Endemic and Other Mycoses : Genetics, Evolutionary Biology ......Onygenales –Endemic Mycoses Where...

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Endemic and Other Mycoses : Genetics, Evolutionary Biology, Environment

[email protected]

John Taylor UC Berkeley

Endemic and Other Mycoses : Genetics, Evolutionary Biology, Environment

UC Berkeley, Northern Arizona University, TGen

John Taylor, Rachel Adams, Cheng Gao, Bridget Barker

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Basidiomycota - Cryptococcus

Ascomycota – Taphrinomycotina - Pneumocystis

Ascomycota – Saccharomycotina - Candida

Ascomycota – Pezizomycota – EurotiomycetesEurotiales - Aspergillus

Ascomycota – Pezizomycota – EurotiomycetesOnygenales – Endemic Mycoses

Where are the agents of endemic mycoses?

Basidiomycota - Cryptococcus

Ascomycota – Taphrinomycotina - Pneumocystis

Ascomycota – Saccharomycotina - Candida

Ascomycota – Pezizomycota – EurotiomycetesEurotiales - Aspergillus

Ascomycota – Pezizomycota – EurotiomycetesOnygenales – Endemic Mycoses

Where are the agents of endemic mycoses?

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CoccidioidesHistoplasmaBlastomyces

Paracoccidioides

Coccidioides

Muñoz et al. 2018. Scientific ReportsDOI:10.1038/s41598-018-22816-6

Onygenales

Aspergillus


Paracoccidioides

Coccidioides


Onygenales

Aspergillus

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Paracoccidioides

Coccidioides


Onygenales

Aspergillus

www.emedicine.com

Healthy Infected

What is coccidioidomycosis?

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Distribution

of

Coccidioides

species

Hector and Laniado-Laborin

2005. PLoSMedicine

What is coccidioidomycosis and why should we care?


Arizona

California

https://www.cdc.gov/fungal/diseases/coccidioidomycosis/statistics.html

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2016


California

Cooksey et al. 2017 MMWR August 11, 2017 / 66(31);833–834

2017

What is coccidioidomycosis and why should we care?https://www.cdph.ca.gov/Programs/CID/DCDC/CDPH%20Document%20Library/CocciEpiSummary2017.pdf

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Move from the patient to the environment.

Move from the patient to the environment.Diagnostics.

How dangerous is this job? Do I need a respirator?

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Move from the patient to the environment.Diagnostics.

How dangerous is this job? Do I need a respirator?Pharmaceuticals.

Is this area so dangerous that I need to take antifungals prophylactically?

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Today’s Question:

What is the role, if any, of native mammals in the life cycle of Coccidioides?

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Background

Small mammals

Chester W. Emmons

1942

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Granuloma in mouse lung

Ashburn and Emmons 1942. Archives of Pathology 34:791-800.

1942

13%

17%

Emmons and Ashburn, 1942

1942

Pocket Mouse

Kangaroo Rat

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C. W. EMMONS

/

/

/

. . . it may be primarily a disease of rodents . . . certain species of rodents constitute a natural reservoir of coccidioidomycosis and by their geographical distribution determine the areas of endemicity of the disease.

1943

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Coccidioides immitis in the soil of the southern San Joaquin Valley.Roger O. Egeberg and Ann Frank Ely

American Journal of the Medical Sciences, February 1956, 151-41956

Coccidioides immitis in the soil of the southern San Joaquin Valley.Roger O. Egeberg and Ann Frank Ely

American Journal of the Medical Sciences, February 1956, 151-41956

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Growth patterns of Coccidioides immitis in the soil of an endemic area.Ann Frank Elconin, Roger O. Egeberg and Robert LubarskyIn: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis.

Public Health Service Publication 575.

428 7.4%Total 31

1957



1957

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1957

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Ecological studies of Coccidioides immitis.Orda A. Plunkett and F. E. Swatek

In: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis.Public Health Service Publication 575.

1957

May 1954, coccidioidomycosis found in 5 UCLA anthropology students excavating an Native American midden.



1957


Soil Samples from the midden were positive.

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1957



80 burrow samples taken near the midden – all negative.



1957



80 burrow samples taken near the midden – all negative.

440 pocket mice and kangaroo rats captured near the midden -- all negative.

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Studies of physical parameters.

Climate: temperature, water and wind

Soil

1957-2018

Morbidity caused by C. immitis was best explained by the interactionbetween two variables, the lengths of droughts and the amounts of rainfall preceding epidemics.

Climate: California

2000

Fisher MC et al. 2000 J. Clin Microbiol 38:807-813

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Relative change in cocci

morbidity

Climate: California

2000



Relative change in cocci

morbidity

Model based on length of drought and mean annual rainfall in the preceding year

Climate: California

2000


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GeoHealth 1, 51–63 (2017)

The results indicate that in both states, coccidioidomycosis incidence

is related to soil moisture levels from previous summers and falls.

Climate: California & Arizona

2017

ClimateSoil

Coccidioides

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ClimateSoil

Coccidioides

ClimateSoil

Coccidioides

Cocci has to eat.

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Background

Fungal Nutrition

Ascomycota, Pezizomycotina

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http://www.botanicalgarden.ubc.ca/potd/2007/07/xylaria_hypoxylon_tentative.php

de.wikipedia.org

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Evolution of Gene Family Size

Sharpton, Stajich et al. 2009. Genome Research

2009

Eurotiales

Onygenales

Sordariomycetes


Gene Family Reductions:

Genes coding enzymes

that digest plants

2009

https://www.123rf.com/photo_27279678_dried-out-dead-plants-lying-in-a-dry-arid-desert-environment.html

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Keratin, hair, skin & connective tissue

www.privemillenia.com

Rock Pocket Mouse

http://www.snipview.com/q/Rock%20pocket%20mouse


Gene Family Reductions:

Genes coding enzymes

that digest animals

2009

Jonah Evans, Texas. Parks and Wildlife Department, http://www.inaturalist.org/photos/407437

Perognathus longimembris

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de.wikipedia.org

Ecology

Many fungi are endophytes, they live in their plant hosts without causing apparent disease. When the leaf, stem or plant dies, the fungus becomes active, consumes the dead plant and reproduces.

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de.wikipedia.org

Ecology

Many fungi are endophytes, they live in their plant hosts without causing apparent disease. When the leaf, stem or plant dies, the fungus becomes active, consumes the dead plant and reproduces.

Hypothesis, Coccidioides spp. are Endozoans, they live in their natural animal hosts without causing apparent disease. When the animal dies, the fungus becomes active, consumes the dead animal and reproduces.

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ClimateSoil

Coccidioides

Cocci has to eat.

ClimateSoil

Animal

Coccidioides

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ClimateSoil

Animal

Coccidioides

ClimateSoil

Animal

Coccidioides

Animals have to eat.

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ClimateSoil

Plant Animal

Coccidioides

ClimateSoil

Plant Animal

Coccidioides

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ClimateSoil

Plant Animal

Coccidioides

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Maricopa

Avenal

California State Hwy 33

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California State Hwy 33

The CocciDx assay*Coccidioides-Specific PCR Assay

Targeting a Transposable Element

*CocciENV Assay. Bowers et al. 2018 Med Mycol doi: 10.1093/mmy/myy007

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Maricopa

Avenal

Coccidioides detectedin burrows at all sites

Maricopa

Avenal

Coccidioides detectedat surface at two sites

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Maricopa

Avenal

Sites where road workers have

contracted coccidioidomycosis.

Maricopa

Avenal

Sites where road workers have

contracted coccidioidomycosis.

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LivingMammal

DeadMammal

Life cycle

Arthroconidia

Taylor and Barker 2018 Med Mycol

LivingMammal

DeadMammal

Long distance dispersal in air

Short distance dispersal in

soil

Life cycle

Arthroconidia


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LivingMammal

DeadMammal



soilMammal inhales

arthroconidia

Life cycle


LivingMammal

DeadMammal



soil

Spherules develop

Mammal inhales arthroconidia

Life cycle


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LivingMammal

DeadMammal

Dissemination via fungal endospores.

Short host life



soil

Spherules develop


Life cycle

Spherules develop


LivingMammal

DeadMammal

Containment inhost granuloma.

Long host life.


Short host life



soil

Spherules develop


Life cycle

Spherules develop


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LivingMammal

DeadMammal


Long host life.


Short host life



soil

Spherules develop


Life cycle

Spherules develop


LivingMammal

DeadMammal


Long host life.


Short host life

Hyphae grow in dead host and produce

arthroconidia



soil

Spherules develop


Life cycle

Arthroconidia


Spherules develop

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LivingMammal

DeadMammal


Long host life.


Short host life


arthroconidia



soil

Spherules develop


Life cycle

Arthroconidia


Spherules develop


Today’s Question:


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Today’s Question:


What do other data say?

Solar Panel Farms

Carrizo Plain: Drought, Plants and Mammals

Cocci in agriculture

Carrizo Plain National Monument

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MMWR / August 24, 2018 / Vol. 67 / No. 33


Nine confirmed coccidioidomycosis cases were identified among 2,410 solar farm workers in California.

The incidence among workers (1,095 per 100,000 persons/year) was 4.4 to 210.6 times higher than background county rates, providing evidence that illness was work-related.

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Nine confirmed coccidioidomycosis cases were identified among 2,410 solar farm workers in California.

The incidence among workers (1,095 per 100,000 persons/year) was 4.4 to 210.6 times higher than background county rates, providing evidence that illness was work-related.

LivingMammal

DeadMammal


Long host life.


Short host life


arthroconidia



soil

Spherules develop


Life cycle

Arthroconidia

Spherules develop

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Nature Climate Change 8:819-824 (2018)

Here [Carrizo Plain], we quantified the responses of 423 sympatric

species of plants, arthropods, birds, reptiles and mammals to California’s

drought of 2012–2015—the driest period in the past 1,200 years for this

global biodiversity hotspot.

Nature Climate Change 8, pages819–824 (2018)

Nature Climate Change 8:819-824 (2018)

Here [Carrizo Plain], we quantified the responses of 423 sympatric

species of plants, arthropods, birds, reptiles and mammals to California’s

drought of 2012–2015—the driest period in the past 1,200 years for this

global biodiversity hotspot.

Nature Climate Change 8, pages819–824 (2018)

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Mammals (n=15)

Plants (n=61)

Prugh et al. 2018 Nature Climate Change Species with changes at p < 0.05

Losers Winners

Mammals (n=15)

Plants (n=61)

Losers Winners

Prugh et al. 2018 Nature Climate Change Species with changes at p < 0.05

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Prugh et al. 2018 Nature Climate Change

Drought Index

Plants


Drought Index Drought Index

Plants Rodents

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Prugh et al. 2018 Nature Climate ChangeOne rodent, the Giant Kangaroo Rat, was very abundant (86%) pre-drought

Plants Rodents

https://www.cdph.ca.gov/Programs/CID/DCDC/CDPH%20Document%20Library/CocciEpiSummary2017.pdf

Millim

eters of P

recipitatio

n

Rain Human Cocci


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ClimateSoil

Plant Animal

Coccidioides

ClimateSoil

Plant Animal

Coccidioides

Is Coccidioides absent from cultivated land?

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ClimateSoil

Plant Animal

Coccidioides


ClimateSoil

Plant Animal

Coccidioides


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Arizona Medicine 1965 22: 281-288

1965

Even in areas highly infective for man, fungus was only isolated in non-cultivated and non-irrigated soils.

Kevin T. Maddy, DVM, MPH


Maricopa

Avenal

Coccidioides detectedin burrows at all sites

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6 Sites

72 soil samples

8.7M ITS1 reads

Native Soils

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1 site, 6 plots

102 Soil Samples

8.8M ITS1 reads

Agricultural Soils

Native, 3,600 OTUs Agricultural. 900 OTUs

Ascos

Fungi

Basidios

Zygos

Chytrids

Ascos

FungiBasidios

Zygos

ChytridsPhyla of Fungi

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Native, 1492 OTUs

Classes of Ascomycota

Agricultural 495 OTUs

Dothideomycetes

Sordariomycetes

Eurotiomycetes

Leotiomycetes

Lecanoromycetes

Pezizomycetes

Ascomycota

Dothideomycetes

Sordariomycetes

Eurotiomycetes

Leotiomycetes

Pezizomycetes

AscomycotaSaccharomycetes

Orders of Eurotiomycetes

Native Soils, 244 OTUs Agricultural Soils, 70 OTUs

Eurotiales

Chaetothyriales

Onygenales

Eurotiomycetes

Eurotiales

Chaetothyriales

Onygenales

Eurotiomycetes

21 OTUS

70 OTUS

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OTU Genus (Taxon) % Reads

Chrysosporium 21.2%

Gymnoascaceae 19.0%

Chrysosporium 17.3%

Spiromastix 16.1%

Auxarthron 2.5%

Coccidioides 2.2%

Chrysosporium 2.0%

Spiromastix 2.0%

Onygenales 2.0%

Auxarthron 1.8%

Auxarthron 1.2%

Native, 70 OTUs Agricultural, 21 OTUs

Onygenales most common OTUs

OTU Genus % Reads

Gymnoascus 31.7%

Chrysosporium 19.9%

Chrysosporium 9.7%

Chrysosporium 9.2%

Spiromastix 6.5%

Uncinocarpus 5.9%

Chrysosporium 4.7%

Chrysosporium 3.9%

Myceliophthora 3.6%

Onygenales 2.7%

Gymnoascoideus 1.0%


Chrysosporium 21.2%

Gymnoascaceae 19.0%

Chrysosporium 17.3%

Spiromastix 16.1%

Auxarthron 2.5%

Coccidioides 2.2%

Chrysosporium 2.0%

Spiromastix 2.0%

Onygenales 2.0%

Auxarthron 1.8%

Auxarthron 1.2%

OTU Genus % Reads

Gymnoascus 31.7%

Chrysosporium 19.9%

Chrysosporium 9.7%

Chrysosporium 9.2%

Spiromastix 6.5%

Uncinocarpus 5.9%

Chrysosporium 4.7%

Chrysosporium 3.9%

Myceliophthora 3.6%

Onygenales 2.7%

Gymnoascoideus 1.0%



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Chrysosporium 21.2%

Gymnoascaceae 19.0%

Chrysosporium 17.3%

Spiromastix 16.1%

Auxarthron 2.5%

Coccidioides 2.2%

Chrysosporium 2.0%

Spiromastix 2.0%

Onygenales 2.0%

Auxarthron 1.8%

Auxarthron 1.2%

OTU Genus % Reads

Gymnoascus 31.7%

Chrysosporium 19.9%

Chrysosporium 9.7%

Chrysosporium 9.2%

Spiromastix 6.5%

Uncinocarpus 5.9%

Chrysosporium 4.7%

Chrysosporium 3.9%

Myceliophthora 3.6%

Onygenales 2.7%

Gymnoascoideus 1.0%



ClimateSoil

Plant Animal

Coccidioides

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ClimateSoil

Plant Animal

Coccidioides

ClimateSoil

Plant Animal

Coccidioides

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• Peggy Lemaux

• Cheng Gao

• Liliam Montoya

• Devin Coleman-Derr

• Jeff Dahlberg

• Anita Sil

• Rachel Brem

• Clarissa Nobile

• Katrina Hoyer

• Aaron Hernday

• Josh Fierer

• Jason Stajich

• Bridget Barker

• Vishnu Chaturvedi

• Jessie Uehling

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• Peggy Lemaux

• Cheng Gao

• Liliam Montoya

• Devin Coleman-Derr

• Jeff Dahlberg

• Anita Sil

• Rachel Brem

• Clarissa Nobile

• Katrina Hoyer

• Aaron Hernday

• Josh Fierer

• Jason Stajich

• Bridget Barker

• Vishnu Chaturvedi

• Jessie Uehling

Questions?

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?

Cocci found in Native American middens

Cocci absent from surrounding soil and rodents

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?

A midden is an old dump for domestic waste which may consist of animal bone, human excrement, botanical material, and remnants of food, pottery, tools and other artifacts and

ecofacts associated with past human occupation.

?https://sercblog.si.edu/?p=5008

Cook-Patton, S, Landscape Ecology

Our findings of elevated nutrients in middens along the Chesapeake Bay . . . and other studies . . . demonstrate a global, albeit variable, trend of soil enrichment at and around archaeological middens that can subsequently influence the composition and abundance of modern plant communities.Although our limited sample size constrains our ability to contrast middens of different ages, these data suggest that the effects of ancient humans on the plant community can persist for over 3,000 years.

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Our findings of elevated nutrients in middens along the Chesapeake Bay . . . and other studies . . . demonstrate a global, albeit variable, trend of soil enrichment at and around archaeological middens that can subsequently influence the composition and abundance of modern plant communities.




Our findings of elevated nutrients in middens along the Chesapeake Bay . . . and other studies . . . demonstrate a global, albeit variable, trend of soil enrichment at and around archaeological middens that can subsequently influence the composition and abundance of modern FUNGAL communities.

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Our findings of elevated nutrients in middens along the Chesapeake Bay . . . and other studies . . . demonstrate a global, albeit variable, trend of soil enrichment at and around archaeological middens that can subsequently influence the composition and abundance of modern FUNGAL communities.

Although our limited sample size constrains our ability to contrast middens of different ages, these data suggest that the effects of ancient humans on the plant community can persist for over 3,000 years.

?

Cocci found in Native American middens

Cocci absent from surrounding soil and rodents

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Coccidioides Texeira et al. 2016 doi 10.3201/eid2206.151565Engelthaller et al. 2016 doi 10.1128/mBio.00550-

16Histoplasma Sepúlveda et al. 2017. doi 10.1128/mBio.01339-17Blastomyces Jiang et al. 2018. doi 10.1007/s13225-018-0403-yParacoccidioides Muñoz et al, 2016. doi 10.1128/mSphere.00213-16 Emergomyces Schwartz et al. 2018. doi 10.1007/s12281-018-0308-y


ParacoccidioidesEmergomyces

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Plants

MammalsArthropods

Birds

Response to one year of drought

Winners

Losers

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Millim

eters of P

recipitatio

n

Endemic and Other Mycoses : Genetics, Evolutionary Biology ......Onygenales –Endemic Mycoses Where...

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