4 pp 303ndash306 2006

[6] H C Gugnani S Sharma and K Wright ldquoA preliminary studyon the occurrence of keratinophilic fungi in soils of JamaicardquoRevista do Instituto de Medicina Tropical de Sao Paulo vol 56no 3 pp 231ndash234 2014

[7] K Pakshir M Rahimi Ghiasi K Zomorodian and A R Ghar-avi ldquoIsolation and molecular identification of keratinophilicfungi from public parks soil in Shiraz Iranrdquo BioMed ResearchInternational vol 2013 Article ID 619576 5 pages 2013

[8] L Sigler and J W Carmichael ldquoTaxonomy ofMalbranchea andsome other hyphomycetes with arthroconidiardquoMycotaxon vol4 pp 349ndash488 1976

[9] C A N Van Oorschot ldquoA revision of Chrysosporium and alliedgenerardquo Studies in Mycology vol 20 pp 1ndash89 1980

[10] R S Currah ldquoTaxonomy of the Onygenales ArthrodermaceaeGymnoascaceae Myxotrichaceae and Onygenaceaerdquo Myco-taxon vol 24 pp 1ndash216 1985

[11] J A von Arx ldquoThe ascomycetes genus Gymnoascusrdquo Persooniavol 13 pp 173ndash183 1986

[12] J Cano and J Gurrao ldquoThe genus Aphanoascusrdquo MycologicalResearch vol 94 pp 355ndash377 1990

[13] S B Lee and J W Taylor ldquoIsolation of DNA from fungalmycelium and single cellsrdquo in Protocols A Guide toMethods andApplications M A Innis H D Gelfand J J Sninsky and T

J White Eds pp 282ndash287 Academic Press San Diego CalifUSA 1990

[14] T J White T Bruns S Lee and J Taylor ldquoAmplification anddirect sequencing of fungal ribosomal RNA genes for phyloge-neticsrdquo in PCR Protocols A Guide to Methods and ApplicationsA Innis D H Gelfand J J Sninsky and T J White Eds pp315ndash322 Academic Press San Diego Calif USA 1990

[15] S F AltschulW GishWMiller EWMyers and D J LipmanldquoBasic local alignment search toolrdquo Journal ofMolecular Biologyvol 215 no 3 pp 403ndash410 1990

[16] K Tamura G Stecher D Peterson A Filipski and S KumarldquoMEGA6molecular evolutionary genetics analysis version 60rdquoMolecular Biology and Evolution vol 30 no 12 pp 2725ndash27292013

[17] H S Randhawa and R S Sandhu ldquoA survey of soil inhabit-ing dermatophytes and related keratinophilic fungi of IndiardquoSabouraudia Journal of Medical and Veterinary Mycology vol4 no 2 pp 71ndash79 1965

[18] S K Deshmukh and S C Agrawal ldquoPrevalence of dermato-phytes and other keratinophilic fungi in soils of MadhyaPradesh (India)rdquoMykosen vol 26 no 11 pp 574ndash577 1983

[19] S K Deshmukh and S A Verekar ldquoPrevalence of Keratinophil-ic fungi in ldquoUsarrdquo Soils of Uttar Pradesh Indiardquo MicrobiologyResearch vol 2 no 2 p e15 2011

[20] S K Deshmukh and S A Verekar ldquoIncidence of keratinophilicfungi from the soils of Vedanthangal Water Bird Sanctuary(India)rdquoMycoses vol 54 no 6 pp 487ndash490 2011

[21] A K Garg ldquoIsolation of dermatophytes and other keratinophil-ic fungi from soils in Indiardquo Sabouraudia Journal ofMedical andVeterinary Mycology vol 4 no 4 pp 259ndash264 1966

[22] N C Dey and L M Kakoti ldquoMicrosporum gypseum in IndiardquoJournal of the IndianMedical Association vol 25 no 5 pp 160ndash164 1955

[23] R K S Kushwaha and S C Agarwal ldquoSome keratinophilicfungi and related dermatophytes from soilsrdquo Proceedings of theIndian National Science Academy vol 42 no B pp 102ndash1101976

[24] C J Singh B G Singh and B S Singh ldquoKeratinophilic fungiof Ghana birds sanctuary Bharatpur (Rajasthan)rdquo Advances inPlant Sciences vol 7 pp 280ndash291 1994

[25] G M Vidyasagar N Hosmani and D Shivkumar ldquoKer-atinophilic fungi isolated from hospital dust and soils of publicplaces at Gulbarga Indiardquo Mycopathologia vol 159 no 1 pp13ndash21 2005

[26] I Singh A Mishra and R K S Kushwaha ldquoDermatophytesrelated keratinophilic and opportunistic fungi in indoor dust ofhouses and hospitalsrdquo Indian Journal of Medical Microbiologyvol 27 no 3 pp 242ndash246 2009

[27] N Jain and M Sharma ldquoDistribution of dermatophytes andother related fungi in Jaipur city with particular reference tosoil pHrdquoMycoses vol 54 no 1 pp 52ndash58 2011

[28] JW Carmichael ldquoChrysosporium and some other aleuriosporichyphomycetesrdquo Canadian Journal of Botany vol 40 pp 1137ndash1173 1962

[29] S A Verekar and S K Deshmukh ldquoIncidence of keratinophilicfungi from caves around Mumbai Maharastra (India)rdquo Journalof Basic and Applied Mycology vol 5 pp 62ndash64 2006

[30] I Singh R K S Kushwaha andP Parihar ldquoKeratinophilic fungiin soil of potted plants of indoor environments inKanpur Indiaand their proteolytic abilityrdquoMycoscience vol 50 no 4 pp 303ndash307 2009

Journal of Mycology 7

[31] S Katiyar and R K S Kushwaha ldquoHuman hair colonizing fungiin water sediments of IndiardquoMycopathologia vol 152 no 2 pp81ndash84 2001

[32] I Singh and R K S Kushwaha ldquoDermatophytes and relatedkeratinophilic fungi in soil of parks and agricultural fields ofUttar Pradesh Indiardquo Indian Journal of Dermatology vol 55 no3 pp 306ndash308 2010

[33] B Sur and G R Ghosh ldquoKeratinophilic fungi from OrissaIndia I isolation from soilsrdquo Sabouraudia Journal ofMedical andVeterinary Mycology vol 18 no 4 pp 269ndash274 1980

[34] S K Deshmukh ldquoIncidence of keratinophilic fungi fromselected soils of Kerala state (India)rdquo Mycopathologia vol 156no 3 pp 177ndash181 2003

[35] G R Ghosh and S Bhatt ldquoKeratinophilic Fungi from ChilkaLake-side Soil Orissa (India)rdquo Indian Journal of Microbiologyvol 40 no 4 pp 247ndash254 2000

[36] P C Jain and S C Agrawal ldquoSome additions to IndianMalbrancheardquo Kavaka vol 7 pp 69ndash72 1979

[37] S K Deshmukh and S C Agrawal ldquoIsolation of dermatophytesand other keratinophilic fungi from soils of Jammu IndiardquoMycoses vol 46 no 5-6 pp 226ndash228 2003

[38] S Kaul and G Sumbali ldquoKeratinolysis by poultry farm soilfungirdquoMycopathologia vol 139 no 3 pp 137ndash140 1997

[39] P Saxena A Kumar and J N Shrivastava ldquoDiversity ofkeratinophilic mycoflora in the soil of Agra (India)rdquo FoliaMicrobiologica vol 49 no 4 pp 430ndash434 2004

[40] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from the vicinity of salt pan soils of MumbaiIndiardquoMycopathologia vol 157 no 3 pp 265ndash267 2004

[41] H C Gugnani A Paliwal-Joshi H Rahman et al ldquoOccurrenceof pathogenic fungi in soil of burrows of rats and of other sitesin bamboo plantations in India and NepalrdquoMycoses vol 50 no6 pp 507ndash511 2007

[42] M Sharma and M Sharma ldquoIncidence of dermatophytes andother keratinophilic fungi in the schools and college playgroundsoils of Jaipur Indiardquo African Journal of Microbiology Researchvol 4 no 24 pp 2647ndash2654 2010

[43] L N Mohapatra H C Gugnani and K Shivrajan ldquoNaturalinfection in laboratory animals due to Trichophyton mentagro-phytes in IndiardquoMycopathologia et Mycologia Applicata vol 24no 3 pp 275ndash280 1964

[44] C A Oyeka ldquoTrichophyton mentagrophytes a keratinophilicfungusrdquo in Biology of Dermatophytes and other KeratinophilicFungi R K S Kushwaha and J Guarro Eds pp 60ndash65 RevistaIberoamericana de Micologia Bilbao Spain 2000

[45] T N Verma B K Sinha and U L Das ldquoIsolation of ker-atinophilic fungi from soil in Bihar (India)rdquo Mykosen vol 25no 8 pp 449ndash452 1982

[46] S K Deshmukh ldquoIncidence of dermatophytes and other ker-atinophilic fungi in the glacier bank soils of the Kashmir valleyIndiardquoMycologist vol 16 no 4 pp 165ndash167 2002

[47] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from Karnala bird sanctuary Maharashtra(India)rdquo Journal of Basic and Applied Mycology vol 1 no 2 pp194ndash196 2002

[48] E Roilides L Sigler E Bibashi H Katsifa N Flaris andC Panteliadis ldquoDisseminated infection due to Chrysosporiumzonatum in a patient with chronic granulomatous disease andreview of non-aspergillus fungal infections in patients with thisdiseaserdquo Journal of ClinicalMicrobiology vol 37 no 1 pp 18ndash251999

[49] L Sigler A L Flis and JW Carmichael ldquoThe genusUncinocar-pus (Onygenaceae) and its synonym Brunneospora new con-cepts combinations and connections to anamorphs in Chrysos-porium and further evidence of relationship with Coccidioidesimmitisrdquo Canadian Journal of Botany vol 76 no 9 pp 1624ndash1636 1998

[50] S A Saidi S Bhatt J L Richard A Sikdar and G R GhoshldquoChrysosporium tropicum as a probable cause of mycosis ofpoultry in Indiardquo Mycopathologia vol 125 no 3 pp 143ndash1471994

[51] T Vissiennon K F Schuppel E Ullrich and A F KuijpersldquoCase report A disseminated infection due to Chrysosporiumqueenslandicum in a garter snake (Thamnophis)rdquoMycoses vol42 no 1-2 pp 107ndash110 1999

[52] G S de Hoog and J Guarro Atlas of Clinical Fungi Centraal-bureau voor Schimmelcultures Baarn The Netherlands 1995

[53] P C Iwen L Sigler S Tarantolo et al ldquoPulmonary infectioncaused by Gymnascella hyalinospora in a patient with acutemyelogenous leukemiardquo Journal of Clinical Microbiology vol38 no 1 pp 375ndash381 2000

[54] P Lyskova ldquoSaprotrophicmicroscopic fungi and dermatophytesaccompanying infections of the skin and nails of patients in theMoravian-Silesian Region (Czech Republic)rdquo Czech Mycologyvol 59 pp 125ndash137 2007

[55] A A Padhye S PMisra andM JThirumalachar ldquoOccurrenceof soil inhabiting dermatophytes and other keratinophilic fungifrom soils in Poonardquo Hindustan Antibiotics Bulletin vol 9 no2 pp 90ndash93 1966

[56] A A Padhye V H Pawar R S Sukapure and M J Thiru-malachar ldquoKeratinophilic fungi from marine soils of BombayIndia Irdquo Hindustan Antibiotics Bulletin vol 10 no 2 pp 138ndash141 1967

[57] A P Garg S Gandotra K G Mukerji and G J F Pugh ldquoEcol-ogy of keratinophilic fungirdquo Proceedings Plant Sciences vol 94no 2-3 pp 149ndash163 1985

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Page 6: Research Article Incidence of Keratinophilic Fungi from ...downloads.hindawi.com/archive/2014/148970.pdf · respectively, as described by White et al. [ ]. Ampli cation was performed

6 Journal of Mycology

in Vidarbha region of Maharashtra which may be attributedto the climatic and environmental conditions such as the soiltype vegetation fauna and human habitations Garg et al[57] emphasized that the climate and perhaps other environ-mental factors are important in determining the distributionof keratinophilic fungi in ecological habitats

Our findings confirm the presence of keratinophilic andrelated dermatophytes in the soils of Vidarbha region Theseareas potentially have a high risk for causing cutaneous fungalinfections in humans and animals and could be considered asa source of these infections

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] S K Deshmukh and S A Verekar ldquoThe occurrence of dermato-phytes and other keratinophilic fungi from the soils of Hima-chal Pradesh (India)rdquo Czech Mycology vol 58 no 1-2 pp 117ndash124 2006

[2] M T Hedayati A Mohseni-Bandpi and S Moradi ldquoA surveyon the pathogenic fungi in soil samples of potted plants fromSari hospitals Iranrdquo Journal of Hospital Infection vol 58 no 1pp 59ndash62 2004

[3] R Vanbreuseghem ldquoTechnique biologique pour lisolement desdermatophytes du solrdquo Annales de la Societe Belge de MedecineTropicale vol 32 pp 173ndash178 1952

[4] S M Zaki Y Mikami A A Karam El-Din and Y A YoussefldquoKeratinophilic fungi recovered from muddy soil in Cairovicinities Egyptrdquo Mycopathologia vol 160 no 3 pp 245ndash2512005

[5] S K Deshmukh and S A Verekar ldquoKeratinophilic fungi fromthe vicinity of meteorite crater soils of Lonar (India)rdquo Myco-pathologia vol 162 no 4 pp 303ndash306 2006

[6] H C Gugnani S Sharma and K Wright ldquoA preliminary studyon the occurrence of keratinophilic fungi in soils of JamaicardquoRevista do Instituto de Medicina Tropical de Sao Paulo vol 56no 3 pp 231ndash234 2014

[7] K Pakshir M Rahimi Ghiasi K Zomorodian and A R Ghar-avi ldquoIsolation and molecular identification of keratinophilicfungi from public parks soil in Shiraz Iranrdquo BioMed ResearchInternational vol 2013 Article ID 619576 5 pages 2013

[8] L Sigler and J W Carmichael ldquoTaxonomy ofMalbranchea andsome other hyphomycetes with arthroconidiardquoMycotaxon vol4 pp 349ndash488 1976

[9] C A N Van Oorschot ldquoA revision of Chrysosporium and alliedgenerardquo Studies in Mycology vol 20 pp 1ndash89 1980

[10] R S Currah ldquoTaxonomy of the Onygenales ArthrodermaceaeGymnoascaceae Myxotrichaceae and Onygenaceaerdquo Myco-taxon vol 24 pp 1ndash216 1985

[11] J A von Arx ldquoThe ascomycetes genus Gymnoascusrdquo Persooniavol 13 pp 173ndash183 1986

[12] J Cano and J Gurrao ldquoThe genus Aphanoascusrdquo MycologicalResearch vol 94 pp 355ndash377 1990

[13] S B Lee and J W Taylor ldquoIsolation of DNA from fungalmycelium and single cellsrdquo in Protocols A Guide toMethods andApplications M A Innis H D Gelfand J J Sninsky and T

J White Eds pp 282ndash287 Academic Press San Diego CalifUSA 1990

[14] T J White T Bruns S Lee and J Taylor ldquoAmplification anddirect sequencing of fungal ribosomal RNA genes for phyloge-neticsrdquo in PCR Protocols A Guide to Methods and ApplicationsA Innis D H Gelfand J J Sninsky and T J White Eds pp315ndash322 Academic Press San Diego Calif USA 1990

[15] S F AltschulW GishWMiller EWMyers and D J LipmanldquoBasic local alignment search toolrdquo Journal ofMolecular Biologyvol 215 no 3 pp 403ndash410 1990

[16] K Tamura G Stecher D Peterson A Filipski and S KumarldquoMEGA6molecular evolutionary genetics analysis version 60rdquoMolecular Biology and Evolution vol 30 no 12 pp 2725ndash27292013

[17] H S Randhawa and R S Sandhu ldquoA survey of soil inhabit-ing dermatophytes and related keratinophilic fungi of IndiardquoSabouraudia Journal of Medical and Veterinary Mycology vol4 no 2 pp 71ndash79 1965

[18] S K Deshmukh and S C Agrawal ldquoPrevalence of dermato-phytes and other keratinophilic fungi in soils of MadhyaPradesh (India)rdquoMykosen vol 26 no 11 pp 574ndash577 1983

[19] S K Deshmukh and S A Verekar ldquoPrevalence of Keratinophil-ic fungi in ldquoUsarrdquo Soils of Uttar Pradesh Indiardquo MicrobiologyResearch vol 2 no 2 p e15 2011

[20] S K Deshmukh and S A Verekar ldquoIncidence of keratinophilicfungi from the soils of Vedanthangal Water Bird Sanctuary(India)rdquoMycoses vol 54 no 6 pp 487ndash490 2011

[21] A K Garg ldquoIsolation of dermatophytes and other keratinophil-ic fungi from soils in Indiardquo Sabouraudia Journal ofMedical andVeterinary Mycology vol 4 no 4 pp 259ndash264 1966

[22] N C Dey and L M Kakoti ldquoMicrosporum gypseum in IndiardquoJournal of the IndianMedical Association vol 25 no 5 pp 160ndash164 1955

[23] R K S Kushwaha and S C Agarwal ldquoSome keratinophilicfungi and related dermatophytes from soilsrdquo Proceedings of theIndian National Science Academy vol 42 no B pp 102ndash1101976

[24] C J Singh B G Singh and B S Singh ldquoKeratinophilic fungiof Ghana birds sanctuary Bharatpur (Rajasthan)rdquo Advances inPlant Sciences vol 7 pp 280ndash291 1994

[25] G M Vidyasagar N Hosmani and D Shivkumar ldquoKer-atinophilic fungi isolated from hospital dust and soils of publicplaces at Gulbarga Indiardquo Mycopathologia vol 159 no 1 pp13ndash21 2005

[26] I Singh A Mishra and R K S Kushwaha ldquoDermatophytesrelated keratinophilic and opportunistic fungi in indoor dust ofhouses and hospitalsrdquo Indian Journal of Medical Microbiologyvol 27 no 3 pp 242ndash246 2009

[27] N Jain and M Sharma ldquoDistribution of dermatophytes andother related fungi in Jaipur city with particular reference tosoil pHrdquoMycoses vol 54 no 1 pp 52ndash58 2011

[28] JW Carmichael ldquoChrysosporium and some other aleuriosporichyphomycetesrdquo Canadian Journal of Botany vol 40 pp 1137ndash1173 1962

[29] S A Verekar and S K Deshmukh ldquoIncidence of keratinophilicfungi from caves around Mumbai Maharastra (India)rdquo Journalof Basic and Applied Mycology vol 5 pp 62ndash64 2006

[30] I Singh R K S Kushwaha andP Parihar ldquoKeratinophilic fungiin soil of potted plants of indoor environments inKanpur Indiaand their proteolytic abilityrdquoMycoscience vol 50 no 4 pp 303ndash307 2009

Journal of Mycology 7

[31] S Katiyar and R K S Kushwaha ldquoHuman hair colonizing fungiin water sediments of IndiardquoMycopathologia vol 152 no 2 pp81ndash84 2001

[32] I Singh and R K S Kushwaha ldquoDermatophytes and relatedkeratinophilic fungi in soil of parks and agricultural fields ofUttar Pradesh Indiardquo Indian Journal of Dermatology vol 55 no3 pp 306ndash308 2010

[33] B Sur and G R Ghosh ldquoKeratinophilic fungi from OrissaIndia I isolation from soilsrdquo Sabouraudia Journal ofMedical andVeterinary Mycology vol 18 no 4 pp 269ndash274 1980

[34] S K Deshmukh ldquoIncidence of keratinophilic fungi fromselected soils of Kerala state (India)rdquo Mycopathologia vol 156no 3 pp 177ndash181 2003

[35] G R Ghosh and S Bhatt ldquoKeratinophilic Fungi from ChilkaLake-side Soil Orissa (India)rdquo Indian Journal of Microbiologyvol 40 no 4 pp 247ndash254 2000

[36] P C Jain and S C Agrawal ldquoSome additions to IndianMalbrancheardquo Kavaka vol 7 pp 69ndash72 1979

[37] S K Deshmukh and S C Agrawal ldquoIsolation of dermatophytesand other keratinophilic fungi from soils of Jammu IndiardquoMycoses vol 46 no 5-6 pp 226ndash228 2003

[38] S Kaul and G Sumbali ldquoKeratinolysis by poultry farm soilfungirdquoMycopathologia vol 139 no 3 pp 137ndash140 1997

[39] P Saxena A Kumar and J N Shrivastava ldquoDiversity ofkeratinophilic mycoflora in the soil of Agra (India)rdquo FoliaMicrobiologica vol 49 no 4 pp 430ndash434 2004

[40] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from the vicinity of salt pan soils of MumbaiIndiardquoMycopathologia vol 157 no 3 pp 265ndash267 2004

[41] H C Gugnani A Paliwal-Joshi H Rahman et al ldquoOccurrenceof pathogenic fungi in soil of burrows of rats and of other sitesin bamboo plantations in India and NepalrdquoMycoses vol 50 no6 pp 507ndash511 2007

[42] M Sharma and M Sharma ldquoIncidence of dermatophytes andother keratinophilic fungi in the schools and college playgroundsoils of Jaipur Indiardquo African Journal of Microbiology Researchvol 4 no 24 pp 2647ndash2654 2010

[43] L N Mohapatra H C Gugnani and K Shivrajan ldquoNaturalinfection in laboratory animals due to Trichophyton mentagro-phytes in IndiardquoMycopathologia et Mycologia Applicata vol 24no 3 pp 275ndash280 1964

[44] C A Oyeka ldquoTrichophyton mentagrophytes a keratinophilicfungusrdquo in Biology of Dermatophytes and other KeratinophilicFungi R K S Kushwaha and J Guarro Eds pp 60ndash65 RevistaIberoamericana de Micologia Bilbao Spain 2000

[45] T N Verma B K Sinha and U L Das ldquoIsolation of ker-atinophilic fungi from soil in Bihar (India)rdquo Mykosen vol 25no 8 pp 449ndash452 1982

[46] S K Deshmukh ldquoIncidence of dermatophytes and other ker-atinophilic fungi in the glacier bank soils of the Kashmir valleyIndiardquoMycologist vol 16 no 4 pp 165ndash167 2002

[47] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from Karnala bird sanctuary Maharashtra(India)rdquo Journal of Basic and Applied Mycology vol 1 no 2 pp194ndash196 2002

[48] E Roilides L Sigler E Bibashi H Katsifa N Flaris andC Panteliadis ldquoDisseminated infection due to Chrysosporiumzonatum in a patient with chronic granulomatous disease andreview of non-aspergillus fungal infections in patients with thisdiseaserdquo Journal of ClinicalMicrobiology vol 37 no 1 pp 18ndash251999

[49] L Sigler A L Flis and JW Carmichael ldquoThe genusUncinocar-pus (Onygenaceae) and its synonym Brunneospora new con-cepts combinations and connections to anamorphs in Chrysos-porium and further evidence of relationship with Coccidioidesimmitisrdquo Canadian Journal of Botany vol 76 no 9 pp 1624ndash1636 1998

[50] S A Saidi S Bhatt J L Richard A Sikdar and G R GhoshldquoChrysosporium tropicum as a probable cause of mycosis ofpoultry in Indiardquo Mycopathologia vol 125 no 3 pp 143ndash1471994

[51] T Vissiennon K F Schuppel E Ullrich and A F KuijpersldquoCase report A disseminated infection due to Chrysosporiumqueenslandicum in a garter snake (Thamnophis)rdquoMycoses vol42 no 1-2 pp 107ndash110 1999

[52] G S de Hoog and J Guarro Atlas of Clinical Fungi Centraal-bureau voor Schimmelcultures Baarn The Netherlands 1995

[53] P C Iwen L Sigler S Tarantolo et al ldquoPulmonary infectioncaused by Gymnascella hyalinospora in a patient with acutemyelogenous leukemiardquo Journal of Clinical Microbiology vol38 no 1 pp 375ndash381 2000

[54] P Lyskova ldquoSaprotrophicmicroscopic fungi and dermatophytesaccompanying infections of the skin and nails of patients in theMoravian-Silesian Region (Czech Republic)rdquo Czech Mycologyvol 59 pp 125ndash137 2007

[55] A A Padhye S PMisra andM JThirumalachar ldquoOccurrenceof soil inhabiting dermatophytes and other keratinophilic fungifrom soils in Poonardquo Hindustan Antibiotics Bulletin vol 9 no2 pp 90ndash93 1966

[56] A A Padhye V H Pawar R S Sukapure and M J Thiru-malachar ldquoKeratinophilic fungi from marine soils of BombayIndia Irdquo Hindustan Antibiotics Bulletin vol 10 no 2 pp 138ndash141 1967

[57] A P Garg S Gandotra K G Mukerji and G J F Pugh ldquoEcol-ogy of keratinophilic fungirdquo Proceedings Plant Sciences vol 94no 2-3 pp 149ndash163 1985

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Page 7: Research Article Incidence of Keratinophilic Fungi from ...downloads.hindawi.com/archive/2014/148970.pdf · respectively, as described by White et al. [ ]. Ampli cation was performed

Journal of Mycology 7

[31] S Katiyar and R K S Kushwaha ldquoHuman hair colonizing fungiin water sediments of IndiardquoMycopathologia vol 152 no 2 pp81ndash84 2001

[32] I Singh and R K S Kushwaha ldquoDermatophytes and relatedkeratinophilic fungi in soil of parks and agricultural fields ofUttar Pradesh Indiardquo Indian Journal of Dermatology vol 55 no3 pp 306ndash308 2010

[33] B Sur and G R Ghosh ldquoKeratinophilic fungi from OrissaIndia I isolation from soilsrdquo Sabouraudia Journal ofMedical andVeterinary Mycology vol 18 no 4 pp 269ndash274 1980

[34] S K Deshmukh ldquoIncidence of keratinophilic fungi fromselected soils of Kerala state (India)rdquo Mycopathologia vol 156no 3 pp 177ndash181 2003

[35] G R Ghosh and S Bhatt ldquoKeratinophilic Fungi from ChilkaLake-side Soil Orissa (India)rdquo Indian Journal of Microbiologyvol 40 no 4 pp 247ndash254 2000

[36] P C Jain and S C Agrawal ldquoSome additions to IndianMalbrancheardquo Kavaka vol 7 pp 69ndash72 1979

[37] S K Deshmukh and S C Agrawal ldquoIsolation of dermatophytesand other keratinophilic fungi from soils of Jammu IndiardquoMycoses vol 46 no 5-6 pp 226ndash228 2003

[38] S Kaul and G Sumbali ldquoKeratinolysis by poultry farm soilfungirdquoMycopathologia vol 139 no 3 pp 137ndash140 1997

[39] P Saxena A Kumar and J N Shrivastava ldquoDiversity ofkeratinophilic mycoflora in the soil of Agra (India)rdquo FoliaMicrobiologica vol 49 no 4 pp 430ndash434 2004

[40] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from the vicinity of salt pan soils of MumbaiIndiardquoMycopathologia vol 157 no 3 pp 265ndash267 2004

[41] H C Gugnani A Paliwal-Joshi H Rahman et al ldquoOccurrenceof pathogenic fungi in soil of burrows of rats and of other sitesin bamboo plantations in India and NepalrdquoMycoses vol 50 no6 pp 507ndash511 2007

[42] M Sharma and M Sharma ldquoIncidence of dermatophytes andother keratinophilic fungi in the schools and college playgroundsoils of Jaipur Indiardquo African Journal of Microbiology Researchvol 4 no 24 pp 2647ndash2654 2010

[43] L N Mohapatra H C Gugnani and K Shivrajan ldquoNaturalinfection in laboratory animals due to Trichophyton mentagro-phytes in IndiardquoMycopathologia et Mycologia Applicata vol 24no 3 pp 275ndash280 1964

[44] C A Oyeka ldquoTrichophyton mentagrophytes a keratinophilicfungusrdquo in Biology of Dermatophytes and other KeratinophilicFungi R K S Kushwaha and J Guarro Eds pp 60ndash65 RevistaIberoamericana de Micologia Bilbao Spain 2000

[45] T N Verma B K Sinha and U L Das ldquoIsolation of ker-atinophilic fungi from soil in Bihar (India)rdquo Mykosen vol 25no 8 pp 449ndash452 1982

[46] S K Deshmukh ldquoIncidence of dermatophytes and other ker-atinophilic fungi in the glacier bank soils of the Kashmir valleyIndiardquoMycologist vol 16 no 4 pp 165ndash167 2002

[47] S K Deshmukh ldquoIsolation of dermatophytes and other ker-atinophilic fungi from Karnala bird sanctuary Maharashtra(India)rdquo Journal of Basic and Applied Mycology vol 1 no 2 pp194ndash196 2002

[48] E Roilides L Sigler E Bibashi H Katsifa N Flaris andC Panteliadis ldquoDisseminated infection due to Chrysosporiumzonatum in a patient with chronic granulomatous disease andreview of non-aspergillus fungal infections in patients with thisdiseaserdquo Journal of ClinicalMicrobiology vol 37 no 1 pp 18ndash251999

[49] L Sigler A L Flis and JW Carmichael ldquoThe genusUncinocar-pus (Onygenaceae) and its synonym Brunneospora new con-cepts combinations and connections to anamorphs in Chrysos-porium and further evidence of relationship with Coccidioidesimmitisrdquo Canadian Journal of Botany vol 76 no 9 pp 1624ndash1636 1998

[50] S A Saidi S Bhatt J L Richard A Sikdar and G R GhoshldquoChrysosporium tropicum as a probable cause of mycosis ofpoultry in Indiardquo Mycopathologia vol 125 no 3 pp 143ndash1471994

[51] T Vissiennon K F Schuppel E Ullrich and A F KuijpersldquoCase report A disseminated infection due to Chrysosporiumqueenslandicum in a garter snake (Thamnophis)rdquoMycoses vol42 no 1-2 pp 107ndash110 1999

[52] G S de Hoog and J Guarro Atlas of Clinical Fungi Centraal-bureau voor Schimmelcultures Baarn The Netherlands 1995

[53] P C Iwen L Sigler S Tarantolo et al ldquoPulmonary infectioncaused by Gymnascella hyalinospora in a patient with acutemyelogenous leukemiardquo Journal of Clinical Microbiology vol38 no 1 pp 375ndash381 2000

[54] P Lyskova ldquoSaprotrophicmicroscopic fungi and dermatophytesaccompanying infections of the skin and nails of patients in theMoravian-Silesian Region (Czech Republic)rdquo Czech Mycologyvol 59 pp 125ndash137 2007

[55] A A Padhye S PMisra andM JThirumalachar ldquoOccurrenceof soil inhabiting dermatophytes and other keratinophilic fungifrom soils in Poonardquo Hindustan Antibiotics Bulletin vol 9 no2 pp 90ndash93 1966

[56] A A Padhye V H Pawar R S Sukapure and M J Thiru-malachar ldquoKeratinophilic fungi from marine soils of BombayIndia Irdquo Hindustan Antibiotics Bulletin vol 10 no 2 pp 138ndash141 1967

[57] A P Garg S Gandotra K G Mukerji and G J F Pugh ldquoEcol-ogy of keratinophilic fungirdquo Proceedings Plant Sciences vol 94no 2-3 pp 149ndash163 1985

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Page 8: Research Article Incidence of Keratinophilic Fungi from ...downloads.hindawi.com/archive/2014/148970.pdf · respectively, as described by White et al. [ ]. Ampli cation was performed

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology