Bacterial adhesion - From mechanism to control.pdf

Biochemical Engineering Journal 48 (2010) 424434

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Biochemical Engineering Journal

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Review

Bacteri

Katsutosa Department ob Project Reseac PRESTO, Japan

a r t i c l

Article history:Received 4 SepReceived in reAccepted 23 N

Keywords:AdhesionBiolmDLVO theorySurface potentBacterial nanoPolysaccharide

adhesion. In reality, cell appendages are responsible for specic andnonspecic cell adhesion tobiotic andabiotic surfaces. This paper reviews conventional physicochemical models and cell appendage-mediatedcell adhesion. State-of-the-art technologies for controlling microbial adhesion and biolm formation arealso described. These technologies are based on the adhesion mechanisms.

2009 Elsevier B.V. All rights reserved.

Contents

1. Introd2. Theor

2.1.2.2.2.3.2.4.

3. Cell su3.1.

3.2.

4. Contr4.1.4.2.4.3.

5. ConclRefer

CorresponTel.: +81 52 73

E-mail add

1369-703X/$ doi:10.1016/j.uction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425y of bacterial adhesion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425Conventional model based on the DLVO theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425Thermodynamic approach and extended DLVO theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 426Estimation of surface potential of bacterial cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 426Complexity of actual bacterial adhesion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 426rface structure mediating bacterial cell adhesion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 427Polysaccharides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4273.1.1. Lipopolysaccharide . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4273.1.2. Exopolymeric substances . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 427Bacterial nanobers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4283.2.1. Pili (Fimbriae) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4283.2.2. Autotransporter adhesin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4293.2.3. Other unique nanobers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 429

ol of bacterial adhesion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 430Antimicrobial agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 430Surface modications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 430Electro-assisted methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 430

usion and future prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 431ences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 431

ding author at: Department of Materials Science and Engineering, Nagoya Institute of Technology, Gokiso-cho, Showa-ku, Nagoya 466-8555, Japan.55214; fax: +81 52 7355214.ress: [email protected] (K. Hori).

see front matter 2009 Elsevier B.V. All rights reserved.bej.2009.11.014al adhesion: From mechanism to control

hi Horia,b,c,, Shinya Matsumotob

f Materials Science and Engineering, Nagoya Institute of Technology, Gokiso-cho, Showa-ku, Nagoya 466-8555, Japanrch Center for Interfacial Microbiology, Nagoya Institute of Technology, Gokiso-cho, Showa-ku, Nagoya 466-8555, JapanScience and Technology Agency, 4-1-8 Honcho Kawaguchi 332-0012, Saitama, Japan

e i n f o

tember 2009vised form 4 November 2009ovember 2009

ialber

a b s t r a c t

Bacterial adhesion is the initial step in colonization and biolm formation. Biolms can, on the one hand,be detrimental to both human life and industrial processes, for example, causing infection, pathogen con-tamination, and slime formation, while on the other hand, be benecial in environmental technologiesand bioprocesses. For control and utilization of bacterial adhesion and biolms, adhesion mechanismsmust be elucidated. Conventional physicochemical approaches based on Lifshitz-van der Waals, elec-trostatic and acidbase interactions provide important models of bacterial adhesion but have a limitedcapacity to provide a complete understanding of the complex adhesion process of real bacterial cells.In conventional approaches, bacterial cells, whose surfaces are structurally and chemically heteroge-neous, are often described from the viewpoint of their overall cellular properties. Cell appendages such aspolysaccharide chains and proteinous nanobers have an important function bridging between cells andthe substratum in conventional adhesion models, but sometimes cause deviation from the models of cell

K. Hori, S. Matsumoto / Biochemical Engineering Journal 48 (2010) 424434 425

1. Introduction

Microbial adhesion is the initial step in colonization and theformation of a biolman accumulated biomass of microorgan-isms and extracellular materials on a solid surface. Biolms can bedetrimental to both human life and industrial processes, causinginfection associated with medical implants [1], pathogen inter-action with host cells [2,3], periodontitis or dental caries [4,5],contamination of food from processing equipment [6,7], enhance-ment of metal corrosion [8], formation of marine biolms on shipshulls [9], and so on. However, microbial adhesion can be also bene-cial, for example, in the degradation of environmental hazardouschemicals in soil [10,11] or in bioreactors forwastewater treatment[12] or off-gas treatment [13], in agricultural uses of root nodulebacteria in the rhizosphere [14], in the degradation of biopoly-mers such as cellulose [15], and in bioocculants used for theseparation of coal particles [16]. Therefore, there are two oppositegoals for the control of microbial adhesion and biolm formation:one is the ptheir enhantechnologiecontrolmicelucidationnecessary.

In this pon the basiLandau-Verapproach, abacteria is dsented forbacterial adprocess at tgies for conare present

2. Theory o

2.1. Conven

Amongbiolms anrange of coldescribed binteractiontheory, thethe summa[18]. Sincevicinity of aBrownianmCoulomb inthe surfacedistance.

chem(B) Onsp. To

he pr ionormis in

ive eble lpulslutioions

ths, wbar

r Bros a sh. Theumic smesherehe bucebarrd surface. When the energy barrier becomes higher andfrom the substratum at lower ionic strengths, however, it

es difcult for the nanobers and EPS to reach the substra-nd bacterial cells become unable to adhere. On the contrary,

ionic strengths, the energy barrier disappears and bac-ells easily and rapidly attain irreversible adhesion. Manyhers have found a link between decreasing bacterial adhe-

a surface depending on ionic strength.revention and inhibition of biolms and the other iscement and promotion. Development of materials ands for surface modication and treatment is desired torobial adhesion and biolm formation. For this purpose,of the mechanisms underlying microbial adhesion is

aper, the theories of bacterial adhesion are outlineds of two physicochemical approaches, the Derjaguin-wey-Overbeek (DLVO) theory and the thermodynamicnd then the complexity of the adhesionprocess of actualescribed. Next, bacterial cell surface structures are pre-better understanding of the molecular mechanism ofhesion since these play important roles in the adhesionhe nanometer scale. Finally, state-of-the-art technolo-trolling microbial adhesion and/or biolm formationed.

f bacterial adhesion

tional model based on the DLVO theory

microorganisms, bacteria are major constituents ofd are about 0.52m in size, that is, nearly in theloidal particles. Therefore, bacterial adhesion has beeny the DLVO theory [17], which originally described theof a colloidal particle with a surface. According to thistotal interaction between a surface and a particle istion of their van der Waals and Coulomb interactionsthe van der Waals attractive force is dominant in thesurface, particles cannot separate from the surface byotion, and thereforeadhere irreversibly. In contrast, theteraction becomes dominant at a distance away frombecause the van der Waals force decreases sharply with

Fig. 2. Sprocess.tobacter

In tcounteticle, fsurfacerepulscal douThis reous soby thestrengenergyming othere ibarrierminimthe ioncell coand adstep, tor prodenergycell anfartherbecomtum, aat highterial cresearc

Fig. 1. Total interaction energy between a bacterial cell andatics of bacterial adhesion process. (A) Usual two-step adhesione-step adhesion model mediated by long nanobers as seen in Acine-l 5.

resence of a charged particle in an aqueous solution,s against the surface charge are attracted by the par-ng an electric double layer. As bacteria and naturalaqueous solution are usually negatively charged [19],lectrostatic energy is caused by overlap of the electri-ayers of bacterial cells and the substratum [17,1922].ive energy increases as the ionic strength of an aque-n decreases because shielding of the surface chargesin the electrical double layers lessens. At low ionichen a bacterial cell approaches a surface, there is an

rier which bacterial cells cannot surmount by swim-wnian motion (Fig. 1) [5,17,23,24]. In these conditions,allowsecondary energyminimumoutside of the energydistance from the surface to the secondary energy

is usually within several nanometers, depending ontrength. In the rst step of cell adhesion, a bacterialto this position by its motility or Brownian motion,s to the surface reversibly (Fig. 2A). In the followingacterial cell uses nanobers, such as pili and agella,s exopolymeric substances (EPS), which can pierce theier due to their small radii, for bridging between the

426 K. Hori, S. Matsumoto / Biochemical Engineering Journal 48 (2010) 424434

sion and decreasing ionic strength, which is consistent with theDLVO theory [19,2532].

2.2. Thermodynamic approach and extended DLVO theory

The thergies of the ithe followin

Gadh = swhere sm,and microoAdhesion iof adhesionprincipallynot the cashas been dinstantaneotime-depen(phase twonot be appenergy minformed [35formation othe substratcontrasts wdistance deto explaincell surfacehydrophilic

Obviousaffects bacrial cells [3moieties imhydrogen-brounding thas a form oactions, namvan Oss, thWaals com[45]. LW cdipoledipovan Oss dehydrophobiare includesmall in baexpressed a

Gadh =

where Gv

electric douinteractionsprinciple, dsive hydratienormous cinteractionsqualitativelthe classicavery strongan extremeadhesion istheory [20,3interactionsand the electhe value a

a distance between the interacting surfaces of less than 5nm isrequired before acidbase interactions can become operative [20].

2.3. Estimation of surface potential of bacterial cells

stimells hby uthatluewotententat thes haes thdiffuMorte su, EPMapp

laine

r0

)

r isspen

medinnaneterin t

chargsionsogniy pong the acte -at thial celyingd be[49

rrevevery

mple

ual bqueny, sorfac

rfaceioninditios, ans a

eratiped.ike sandia haing

ignion [5modynamic approach is based on the surface free ener-nteracting surfaces [33,34], which are calculated usingg equation:

m sl ml (1)

sl, and ml are the solidmicroorganism, solidliquid,rganismliquid interfacial free energies, respectively.s favored if the free energy is negative as a result. However, it should be noted that thermodynamicsassumes that the process is reversible, which is oftene [35]. Based on the DLVO theory, bacterial adhesionescribed as a two-phase process including an initial,us and reversible physical phase (phase one) and adent and irreversible molecular and cellular phase) [36]. However, the thermodynamic approach can-lied to the adhesion in phase one at the secondaryimum, where a new cellsubstratum interface is not,37]. Thus, the thermodynamic approach, in which thef a new cellsubstratum interface at the expense ofummedium and cellmedium interfaces is calculated,ith the DLVO theory, in which the interaction energy ispendent. However, the thermodynamic approach helpsa common observation: bacteria with a hydrophobicprefer hydrophobic material surfaces; those with acell surface prefer hydrophilic surfaces [36].ly, hydrophobicity is an important factor that greatlyterial adhesion and the self-agglutination of bacte-642]. Hydrophobic interaction between two apolarmersed in water is the sole consequence of the

onding energy of cohesion of the water molecules sur-ese moieties [43]. Hydrogen-bonding can be viewed

f more general electron-donor/electron-accepter inter-ely, Lewis acidbase interactions [44]. According to

e surface tension () consists of the Lifshitz-van derponent LW and the Lewis acidbase component AB

omprises the London dispersion force, the Keesomle force, and the Debye dipole-induced dipole force.veloped the extended DLVO theory, in which thec/hydrophilic interactions and osmotic interaction alsod [46,47]. Since the osmotic interaction is negligiblycterial adhesion, the total adhesion energy can bes:

GvdW + Gdl + GAB (2)dW is the Lifshitz-van der Waals interaction, Gdl is theble layer interaction, and GAB relates to acidbase. The latter component introduces a component that, inescribes attractive hydrophobic interactions and repul-on effects. The inuence of the acidbase interactions isompared with electrostatic and Lifshitz-van der Waals. In some cases, the extended DLVO theory seems toy predict experimental adhesion results better thanl DLVO theory; the extended DLVO theory predictsinteraction due to acidbase interactions leading to

ly deep minimum without an energy barrier, whereasnot expected to occur according to the classical DLVO5,48]. However, the distance dependence of acidbaseis also relatively short-ranged. Acidbase interactionstric double layer interaction decay exponentially fromt close contact [47], and calculations have shown that

To eterial c(EPM)foundzero vathe -pface poout thparticldescribwhichetrate.accuramodelchangebe exp

=(

wherecells suof thethe Doparamgroupsof thedimenare reclated bapplyithat ththan thand thbacterby apprier hasurfacefrom iunder[49].

2.4. Co

Actand freUsuallbare suthe suconditof consurfaceing lmconsiddevelo

Unlturallybactercontainwith stributiate the height of the energy barrier, -potentials of bac-ave been calculated from the electrophoretic mobility

sing the Smoluchowski equation. However, it has beenin many bacterial strains, the EPM approaches a non-ith increasing ionic strength [49,50]. This suggests thattial is inappropriate for accurately measuring the sur-ial of bacterial cells. Ohshima et al. [5155] have pointede Smoluchowski equation can be applied to only rigidving no polymers, and have developed a model thate EPMof particles having a soft polymer surface layer insedouble layer ions andwatermolecules can freelypen-isaki et al. [49,50] used the Ohshima model to estimaterface potentials of actual bacterial cells. In the Ohshima() is described by the following formula and the EPM

roaching a non-zero value alongwith ionic strength cand:(

0/m + DON/1/m + 1/

)+ zeN

2(3)

the relative permittivity of the medium in which theded, 0 is the permittivity of a vacuum, is the viscosityum, 0 is the surface potential of the particles, DON ispotential of the polymer layer, m is the Debye-Hckelof the polymer layer, z is the valence of the chargedhe polymers, e is the electron charge, N is the densityed groups, and is the softness parameter, which hasof reciprocal length. It is reasonable that bacterial cellszed as soft particles that are covered with or encapsu-lymers, for example, polysaccharides and proteins. Bye Ohshima model to bacterial cells, it has been revealedual surface potential of bacterial cells is much smallerpotential calculated from the Smoluchowski equatione energy barrier disappears or is sufciently low forlls to surmount it even at low ionic strengths, where,the -potential to the DLVO theory, a high energy bar-

en thought to prevent direct interaction of a cell and a]. However, the high energy barrier preventing the cellsrsibly adhering to a surface does seem to be presentlow ionic strength conditions even for a soft particle

xity of actual bacterial adhesion

acterial adhesion is an extremely complicated processtly deviates from the adhesionmodels described above.lid materials in various environments do not exposees, and various organic and inorganic matter adsorbs tos before microorganisms adhere, forming layers calledg lms [2,20,56,57]. The physicochemical propertiesning lms are quite different from the original bared interactions of microorganisms with the condition-lso differ accordingly [58]. This should be taken intoon when materials that prevent biolm formation are

imple colloidal particles, a bacterial surface is struc-chemically heterogeneous. For example, Gram-negativeve an outer membrane (OM) consisting of a lipid bilayerlipopolysaccharide (LPS) at the outer layer of the OMcant variations in the coverage density and local dis-961]. The contribution of LPS to cell adhesion will


be described later. Various kinds of OM proteins are heteroge-neously embedded in the OM and many of them protrude outof cells, forming into cell appendages. Pili and agella are typi-cal cell appendages, have lengths from hundreds of nanometers toseveral micters of sevenanobersntheory and/of cell adheIn addition,ally contribterms of therties. A hydthe hydrophinterface [3

Hori et atobacter spbacteriumvolatile orgis notewortcoated withmorphologiitrichate pithree types5 cells havecopy technidefective inadhesion wat 0.015mMindependenionic strengculture con[64]. Theseates from tthe wild-tyadhesion imcells is stillattain irreveity of the suby the nanoalso lost theinmonolayrial nanobbut also to c

3. Cell surf

As descrbial adhesiohave functitum. Whilerather thanessential foand functio

3.1. Polysac

3.1.1. LipopLipopoly

and an outetant for bac(A-band) pounits [69],posed of dihas much l

higher concentration of amino sugars, but a low concentration ofsulfate and rhamnose [71]. The B-band has been shown to formhydrogen bonds of approximately 2.5 kT J (where k is Boltzmannconstant and T is absolute temperature) each with mineral sur-

t is shor ahe ins inof seed clesize ofnds wseudoredLPSowem-m

lt ton th

Exopare ccaplubleiolmwhicouns ans [76acro

s [80are oS maonsibn EPtrostf theower ofindinconfor

d indefect, doeon tokelyhoolpro

as spdeveasbetact otha

syntulatered won tollum

djusted pmoof

t. Ine cerometers, forming long brous structures with diame-ral nanometers to tens of nanometers. These bacterialot onlypierce theenergybarrier describedby theDLVOor tether a cell body to surfaces but also cause deviationsion behavior from that predicted by the DLVO theory.although different structures on the same cell individu-ute to the net cell character, they are often described ineir combined contribution to the overall cellular prop-rophobic part localized at a bacterial nanober againstilic main cell surface specically orients the cell at the

8].l. [13] reported the highly adhesive bacterium Acine-. Tol 5, which was isolated as a toluene-degradingfrom a bioreactor for treatment of off-gas containinganic carbons. The adhesiveness of this toluene degraderhy. The inner walls of plastic tips and pipettes becomecells immediately just by cell sampling. Although twocally different nanobers, namely, anchor-like and per-lus-like nanobers, were initially found [62], at leastof peritrichate nanobers as well as the anchor on Tolbeen identied using state-of-the-art electron micro-ques. The less adhesive mutant T1 of this bacterium isthese nanobers [63]. This mutant exhibits decreasedith decreasing ionic strength and does not adhere at all, whereas adhesion of the wild type of Tol 5 is fullyt of ionic strength. Even the wild-type strain exhibitsth-dependent adhesionwhen the cells are grownunderdition, in which those nanobers are scarcely producedobservations imply that adhesion of Tol 5 cells devi-he DLVO theory due to these nanobers. In addition,pe cells expressing these nanobers attain irreversiblemediately under conditions in which adhesion of T1reversible [63]. Tol 5 cells are considered to be able torsible adhesion rapidly without approaching the vicin-

bstratum through the long distant interactionmediatedbers (Fig. 2B). On the other hand, the mutant T1 hasself-agglutinating property of the wild type, resulting

er adsorption to hydrocarbon surfaces [65]. Thus, bacte-ers contribute not only to cell adhesion to solid surfacesell agglutination.

ace structure mediating bacterial cell adhesion

ibed above, cell surface structures directly affect micro-n to solid surfaces. EPS and proteinous cell appendagesons for bridging between the cell body and a substra-EPS is important for development of biolm structurefor cell adhesion, proteinous cell appendages are oftenr the initial interaction between cells and a substratum,n as adhesin.

charides

olysaccharidesaccharide is composedof lipidA, core polysaccharides,rmost region of O antigen units [66,67] and is impor-

terial initial surface adhesion [68]. The common antigenlymer is composed of 1020 repeating -D-rhamnosewhile the serotype-specic antigen (B-band) is com-- to pentasaccharide repeating units [70]. The B-bandonger polysaccharides than the A-band as well as a

faces. Ito anclated tsurfacebarrierhinderhypothdistancgen bothat Pstratedlacking[75]. Hagelludifcueffect o

3.1.2.EPS

such asinto so[76]. Bof EPS,EPS acbiolmbiolmothermstancewhichThe EPis respbetweeas elecforce obond. Hnumbetotal b

Thebiolminvolvestrainponenadhesiis unliand Sccholerawhereof EPS

It hby constratedthe bioup-regcompaadhesiof ageCells aincreas

Themationinteresmediatuggested that 1000 or fewer such bonds are sufcientcell rmly to a surface [72]. Simoni et al. [73] calcu-

teraction energy between cells of Pseudomonas sp. anda sand column and concluded that there was an energyveral hundred kT J per cell at about 20nm and that LPSose contact of cells with surfaces. Consequently, theyed that LPS would bind the cells to the surface from aabout 20nm, and assumed that LPS could form hydro-ith the substratum. Makin and Beveridge [74] showedmonas aeruginosa PAO1 lacking B-band LPS demon-uced adhesion to hydrophilic surfaces. Escherichia coli, as in P. aeruginosa, also had decreased ability to adherever, because these LPS mutants were also defective inediated motility and type 1 pilus production, it was

determine if the loss of LPS showed a direct or indirecte cell adhesion [68].

olymeric substanceslassied into bound EPS that includes tightly bound EPSsular polymer and loosely bound EPS such as slime, andEPS that includes polymers released into bulk waterstructure is largely associated with the production

ch provides the structural support for biolms [77,78].ts for roughly 5090% of the total organic carbon ofd is considered to be the primary matrix material of,79]. EPS is composed of primary polysaccharides andmolecules such as proteins, DNA, lipids andhumic sub-]. In this review, we mainly focus on polysaccharides,ften investigated in regard to bacterial adhesion [81].trix that keeps the microorganisms together in biolmsle for adhesion to a given surface [82,83]. InteractionsS and surfaces are caused by noncovalent bonds, suchatic attraction and hydrogen bonds [84]. The bindingse interactions is weak compared with a covalent CCver, theseweak interactions aremultiplied by the largebinding sites available in the macromolecules, and theg force exceeds that of covalent CC bonds [78,85].tribution of EPS production to bacterial adhesion andmation has been examined by mutation of genesEPS synthesis. Danese et al. [77] showed that an E. colitive in the production of colanic acid, a major EPS com-s not develop normal biolm architecture. Since initialthe surface was not affected, however, colanic acid

to be involved in the rst step of cell adhesion. Yildiznik [86] demonstrated that a wild-type strain of Viblioduces a small amount of EPS and forms a thin biolm,ontaneous variants that produce an increased amountlop thick biolms [87].en reported that changes in geneexpressionare inducedf cells with a surface [88]. Davies et al. [89,90] demon-t the transcription of algC, a key gene involved inhesis of alginate required for the synthesis of EPS, isd three- to ve-fold in adhered cells of P. aeruginosaith their planktonic counterparts within minutes ofsurfaces. Garrett et al. [91] linked the down-regulationsynthesis with the up-regulation of alginate synthesis.

ing to an immobile life on surfaces lost their agella androduction of EPS.lecular mechanisms contributing to the biolm for-Staphylococcus epidermidis have attracted signicantthis bacterium, polysaccharide and protein factors

ll adhesion to native polymers [9294]. It was also


shown that S. epidermidis can adhere to surfaces coated by aconditioning lm containing extracellular matrix proteins suchas brinogen or bronectin [95]. Following the adhesion to thesurface, polysaccharide intercellular adhesin (PIA) mediates theintercellular adhesion essential for accumulation of multilayeredS. epidermidis biolms [96,97]. The major PIA is a homoglycancomposed of at least 130 -1,6-linked N-acetylated and non-N-acetylated glucosaminyl residues and ones with positive charge[98]. PIA is synthesized by the icaADBC locus encoding the PIA syn-thesis apparatus [99]. Inactivation of the icaADBC locus by Tn917insertion led to a biolm- and PIA-negative phenotype of S. epider-midis [100].

3.2. Bacterial nanobers

Manykinds of bacteria havelamentous cell appendages,whichare several to tens nanometers in diameter and hundreds to thou-sands of nanometers in length, such as agella and pili. Thesebacterial nanobers have been shown to function as adhesin.Some bacterial nanobers mediate cell adhesion to abiotic surfacesand are involved in biolm formation. Others specically bind tobiomolecules on host cells and/or extracellular matrices (ECMs),such as collagen and bronectin, and are involved in pathogenicinfection.

3.2.1. Pili (Fimbriae)The most well-known proteinous adhesin of Gram-negative

bacteria is a hair-like nanober called a pilus or mbria [3]. (Thelatter (pl: complexesgle proteinarranged ina pilus contThere are seular structusecretion anone type of

Type IVinosa havebiolm formin both nonand biolm

hosts [101]. Type IV pili extend from the poles of a bacterial cell andmediate the movement of bacteria over surfaces without the useof agella. These movements are known as social gliding in Myx-ococcus xanthus and twitching in organisms such as P. aeruginosaand Neisseria gonorrhoeae [102]. In fact, twitching motility of cellswas visualized by direct observation of extension, xation to a sur-face at the distal end, and retraction of type IV pili in P. aeruginosaunder a uorescencemicroscope [103]. These surfacemotilities arethought to contribute to enlargement and development of micro-colonies and biolms. Prepilin, a precursor of major pilin of typeIV pili, is secreted through the inner membrane (IM) by the Sec-dependent pathway, and thereafter it is processed into a maturepilin by peptidase localized at the IM. The mature pilin subunits areassembled by the IM assembly complex towards the OM throughthe periplasm [3]. The assembled pili are translocated across theOM by a system related to the type II protein secretion system,where a multimeric OM protein forms a gated pore [3,101,104].

Type 1 pili and P pili are also well-known adhesive mbriae,which are present on Gram-negative bacteria such as E. coli andSalmonella species. These types of pili are also composed of majorpilin assembled into a nanober but are peritrichate unlike polartype IV pili. It has never been reported that these peritrichate piliare responsible for twitching motility. They are important viru-lence factors of pathogens for adhesion to host cells. They aresecreted and assembled by the chaperone-usher pathway, inwhichaperiplasmic chaperoneandanOMassemblyplatform, the usher,are required (Fig. 3A) [3,105107]. After translocation into theperiplasm through the IM by the Sec-dependent pathway, sub-

onstechafold

tureexesbly isitan[10nd Ptoges. Mtivel, is lemb

Fig. 3. Overvi P piliautotransportmbriae) is a synonym for the former (pl: pili).) Pili areconsisting of several kinds of protein subunits, and a sin-subunit called a major pilin stacks by hundreds, beingto a helix to form a long rod-shaped body. The tip ofains several different proteins capped by the adhesin.veral kinds of pili, which are varied in function, molec-re, localization on a cell surface and mechanisms ofd assembly. A bacterial cell frequently has more thanpilus.pili in many Gram-negative bacteria including P. aerug-been studied most in terms of the relationship withation. This type of pili has been reported to be involvedspecic adhesion to abiotic surfaces for colonizationformation, and specic binding to target molecules in

units cby a mproperpremacomplassemconcomsurface1 pili atively,operonrespecP pilusare ass

ews of the translocation and assembly of nanober proteins. (A) Type 1 pili ander system.ituting the pili interact with the chaperone, which actsnism called donor strand complementation to allowing of the subunits while simultaneously preventingsubunitsubunit interactions. The chaperone-subunitin the periplasm are targeted to the OM usher. Fiberthought to occur at the periplasmic face of the usher,twith secretionof theber through theusher to the cell8]. In E. coli strains, the structural pilus subunits of Typepili are encoded by m and pap gene clusters, respec-

ther with the chaperone and the usher in the respectiveajor pilins of type 1 pili and P pili are FimA and PapA,y. An adhesin subunit, FimH in type 1 pilus or PapG inocated at the distal end of each pilus bril. These pililed in a top-down fashion, with the adhesin subunit

secreted by the chaperone-usher system. (B) TAAs secreted by the


incorporated rst. These adhesin subunits bind specically to tar-get molecules such as sugars or glycolipids of hosts; for example,FimH is the mannose-specic adhesin [109].

Compared with Gram-negative bacteria, information about piliof Gram-poCorynebacteognized un(23nm) areviewed bof Streptocothe adhesioGram-negainteractionsbonded copproteins cancalled sortamotifs in thmembraneprogressivetide bonds,peptidoglyc

3.2.2. AutotRecently

mbrial adhclass of virpili, they aGram-negafrom the trtion systemsystems amteins are sproteins. Toone is monis a novel s(TAAs), whiafter their sdependentthe C-termforms a -bnal passengsurface thro

Virtuallyseparates t[115]. Thisdomain remsurface or ctrast, in alldomain remwhich therThe transloconsist of 1an antiparawith a hydcase of TAAstrands and-barrel.

The methrough theof energy frpassenger dto drive setional ATADis absent insupposed totides, proba

be unable to cross the pore formed by a fused trimeric -barrel(Fig. 3B).

TAAs have been found recently in many Gram-negativepathogens, for example, Yersinia spp. YadA [118], Moraxella

alisU1,12

adA [yceof a

tendptider 300wit

-stalermre [1of thandnly dmily.ds thortel poomaiin c

n ascteriatotyen 1is fomo

calleheadA, Hiary snary

havns arn, an27,13high

shavly hoow rs. Thsed iicatetter urface

OtherGrat col. creg wi

le celfe cyed bve naeterande strxtenas thditio140]sitive bacteria is limited to a few groups such asria and Streptococci. They have largely gone unrec-til recently, likely because they are extremely thinnd difcult to observe [110]; however, these arey Scott and Zhner [111] and Telford et al. [112]. Piliccus sp. have also been shown to have key roles inn and invasion process and in pathogenesis. Unliketive pili, whose subunits associate via noncovalent, Gram-positive pili consist of multiple, covalentlyies of a single backbone pilin, to which a few accessorybe added. For their assembly, a transpeptidase enzymese is required. Sortase recognizes specic sequencee pilin subunits, which are secreted thorough the cellby the Sec-machinery, elongates the pilus oligomer byaddition of subunits joined by intermolecular isopep-and then tethers the entire assembly to the cell wallan (PG) [112114].

ransporter adhesin, autotransporter adhesins (ATADs), which are non-esins, have attracted considerable attention as a new

ulence factors [115]. Unlike long, polymeric, hair-likere short monomeric or oligomeric nanobers seen intive bacteria. The designation autotransporter comesanslocation mechanism known as the type V secre-, which is one of the most widely distributed secretionong Gram-negative bacteria [106]. In this system, pro-ecreted out of cells without the mediation of other

date, two variations have been reported in ATADs;omeric conventional autotransporters, and the otherubfamily known as trimeric autotransporter adhesinsch recent studies have identied [116]. In both types,ecretion into the periplasm across the IM by the Sec-system and procession of an N-terminal signal peptide,inal translocator domain is inserted into the OM andarrel structure to form a pore. Subsequently, an inter-er domain is secreted from the periplasm to the cellugh the pore.all conventional types undergo a cleavage event that

he passenger domain from the translocator domaincleavage is often autoproteolytic, and the passengerains either non-covalently associated with the cellan be released into the extracellular milieu. By con-TAAs that have been examined to date, the passengerains covalently linked to the translocator domain,

efore becomes the membrane anchor domain [116].cator domains in both conventional types and TAAs2 transmembrane -strands, which are arranged inllel fashion in the OM and form a -barrel porerophilic inside and a hydrophobic outside. In thes, one polypeptide has a C-terminal containing 4 -three of them are assembled into a 12-stranded

chanism of translocation of the passenger domaintranslocator is still controversial, but it is independent

om ATP and there is a hypothesis that the folding of theomain at the cell surfacemayprovide a source of energycretion through the translocator [117]. The conven-s contain an intramolecular chaperone domain, whichTAAs [116]. As for TAAs, the passenger domains arebe translocated across the pore as separate polypep-

bly unfoldedor partially folded as a folded trimerwould

catarrhHsf [12tidis Nactinoma stackthat expolypeto ovefeaturea headthe N-tstructuon thatdiverseis the othis fa-stranand a s-barrstalk dare richfunctiothe bathe proing of tUspAsthe comis alsofar thein Yadsecondquaterto datedomaicollage[115,1

TheofTAARecentworkof TAAbeen ucomplthe becell-su

3.2.3.The

the rs[135].Cwashinof singphic lifollowadhesimicromstalkates this an ewhereand adet al. [spA1 andA2 [119,120],Haemophilus inuenzaeHia and2], Xanthomonas oryzae XadA [123], Neisseria meningi-124], Bartonella henselae BadA [125] and Actinobacillustemcomitans EmaA [126]. The architecture of TAAs is notsingle major subunit as seen in pili, but a brous ones in the direction of the amino acid (a.a.) sequence of thechain. Although TAAs vary in size from about 300 a.a.0 a.a., their molecular organizations have a commonh variations; they form homotrimeric structures withk-membrane anchor architecture in the orientation ofinal toward the C-terminal, forming a lollipop-shaped20,127]. Therefore, the length of the nanober dependse polypeptide.Whereas the head and stalk domains arefound in different combinations, themembrane anchoromain that is homologous for all TAAs and thus denesThe membrane anchor contains four transmembranehat construct the fused trimeric 12-stranded -barrelcoiled-coil segment, which is considered to occlude there after export and folding of the passenger domain. Thens of TAAs are brous, highly repetitive structures thatoiled coils and extremely variable in length [127]. Theyspacers to project the head domains located away froml cell surface. For example, the stalk of Yersinia YadA,pe of TAAs, contains a right-handed coiled coil consist-5-residue repeats [128], whereas the stalk of Moraxellarmed by a left-handed coiled coil [120]. According ton oligomeric structure of coiled coils, this family (TAA)d Oca (oligomeric coiled coil adhesin) family [129]. Sodomain has been solved by X-ray crystallography onlya and BadA. Although both of YadA and Hia have thetructures that are rich in -strands, their tertiary andstructures are quite different [127]. All TAAs reportede a common function: adhesion to a host. The heade known to bind to ECM proteins such as bronectin,d laminin, and to mediate self-agglutination of cells0,131].sequence diversity and distinct mosaic-like structures

e lead todifculties in theannotationof their sequences.wever, Szczesny and Lupas [132] have developed a

eferred to as daTAA for the accurate domain annotationis useful web-based annotation platform has alreadyn the annotation and analysis of domain structures ofd TAAs [133,134] and has the potential to contribute tonderstanding of the molecular structures that controlinteractions.

unique nanobersm-negative bacterium Caulobacter crescentus is one ofonizers of submerged surfaces in aquatic environmentsscentus cells attached toa surfaceare capableof resistingth strong jets of water, suggesting that the attachmentls is extremely strong [136]. This bacteriumhasadimor-cle consisting of a stage as a swimming swarmer celly a stage as a nonmotile sessile cell that has a polarnober approximately 100nm in diameter and severals in length [137,138]. This adhesive nanober is called atipped by holdfast, a polysaccharide adhesin that medi-ong adhesion of the stalked cells to surfaces. The stalksion of the cell envelope containing IM, PG, and OM,e holdfast is composed of extracellular polysaccharidesnal components such as proteins [139]. Recently, Tsangreported that adhesion strength between the hold-


fast and the substrate is at least 68N/mm2, which is the strongestever measured for a biological adhesive. Although polymers ofN-acetylglucosamine, which are an important component in theholdfast, were revealed to play a critical role in the adhesive force[139], the cof the holdf

Recentlymorphologeuryarchaecalled hamlength andregion at tbasic structfrom the lbarbwire. Aries a triparmolecular hand anchorposed of a pof moleculathe hami mto surfaceshami mighstring-of-peother bacte

4. Control

Many mexpressdifftonic state.infection, nby every pomechanismTherefore, idifcult agable againstfor controlldeveloped rmation for ilimitations

4.1. Antimi

Utilizatiway to congenerally retive againstpathogenicpersistent a

Kim ettypes, namtheir effectmost commvarious comtiveness of clower thanchlorine arechlorine prwhen in itsThe environshould be nchemicals oare tolerantis one of th

devices [150152]. The decrease in the susceptibility of biolms tosilver is not as conspicuous as that to chlorine, but at similar levelas tobramycin, an antibiotic [146]. In fact, the ineffectiveness ofsilver against biolm formation in water distribution systems has

ecenf anownmigh46].s mirgan

rface

eral a[154]e) to

as abcoli fhaines, thteinsO-brnd yeen th

rednsitye hycoation pgroucteriiatiouce lohylenconte reas kinenationdedheetely cg readueon t

te anwer

origiontra pformadv

d thacell

ated

ectro

iousctro-ectrobetwcha

ng Sss stehemical and biophysical basis for the impressive forceast adhesin is still unclear., anovel anduniqueperitrichatenanoberwith strikingy was reported on cells of the archaea designated SM1on living in cold, suldic springs [141]. This nanoberus (plural hami) is 78nm in diameter, 13m inconsists of a hook region at the tip and a pricklehe center stalk. The hamus lament possesses a helicalure, and at periodic distances, three prickles emanateament, giving it the character of industrially producedt the distal end of the hook region, the hamus car-tite grappling hook with barbs. The architecture of thisook is reminiscent of man-made shhooks, grapples

s. Although the hamus was reported to be mainly com-rotein of 120kDa, there have been no further reportsr information about the hami. The authors showed thatediate strong adhesion of single cells to each other andof different chemical nature. They supposed that thet play a crucial role in the formation of the microbialarls communities formed by SM1 euryarchaeon andria [142].

of bacterial adhesion

icroorganisms in biolms or in a sessile conditionerentphysiological phenotypes fromthose in theplank-To obtain or effectively attain resistance to antibiotics,utrition, and so on, microorganisms adhere to surfacesssible means. In other words, they have evolved thefor adhesion under various environmental conditions.nhibition of adhesion and/or biolm formation is quiteinst all microorganisms in environments even if possi-specic target species. Nevertheless, effective methodsing biolm formation or microbial adhesion have beenecently. On the other hand, enhancement of biolm for-ts utilization is not so difcult. Here, the usefulness andof such control technologies are described.

crobial agents

onof antimicrobial agents is aneasyand frequentlyusedtrol biolms. However, microorganisms in biolms aresistant to many antimicrobial materials that are effec-planktonic cells [143,144]. In particular, resistance ofbacteria in biolms to antibiotics is at the root of manynd chronic bacterial infections [144,145].al. [146] categorized antimicrobial agents into threeely, antibiotics, oxidants, and biocides, and examinediveness on planktonic cells and biolms. Chlorine, theondisinfectant, ismoderately oxidative and reactswithponents of bacterial cells [146]. However, the effec-hlorine against biolms is about 4 orders of magnitudeagainst planktonic cells [146]. Higher concentrations ofrequired for effective disinfection against biolms, but

oduces harmful disinfectant by-products, particularlypresence with high levels of organic matter [147,148].mental risk of contaminationwith antimicrobial agentsoted. In addition, the continuous utilization of sameften results in the occurrence of microorganisms whichto them [149]. Silver, which has no oxidizing capacity,e most widely used biocides, in particular, in medical

been rkinds owas shwhichtion [1biolmmicroo

4.2. Su

Sevet al.bromidfacewand E.(PEO) cvolumas prothat PEteria abetwesurfaceand dethat arbrushbasedtionaland ba

Radintrodpolyetcan beand thvarioufeatureprevenrst adto PE spositivopeninbiolmbiolmsion rasurfaceof the

In csion tobiolmsurfaceshowesubtilisinactiv

4.3. El

Varan eleThe elactionsurfaceadheristainletly reported [153]. However, the combination of twotimicrobial agents, for example, silver and tobramycinto enhance antimicrobial efciency against biolms,t be an effective strategy for preventing biolm forma-The use of antimicrobial agents before development ofght also be an effective strategy, preventing adhesion ofisms.

modications

nti-adhesive surfaces have been reported to date. Tillercovalently attached poly(4-vinyl-N-hexylpyridiniumglass slides to create a sterile surface. The resultant sur-

le topreventup to944%of S. epidermidis,P. aeruginosa,rom adhering to the surface. Since poly(ethylene oxide)s are highly mobile and have extremely large exclusioneymake the surface difcult for incomingparticles suchto approach [155]. Roosjen et al. [156] demonstratedushes on a glass surface inhibited the adhesion of bac-ast by decreasing the Lifshitz-van der Waals attractione cells and the glass surface. ThePEO-brush-coated glassuced bacterial adhesion with optimized chain lengthby more than 98% [157]. However, P. aeruginosa strains

drophobic and release surfactants adhered to the PEO-ng due to acidbase interactions [158]. Modicationsoly(ethylene glycol) (PEG) employing different func-ps and structures have also been proposed for proteinal adhesion control [159161].n-induced graft polymerization (RIGP) can be used tong graft chains on common polymer materials, such ase (PE), and the density and length of the graft chainsrolled by adjusting the time of electron beam exposurection time of vinyl monomer [162]. RIGP also allowsds of monomers to be further chemically modied. Thisbles the chains to obtain functional properties such asor promotion of bacterial adhesion. Terada et al. [163]negatively charged glycidyl methacrylate (GMA) chainss by RIGP and subsequently converted the chains intoharged diethylamino (DEA) groups by an epoxy-ring-ction. Nitrifying bacteria, which have difculty formingto their poor EPS production, successfully formed a

he DEA-modied PE surface [164,165]. The initial adhe-d the amount of bacteria adhered to the DEA-modiede 610-fold and 3-fold larger, respectively, than thosenal PE surface.ast, Gottenbos et al. [166] showed that bacterial adhe-ositively charged surface is enhanced but subsequent

ation is slower, indicating that a positively chargedersely affects biolm growth. Terada et al. [167] alsot approximately 80% of E. coli cells and 60% of Bacilluss adhering to highly positively charged surfaces wereafter a contact time of 8h.

-assisted methods

approaches for controlling bacterial adhesion based onassisted method have also been reported [168170].-assisted method utilizes the electro-repulsive inter-een bacteria and cathodic surfaces with a negativerge. It was reported that more than 75% of initiallytaphylococci was stimulated to detach from surgicalel by the application of less than6.0A/cm2 of cathodic


or block current [171]. Block current means altering the volt-age continuously between positive and negative at a constantperiod. However, the detached bacteria could again accumulateon the surface, which caused prolongation of bacterial adhesion.On the othethe anodesion, biolman anodic cto remain obacteria onadhesion [1applicationcation of banodic curran effectiveWake et al.block curreyears. In adgested to be[168].

5. Conclus

TheDLVof the physmodel of baface potentparticle theis importanbiolm formand electro

Cell appand surfacetimes causeMolecular icell adhesiotures responbetween thfaces are elumethods folar informatdevelopmegiesandofninfection.

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-assisted methods.endages not only function as bridges between cellss in the conventional adhesion models but also some-the deviation of actual cell adhesion from the models.

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[42] AgrM

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