TRENDS in Microbiology Vol.9 No.1 January 20019Research UpdateResearch Updatehttp://tim.trends.com 0966-842X/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0966-842X(00)01891-6Research UpdateMeeting ReportBiofilms adhere to stayHoward F. Jenkinson and Hilary M. Lappin-ScottThe 147th Ordinary Meeting of the Societyfor General Microbiology was held at theUniversity of Exeter, Exeter, UK,12–15September 2000.In their natural environments, bacteria donot exist as isolated cells but grow andsurvive in organized communities. Thesecan form flocculents in suspension, liquid-surface pellicles, or mats, but themicrobial communities that develop atphase interfaces, such as solid–liquid orair–liquid interfaces, are termed biofilms.Biofilms have multiple impacts on theEarth’s resources: they can be essential (insewerage processing); useful (for fooddigestion); inconvenient (on slipperysteps); unpleasant (as dental plaque);destructive (within water conduits); or caneven prove to be fatal (on medicalprostheses). The biofilm concept, whichwas coined in 1978 by Bill Costerton(Montana State University, Bozeman,MT, USA), is now widely embraced bymicrobiologists, engineers and computerscientists, but sadly is still poorlyrepresented within many teachingcurricula. The 147th Ordinary Meeting ofthe Society for General Microbiologyfeatured two symposia entitled‘Community Structure and Cooperation inBiofilms’ and ‘Medical Implications ofBiofilms’, and provided novel insights intohow microorganisms organize and behavein communities, the collective strengths ofwhich are inevitably greater than thesums of the individual components.Indeed, the biofilm could be considered asan evolutionary unit. It is from thismicrobial metropolis that pioneers emergeto found rural settlements upon whichnew microbial civilizations can arise. Poetry in motionThe biofilm icon is of interacting,organized, 3-D structures of organismsenveloped by extracellular polymericsubstances (EPS), with networks ofintervening water channels and multiplelayers of cells1. However, the physical andbiological structures of biofilms are subjectto multiple intrinsic and environmentalinfluences. Many physical properties ofbiofilms can be attributed to the EPSmatrix. Hans-Curt Flemming (Universityof Duisburg, Germany) described how EPScan behave as a gel or as a viscoelasticfluid, with proteins, Ca2+ions, thealignment of the polysaccharide chainsand the water content all influencingbiofilm stability. Under turbulent flow,biofilms composed of complex communitiesripple and creep across surfaces(Paul Stoodley, Montana State University,Bozeman, MT, USA), which is consistentwith EPS behaving as a viscoelastic fluid.It is this structural fluidity, along with abiological fluidity of microbial cellscontinually entering into and departingfrom associations, that makes the biofilm adynamic entity. From the initial adhesionof cells to a surface, their growth andaccumulation – through diversificationand reorganization – to dynamic maturityis surely poetry in motion (Fig. 1). In the life and times of a biofilm, theinitial adhesion of the bacterial cell to aconditioned surface is considered arandom event. If cells adhere then divideand accumulate, a linking film is produced(Henk Busscher, University of Groningen,Groningen, The Netherlands), onto whichfurther attachment and accumulation ofcells can occur (Fig. 1). During thedevelopment of polymicrobial populationssuch as dental plaque, every neworganism that binds to the linking filmpresents a new surface(Paul Kolenbrander, National Institutesof Health, Bethesda, MD, USA) andtherefore forms a basis for the accretion ofdefined organism groupings. The linkingfilm also provides a means for stabilizingcommunities that are continuouslysubject to physical shear forces. So how do bacteria know when they areon a surface? The recognition signals arestill a mystery, but it is clear that surfacegrowth is associated with massivetranscriptional upheavals. Thus, it hasbeen reported that the transcription of 38%of Escherichia coli genes is affectedfollowing cell attachment2. These bacterialcells send signals to each other, butevidence for the Gram-negative bacterialcommunication molecules, acyl homoserinelactones (AHLs), playing a major role inbiofilm formation is surprisingly notcompelling (David Davies, BinghamptonUniversity, New York, NY, USA). Althoughit does seem likely that AHLs andcell-density-dependent regulation playroles in EPS matrix deposition and in thedispersal of bacteria from biofilms3,precisely how the genetic switches andcascades are coordinated during surfacegrowth still awaits discovery.Resilience and resistanceAside from the fundamental interest inhow these microbial communities form, itis their unique characteristics that areunder scrutiny. The increased resistanceproperties of biofilm cells to externalinfluences such as antibiotics, hostdefences, antiseptics and shear forces,concerns medicine and industry, and theresilience of the communities fascinatesmicrobiologists (for a review on thissubject see pp. 34–39). Resilience happensbecause microorganisms help each other.Phil Marsh (CAMR, Porton Down,Salisbury, UK) and colleagues havedemonstrated that, within dental plaquecommunities, anaerobic bacteria surviveand grow in close physicalinterconnections (coaggregations) withspecific aerobic organisms that generatean oxygen-depleted environment.Paradoxically, bacterial species that are indirect competition for a primary nutrientsource also work out ways to survive inbiofilm communities, as demonstrated bySoeren Molin (Technical University ofDenmark, Lyngby, Denmark) forPseudomonas putida and Acinetobactersp. degrading toluene. Using green or redfluorescent protein reporter–promoterfusions, Molin and colleagues have shownthat P. putida cells quickly cluster aroundAcinetobacter cells in a nutritional inter-relationship that temporally strangles theAcinetobacter before the biofilm remodels. But why are biofilm bacteria lesssusceptible to antimicrobial agents? It isnow clear that EPS do not necessarilyprovide a diffusion barrier to inhibitorycompounds (David Allison andPeter Gilbert, University of Manchester,TRENDS in Microbiology Vol.9 No.1 January 2001http://tim.trends.com10Research UpdateResearch UpdateManchester, UK), but that biofilm bacteriaare inherently more resistant. Forexample, small-colony variants ofStaphylococcus aureus, generated