Skip to main content
SpringerLink
Log in

“Biofilmology”: a multidisciplinary review of the study of microbial biofilms

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The observation of biofilm formation is not a new phenomenon. The prevalence and significance of biofilm and aggregate formation in various processes have encouraged extensive research in this field for more than 40 years. In this review, we highlight techniques from different disciplines that have been used to successfully describe the extracellular, surface and intracellular elements that are predominant in understanding biofilm formation. To reduce the complexities involved in studying biofilms, researchers in the past have generally taken a parts-based, disciplinary specific approach to understand the different components of biofilms in isolation from one another. Recently, a few studies have looked into combining the different techniques to achieve a more holistic understanding of biofilms, yet this approach is still in its infancy. In order to attain a global understanding of the processes involved in the formation of biofilms and to formulate effective biofilm control strategies, researchers in the next decade should recognise that the study of biofilms, i.e. biofilmology, has evolved into a discipline in its own right and that mutual cooperation between the various disciplines towards a multidisciplinary research vision is vital in this field.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adav SS, Lee DJ, Show KY, Tay JH (2008) Aerobic granular sludge: recent advances. Biotechnol Adv 26:411–423

    Article  CAS  PubMed  Google Scholar 

  • Adav SS, Lin JCT, Yang Z, Whiteley CG, Lee DJ, Peng XF, Zhang ZP (2010) Stereological assessment of extracellular polymeric substances, exo-enzymes, and specific bacterial strains in bioaggregates using fluorescence experiments. Biotechnol Adv 28:255–280

    Article  CAS  PubMed  Google Scholar 

  • Ahimou F, Boonaert CJP, Adriaensen Y, Jacques P, Thonart P, Paquot M, Rouxhet PG (2007) XPS analysis of chemical functions at the surface of Bacillus subtilis. J Colloid Interface Sci 309:49–55

    Article  CAS  PubMed  Google Scholar 

  • Allison DG, Brown MR, Evans DE, Gilbert P (1990a) Surface hydrophobicity and dispersal of Pseudomonas aeruginosa from biofilms. FEMS Microbio Lett 71:101–104

    Article  CAS  Google Scholar 

  • Allison DG, Evans DJ, Brown MR, Gilbert P (1990b) Possible involvement of the division cycle in dispersal of Escherichia coli from biofilms. J Bact 172:1667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amory DE, Mozes N, Hermesse MP, Leonard AJ, Rouxhet PG (1988) Chemical analysis of the surface of microorganisms by X-ray photoelectron spectroscopy. FEMS Microbio Lett 49:107–110

    Article  Google Scholar 

  • Andrews JS, Rolfe SA, Huang WE, Scholes JD, Banwart SA (2010) Biofilm formation in environmental bacteria is influenced by different macromolecules depending on genus and species. Environ Microbiol 12:2496–2507

    Article  CAS  PubMed  Google Scholar 

  • Barrios AFG, Zuo R, Ren D, Wood TK (2006) Hha, YbaJ, and OmpA regulate Escherichia coli K12 biofilm formation and conjugation plasmids abolish motility. Biotechnol Bioeng 93:188–200

    Article  CAS  PubMed  Google Scholar 

  • Bassler BL (2002) Small talk: cell-to-cell communication in bacteria. Cell 109:421

    Article  CAS  PubMed  Google Scholar 

  • Bauer FF, Govender P, Bester MC (2010) Yeast flocculation and its biotechnological relevance. Appl Micro Biotechnol 88:31–39

    Article  CAS  Google Scholar 

  • Beenken KE, Dunman PM, McAleese F, MacApagal D, Murphy E, Projan SJ, Blevins JS, Smeltzer MS (2004) Global gene expression in Staphylococcus aureus biofilms. J Bact 186:4665–4684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beier BD, Berger AJ (2009) Method for automated background subtraction from Raman spectra containing known contaminants. Analyst 134:1198–1202

    Article  CAS  PubMed  Google Scholar 

  • Beier BD, Quivey RG, Berger AJ (2010) Identification of different bacterial species in biofilms using confocal Raman microscopy. J Biomed Opt 15:066001

    Article  PubMed  PubMed Central  Google Scholar 

  • Bellon-Fontaine MN, Rault J, Van Oss CJ (1996) Microbial adhesion to solvents: a novel method to determine the electron-donor/electron-acceptor or Lewis acid–base properties of microbial cells. Colloids Surf B Biointerfaces 7:47–53

    Article  CAS  Google Scholar 

  • Beloin C, Ghigo JM (2005) Finding gene-expression patterns in bacterial biofilms. Trends Microbiol 13:16–19

    Article  CAS  PubMed  Google Scholar 

  • Beloin C, Valle J, Latour-Lambert P, Faure P, Kzreminski M, Balestrino D, Haagensen Ja J, Molin S, Prensier G, Arbeille B, Ghigo JM (2004) Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51:659–674

    Article  CAS  PubMed  Google Scholar 

  • Biggs CA, Lant PA (2000) Activated sludge flocculation: on-line determination of floc size and the effect of shear. Water Res 34:2542–2550

    Article  CAS  Google Scholar 

  • Biggs CA, Ford AM, Lant PA (2001) Activated sludge flocculation: direct determination of the effect of calcium ions. Water Sci Technol 43:75

    Article  CAS  PubMed  Google Scholar 

  • Bos R, Van Der Mei HC, Busscher HJ (1999) Physico-chemistry of initial microbial adhesive interactions—its mechanisms and methods for study. FEMS Microbiol Rev 23:179–230

    Article  CAS  PubMed  Google Scholar 

  • Bosch A, Serra D, Prieto C, Schmitt J, Naumann D, Yantorno O (2006) Characterization of Bordetella pertussis growing as biofilm by chemical analysis and FT-IR spectroscopy. Appl Micro Biotechnol 71:736–747

    Article  CAS  Google Scholar 

  • Brackman G, Hillaert U, Van Calenbergh S, Neils HJ, Coenye T (2009) Use of quorum sensing inhibitors to interfere with biofilm formation and development in Burkholderia multivorans and Burkholderia cenocepacia. Res Microbiol 160:144–151

    Article  CAS  PubMed  Google Scholar 

  • Branda SS, Chu F, Kearns DB, Losick R, Kolter R (2006) A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol 59:1229–1238

    Article  CAS  PubMed  Google Scholar 

  • Busscher HJ, Weerkamp AH (1987) Specific and non-specific interactions in bacterial adhesion to solid substrata. FEMS Microbio Lett 46:165–173

    Article  CAS  Google Scholar 

  • Carmona P, Bellanato J, Escolar E (1997) Infrared and Raman spectroscopy of urinary calculi: a review. Biospectroscopy 3:331–346

    Article  CAS  Google Scholar 

  • Cerca N, Pier GB, Vilanova M, Oliveira R, Azeredo J (2005) Quantitative analysis of adhesion and biofilm formation on hydrophilic and hydrophobic surfaces of clinical isolates of Staphylococcus epidermidis. Res Microbiol 156:506–514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheung HY, Chan GKL, Cheung SH, Sun SQ, Fong WF (2007) Morphological and chemical changes in the attached cells of Pseudomonas aeruginosa as primary biofilms develop on aluminium and CaF2 plates. J App Microbiol 102:701–710

    Article  CAS  Google Scholar 

  • Choo-Smith LP, Maquelin K, Van Vreeswijk T, Bruining HA, Puppels GJ, Nan T, Kirschner C, Naumann D, Ami D, Am V, Orsini F, Sm D, Lamfarraj H, Sockalingum GD, Manfait M, Allouch P, Endtz HP (2001) Investigating microbial (micro)colony heterogeneity by vibrational spectroscopy. Appl Environ Microbiol 67:1461–1469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen Y (2002) Bioremediation of oil by marine microbial mats. Int Microbiol 5:189–193

    Article  CAS  PubMed  Google Scholar 

  • Cooksey KE (1992) Extracellular polymers in biofilms. Biofilms—science and technology 223:137–147

  • Costerton JW (2007) The biofilm primer. Springer, Hiedelberg

    Book  Google Scholar 

  • Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318

    Article  CAS  PubMed  Google Scholar 

  • Danese PN, Pratt LA, Kolter R (2000) Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J Bact 182:3593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davey ME, O’Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Kievit TR, Gillis R, Marx S, Brown C, Iglewski BH (2001) Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl Environ Microbiol 67:1865–1873

    Article  PubMed  PubMed Central  Google Scholar 

  • De Souza AA, Takita MA, Coletta HD, Caldana C, Yanai GM, Muto NH, De Oliveira RC, Nunes LR, Machado MA (2004) Gene expression profile of the plant pathogen Xylella fastidiosa during biofilm formation in vitro. FEMS Microbio Lett 237:341–353

    Article  Google Scholar 

  • Delille A, Quiles F, Humbert F (2007) In situ monitoring of the nascent Pseudomonas fluorescens biofilm response to variations in the dissolved organic carbon level in low-nutrient water by attenuated total reflectance–Fourier transform infrared spectroscopy. Appl Environ Microbiol 73:5782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denyer SP, Davies MC, Evans JA, Finch RG, Smith DG, Wilcox MH, Williams P (1990) Influence of carbon dioxide on the surface characteristics and adherence potential of coagulase-negative staphylococci. J Clin Microbiol 28:1813–1817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Domka J, Lee J, Wood TK (2006) YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl Environ Microbiol 72:2449–2459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dufrêne YF, Rouxhet PG (1996) Surface composition, surface properties, and adhesiveness of azospirillum brasilense—variation during growth. Can J Microbiol 42:548–556

    Article  Google Scholar 

  • Dufrene YF, Vermeiren H, Vanderleyden J, Rouxhet PG (1996) Direct evidence for the involvement of extracellular proteins in the adhesion of Azospirillum brasilense. Microbiol 142:855–865

    Article  CAS  Google Scholar 

  • Eboigbodin KE, Biggs CA (2008) Characterization of the extracellular polymeric substances produced by Escherichia coli using infrared spectroscopic, proteomic, and aggregation studies. Biomacromolecules 9:686–695

    Article  CAS  PubMed  Google Scholar 

  • Eboigbodin KE, Newton JRA, Routh AF, Biggs CA (2005) Role of nonadsorbing polymers in bacterial aggregation. Langmuir 21:12315–12319

    Article  CAS  PubMed  Google Scholar 

  • Eboigbodin KE, Newton JRA, Routh AF, Biggs CA (2006) Bacterial quorum sensing and cell surface electrokinetic properties. Appl Micro Biotechnol 73:669–675

    Article  CAS  Google Scholar 

  • Eboigbodin KE, Ojeda JJ, Biggs CA (2007) Investigating the surface properties of Escherichia coli under glucose controlled conditions and its effect on aggregation. Langmuir 23:6691–6697

    Article  CAS  PubMed  Google Scholar 

  • Erable B, Du Eanu NM, Ghangrekar MM, Dumas C, Scott K (2010) Application of electro-active biofilms. Biofouling 26:57–71

    Article  CAS  PubMed  Google Scholar 

  • Evans LR, Linker A (1973) Production and characterization of the slime polysaccharide of Pseudomonas aeruginosa. J Bact 116:915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flemming HC, Wingender J (2001) Relevance of microbial extracellular polymeric substances (EPSs)—part II: technical aspects. Water Sci Technol 43:9–16

    Article  CAS  PubMed  Google Scholar 

  • Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    Article  CAS  PubMed  Google Scholar 

  • Flemming HC, Neu TR, Wozniak DR (2007) The EPS matrix: the “house of biofilm cells”. J Bact 189:7945–7947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geoghegan M, Andrews JS, Biggs CA, Eboigbodin KE, Elliott DR, Rolfe S, Scholes J, Ojeda JJ, Romero-González ME, Edyvean RGJ (2008) The polymer physics and chemistry of microbial cell attachment and adhesion. Faraday Discuss 139:85–103

    Article  CAS  PubMed  Google Scholar 

  • Gohar M, Økstad OA, Gilois N, Sanchis V, Kolsto AB, Lereclus D (2002) Two-dimensional electrophoresis analysis of the extracellular proteome of Bacillus cereus reveals the importance of the PlcR regulon. Proteomics 2:784–791

    Article  CAS  PubMed  Google Scholar 

  • Gohar M, Faegri K, Perchat S, Ravnum S, Økstad OA, Gominet M, Kolsto AB, Lereclus D (2008) The PlcR virulence regulon of Bacillus cereus. PLoS ONE 3:2793

    Article  CAS  Google Scholar 

  • Götz F (2002) Staphylococcus and biofilms. Mol Microbiol 43:1367–1378

    Article  PubMed  Google Scholar 

  • Hall-Stoodley L, Stoodley P (2002) Developmental regulation of microbial biofilms. Curr Opin Biotechnol 13:228–233

    Article  CAS  PubMed  Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108

    Article  CAS  PubMed  Google Scholar 

  • Hamadi F, Latrache H, Zahir H, Elghmari A, Timinouni M, Ellouali M (2008) The relation between Escherichia coli surface functional groups’ composition and their physicochemical properties. Braz J Microbiol 39:10–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Hatzimanikatis V, Lee KH (1999) Dynamical analysis of gene networks requires both mRNA and protein expression information. Met Eng 1:275–281

    Article  CAS  Google Scholar 

  • Heber JR, Sevenson R, Boldman O (1952) Infrared spectroscopy as a means for identification of bacteria. Science 116:111–112

    Article  Google Scholar 

  • Henrici AT (1933) Studies of freshwater bacteria: I. A direct microscopic technique. J Bact 25:277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herben PFG, Mozes N, Rouxhet PG (1990) Variation of the surface-properties of Bacillus licheniformis according to age, temperature and aeration. Biochim Biophys Acta 1033:184–188

    Article  CAS  PubMed  Google Scholar 

  • Herzberg M, Kaye IK, Peti W, Wood TK (2006) YdgG (TqsA) controls biofilm formation in Escherichia coli K-12 through autoinducer 2 transport. J Bact 188:587–598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong Y, Brown DG (2008) Electrostatic behaviour of the charge-regulated bacterial cell surface. Langmuir 24:5003–5009

    Article  CAS  PubMed  Google Scholar 

  • Hong Y, Brown DG (2010) Alteration of bacterial surface electrostatic potential and pH upon adhesion to a solid surface and impacts to cellular bioenergetics. Biotechnol Bioeng 105:965–972

    CAS  PubMed  Google Scholar 

  • Hu JY, Fan Y, Lin YH, Zhang HB, Ong SL, Dong N, Xu JL, Ng WJ, Zhang LH (2003) Microbial diversity and prevalence of virulent pathogens in biofilms developed in a water reclamation system. Res Microbiol 154:623–629

    Article  CAS  PubMed  Google Scholar 

  • Huang Z, Meric G, Liu Z, Ma R, Tang Z, Lejeune P (2009) luxS-based quorum-sensing signaling affects biofilm formation in Streptococcus mutans. J Mol Microbiol Biotechnol 17:12–19

    Article  CAS  PubMed  Google Scholar 

  • Hudson SD, Chumanov G (2009) Bioanalytical applications of SERS (surface-enhanced Raman spectroscopy). Anal Bioanal Chem 394:679–686

    Article  CAS  PubMed  Google Scholar 

  • Irnov I, Winkler WC (2010) A regulatory RNA required for antitermination of biofilm and capsular polysaccharide operons in Bacillales. Mol Microbiol 76:559–575

    Article  CAS  PubMed  Google Scholar 

  • Ivleva NP, Wagner M, Horn H, Niessner R, Haisch C (2009) Towards a nondestructive chemical characterization of biofilm matrix by Raman microscopy. Anal Bioanal Chem 393:197–206

    Article  CAS  PubMed  Google Scholar 

  • Jenal U, Malone J (2006) Mechanisms of cyclic-di-GMP signaling in bacteria. Genetics 40:385

    Article  CAS  Google Scholar 

  • Karunakaran E, Biggs CA (2011) Mechanisms of Bacillus cereus biofilm formation: an investigation of the physicochemical characteristics of cell surfaces and extracellular proteins. Appl Micro Biotechnol 89:1161–1175

    Article  CAS  Google Scholar 

  • Kearns DB, Chu F, Branda SS, Kolter R, Losick R (2005) A master regulator for biofilm formation by Bacillus subtilis. Mol Microbiol 55:739–749

    Article  CAS  PubMed  Google Scholar 

  • Keiding K, Wybrandt L, Nielsen PH (2001) Remember the water—a comment on EPS colligative properties. Water Sci Technol 43:17

    Article  CAS  PubMed  Google Scholar 

  • Khoo X, Hamilton P, O’Toole GA, Snyder BD, Kenan DJ, Grinstaff MW (2009) Directed assembly of PEGylated-peptide coatings for infection-resistant titanium metal. J Am Chem Soc 131:10992–10997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klodzinska E, Szumski M, Dziubakiewicz E, Hrynkiewicz K, Skwarek E, Janusz W, Buszewski B (2010) Effect of zeta potential value on bacterial behaviour during electrophoretic separation. Electrophoresis 31:1590–1596

    Article  CAS  PubMed  Google Scholar 

  • Körstgens V, Flemming HC, Wingender J, Borchard W (2001) Influence of calcium ions on the mechanical properties of a model biofilm of mucoid Pseudomonas aeruginosa. Water Sci Technol 43:49

    Article  PubMed  Google Scholar 

  • Lawrence JR, Swerhone GDW, Kuhlicke U, Neu TR (2007) In situ evidence for microdomains in the polymer matrix of bacterial microcolonies. Can J Microbiol 53:450–458

    Article  CAS  PubMed  Google Scholar 

  • Liang Z, Li W, Yang S, Du P (2010) Extraction and structural characteristics of extracellular polymeric substances (EPS), pellets in autotrophic nitrifying biofilm and activated sludge. Chemosphere 81:626–632

    Article  CAS  PubMed  Google Scholar 

  • Marshall KC (1976) Interfaces in microbial ecology. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Mayer C, Moritz R, Kirschner C, Borchard W, Maibaum R, Wingender J, Flemming HC (1999) The role of intermolecular interactions: studies on model systems for bacterial biofilms. Int J Biol Macromol 26:3–16

    Article  CAS  PubMed  Google Scholar 

  • McLean RJ, Whiteley M, Stickler DJ, Fuqua WC (1997) Evidence of autoinducer activity in naturally occurring biofilms. FEMS Microbiol Lett 154:259–263

    Article  CAS  PubMed  Google Scholar 

  • Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199

    Article  CAS  PubMed  Google Scholar 

  • Moorthy S, Watnick PI (2005) Identification of novel stage-specific genetic requirements through whole genome transcription profiling of Vibrio cholerae biofilm development. Mol Microbiol 57:1623–1635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mozes N, Amory DE, Leonard AJ, Rouxhet PG (1989) Surface properties of microbial cells and their role in adhesion and flocculation. Colloids Surf 42:313–329

    Article  CAS  Google Scholar 

  • Mukherjee J, Ow SY, Noirel J, Biggs CA (2011) Quantitative protein expression and cell surface characteristics of Escherichia coli MG1655 biofilms. Proteomics 11:339–351

    Article  CAS  PubMed  Google Scholar 

  • Neu TR, Lawrence JR (2009) Extracellular polymeric substances in microbial biofilms. In: Imoran A, Brennan P, Holst O, Von Itzstein M (eds) Microbial glycobiology: structures, relevance and applications. Elsevier, San Diego, pp 735–758

    Google Scholar 

  • Neu TR, Marshall KC (1990) Bacterial polymers: physicochemical aspects of their interactions at interfaces. J Biomat Appl 5:107–133

    Article  CAS  Google Scholar 

  • Neu TR, Manz B, Volke F, Dynes JJ, Hitchcock AP, Lawrence JR (2010) Advanced imaging techniques for assessment of structure, composition and function in biofilm systems. FEMS Microbiol Ecol 72:1–21

    Article  CAS  PubMed  Google Scholar 

  • Nichols PD, Michael Henson J, Guckert JB, Nivens DE, White DC (1985) Fourier transform-infrared spectroscopic methods for microbial ecology: analysis of bacteria, bacteria–polymer mixtures and biofilms. J Microbiol Meth 4:79–94

    Article  CAS  Google Scholar 

  • Norris KP (1959) Infra-red spectroscopy and its application to microbiology. Epidemiol Infect 57:326–345

    CAS  Google Scholar 

  • Ojeda JJ, Romero-Gonzalez ME, Bachmann RT, Edyvean RGJ, Banwart SA (2008) Characterization of the cell surface and cell wall chemistry of drinking water bacteria by combining XPS, FTIR spectroscopy, modelling, and potentiometric titrations. Langmuir 24:4032–4040

    Article  CAS  PubMed  Google Scholar 

  • Oosthuizen MC, Steyn B, Theron J, Cosette P, Lindsay D, Von Holy A, Brozel VS (2002) Proteomic analysis reveals differential protein expression by Bacillus cereus during biofilm formation. Appl Environ Microbiol 68:2770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Toole GA, Gibbs KA, Hager PW, Phibbs PV Jr, Kolter R (2000) The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa. J Bact 182:425

    Article  PubMed  PubMed Central  Google Scholar 

  • Otto K, Norbeck J, Larsson T, Karlsson KA, Hermansson M (2001) Adhesion of type 1-fimbriated Escherichia coli to abiotic surfaces leads to altered composition of outer membrane proteins. J Bact 183:2445–2453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pastuszka JS, Talik E, Hacura AA, Oka J, Wlaz OA (2005) Chemical characterization of airborne bacteria using X-ray photoelectron spectroscopy (XPS) and Fourier transform infrared spectroscopy (FTIRS). Aerobiologia 21:181–192

    Article  Google Scholar 

  • Pham TK, Roy S, Noirel J, Douglas I, Wright PC, Stafford GPA (2010) Quantitative proteomic analysis of biofilm adaptation by the periodontal pathogen Tannerella forsythia. Proteomics 10:3130–3141

    Article  CAS  PubMed  Google Scholar 

  • Pink J, Smith-Palmer T, Chisholm D, Beveridge TJ, Pink DA (2005) An FTIR study of Pseudomonas aeruginosa PAO1 biofilm development: interpretation of ATR–FTIR data in the 1500–1180 cm−1 region. Biofilms 2:165–175

    Article  Google Scholar 

  • Poortinga AT, Bos R, Norde W, Busscher HJ (2002) Electric double layer interactions in bacterial adhesion to surfaces. Surf Sci Rep 47:1–32

    Article  CAS  Google Scholar 

  • Prigent-Combaret C, Prensier G, Le Thi TT, Vidal O, Lejeune P, Dorel C (2000) Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ Microbiol 2:450–464

    Article  CAS  PubMed  Google Scholar 

  • Quilès F, Humbert F, Delille A (2010) Analysis of changes in attenuated total reflection FTIR fingerprints of Pseudomonas fluorescens from planktonic state to nascent biofilm state. Spectrochim Acta A Mol Biomol Spectrosc 75:610–616

    Article  PubMed  CAS  Google Scholar 

  • Reeser RJ, Medler RT, Billington SJ, Jost BH, Joens LA (2007) Characterization of Campylobacter jejuni biofilms under defined growth conditions. Appl Environ Microbiol 73:1908–1913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren DC, Bedzyk LA, Ye RW, Thomas SM, Wood TK (2004) Differential gene expression shows natural brominated furanones interfere with the autoinducer-2 bacterial signaling system of Escherichia coli. Biotechnol Bioeng 88:630–642

    Article  CAS  PubMed  Google Scholar 

  • Resch A, Rosenstein R, Nerz C, Gotz F (2005) Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Appl Environ Microbiol 71:2663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riedewald F, Sexton A (2006) The biofilm busters. TCE 776:27–29

    CAS  Google Scholar 

  • Rijnaarts HHM, Norde W, Lyklema J, Zehnder AJB (1995) The isoelectric point of bacteria as an indicator for the presence of cell surface polymers that inhibit adhesion. Colloids Surf B Biointerfaces 4:191–197

    Article  CAS  Google Scholar 

  • Roettger BF, Ladisch MR (1989) Hydrophobic interaction chromatography. Biotechnol Adv 7:15–29

    Article  CAS  PubMed  Google Scholar 

  • Romani AM, Fund K, Artigas J, Schwartz T, Sabater S, Obst U (2008) Relevance of polymer matrix enzymes during biofilm formation. Microbiol Ecol 56:427–436

    Article  CAS  Google Scholar 

  • Rosenberg M, Gutnick D, Rosenberg E (1980) Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbio Lett 9:29–33

    Article  CAS  Google Scholar 

  • Rouxhet PG, Mozes N, Dengis PB, Dufrêne YF, Gerin PA, Genet MJ (1994) Application of X-ray photoelectron spectroscopy to microorganisms. Colloids Surf B Biointerfaces 2:347–369

    Article  CAS  Google Scholar 

  • Rozgonyi F, Szitha KR, Ljungh Å, Baloda SB, Hjertén S, Wadström T (1985) Improvement of the salt aggregation test to study bacterial cell-surface hydrophobicity. FEMS Microbio Lett 30:131–138

    Article  Google Scholar 

  • Sandt C, Smith-Palmer T, Comeau J, Pink D (2009) Quantification of water and biomass in small colony variant PAO1 biofilms by confocal Raman microspectroscopy. Appl Micro Biotechnol 83:1171–1182

    Article  CAS  Google Scholar 

  • Sauer K, Camper AK (2001) Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J Bact 183:6579–6589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schembri MA, Kjaergaard K, Klemm P (2003) Global gene expression in Escherichia coli biofilms. Mol Microbiol 48:253–267

    Article  CAS  PubMed  Google Scholar 

  • Schmitt J, Flemming HC (1998) FTIR-spectroscopy in microbial and material analysis. Int Biodeterior Biodegradation 41:1–11

    Article  CAS  Google Scholar 

  • Schwartz T, Jungfer C, Heißler S, Friedrich F, Faubel W, Obst U (2009) Combined use of molecular biology taxonomy, Raman spectrometry, and ESEM imaging to study natural biofilms grown on filter materials at waterworks. Chemosphere 77:249–257

    Article  CAS  PubMed  Google Scholar 

  • Shelud’ko AV, Kulibiakina OV, Shirokov AA, Petrova LP, Matora LI, Katsy EI (2008) The effect of mutations in the synthesis of lipopolysaccharides and calcofluor-binding polysaccharides on biofilm formation by Azospirillum brasilense. Mikrobiologiia 77:358–363

    PubMed  Google Scholar 

  • Sheng GP, Yu HQ, Li XY (2010) Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review. Biotechnol Adv 28:882–894

    Article  CAS  PubMed  Google Scholar 

  • Simoes LC, Simoes M, Vieira MJ (2007) Biofilm interactions between distinct bacterial genera isolated from drinking water. Appl Environ Microbiol 73:6192–6200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skiadas I, Gavala H, Schmidt J, Ahring B (2003) Anaerobic granular sludge and biofilm reactors. In: Scheper T (ed) Biomethanation II. Springer, Heidelberg, pp 35–67

    Chapter  Google Scholar 

  • Steyn B, Oosthuizen MC, MacDonald R, Theron J, Brözel VS (2001) The use of glass wool as an attachment surface for studying phenotypic changes in Pseudomonas aeruginosa biofilms by two-dimensional gel electrophoresis. Proteomics 1:871–879

    Article  CAS  PubMed  Google Scholar 

  • Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209

    Article  CAS  PubMed  Google Scholar 

  • Sztajer H, Lemme A, Vilchez R, Schulz S, Geffers R, Yip CYY, Levesque CM, Cvitkovitch DG, Wagner-Dobler I (2008) Autoinducer-2-regulated genes in Streptococcus mutans UA159 and global metabolic effect of the luxS mutation. J Bact 190:401–415

    Article  CAS  PubMed  Google Scholar 

  • Tapia JM, Muñoz JA, González F, Blázquez ML, Malki M, Ballester A (2009) Extraction of extracellular polymeric substances from the acidophilic bacterium Acidiphilium 3.2Sup(5). Water Sci Technol 59:1959

    Article  CAS  PubMed  Google Scholar 

  • Torimura M, Ito S, Kano K, Ikeda T, Esaka Y, Ueda T (1999) Surface characterization and on-line activity measurements of microorganisms by capillary zone electrophoresis. J Chromatogr B Biomed Sci Appl 721:31–37

    Article  CAS  PubMed  Google Scholar 

  • Trémoulet F, Duché O, Namane A, Martinie B, Labadie JC (2002) A proteomic study of Escherichia coli O157: H7 NCTC 12900 cultivated in biofilm or in planktonic growth mode. FEMS Microbio Lett 215:7–14

    Article  Google Scholar 

  • Van Alen T, Claus H, Zahedi RP, Groh J, Blazyca H, Lappann M, Sickmann A, Vogel U (2010) Comparative proteomic analysis of biofilm and planktonic cells of Neisseria meningitidis. Proteomics 10:4512–4521

    Article  PubMed  CAS  Google Scholar 

  • Van Der Mei HC, Bos R, Busscher HJ (1998) A reference guide to microbial cell surface hydrophobicity based on contact angles. Colloids Surf B Biointerfaces 11:213–221

    Article  Google Scholar 

  • Van Der Mei HC, De Vries J, Busscher HJ (2000) X-ray photoelectron spectroscopy for the study of microbial cell surfaces. Surf Sci Rep 39:1–24

    Article  Google Scholar 

  • Van Loosdrecht MC, Lyklema J, Norde W, Schraa G, Zehnder AJ (1987a) The role of bacterial cell wall hydrophobicity in adhesion. Appl Environ Microbiol 53:1893

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Loosdrecht MC, Lyklema J, Norde W, Schraa G, Zehnder AJ (1987b) Electrophoretic mobility and hydrophobicity as a measure to predict the initial steps of bacterial adhesion. Appl Environ Microbiol 53:1898–1901

    Article  PubMed  PubMed Central  Google Scholar 

  • Vilain S, Cosette P, Hubert M, Lange C, Junter GA, Jouenne T (2004a) Comparative proteomic analysis of planktonic and immobilized Pseudomonas aeruginosa cells: a multivariate statistical approach. Anal Biochem 329:120–130

    Article  CAS  PubMed  Google Scholar 

  • Vilain S, Cosette P, Zimmerlin I, Dupont JP, Junter GA, Jouenne T (2004b) Biofilm proteome: homogeneity or versatility? J Proteome Res 3:132–136

    Article  CAS  PubMed  Google Scholar 

  • Wagner M, Ivleva NP, Haisch C, Niessner R, Horn H (2009) Combined use of confocal laser scanning microscopy (CLSM) and Raman microscopy (RM): investigations on EPS-matrix. Water Res 43:63–76

    Article  CAS  PubMed  Google Scholar 

  • Walker SL, Hill JE, Redman JA, Elimelech M (2005) Influence of growth phase on adhesion kinetics of Escherichia coli D21g. Appl Environ Microbiol 71:3093–3099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welin J, Wilkins JC, Beighton D, Wrzesinski K, Fey SJ, Mose-Larsen P, Hamilton IR, Svensäter G (2003) Effect of acid shock on protein expression by biofilm cells of Streptococcus mutans. FEMS Microbio Lett 227:287–293

    Article  CAS  Google Scholar 

  • Whiteley M, Bangera MG, Bumgarner RE, Parsek MR, Teitzel GM, Lory S, Greenberg EP (2001) Gene expression in Pseudomonas aeruginosa biofilms. Nature 413:860–864

    Article  CAS  PubMed  Google Scholar 

  • Wilson WW, Wade MM, Holman SC, Champlin FR (2001) Status of methods for assessing bacterial cell surface charge properties based on zeta potential measurements. J Microbiol Meth 43:153–164

    Article  CAS  Google Scholar 

  • Wood TK (2009) Insights on Escherichia coli biofilm formation and inhibition from whole-transcriptome profiling. Environ Microbiol 11:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wozniak DJ, Wyckoff TJO, Starkey M, Keyser R, Azadi P, O’Toole GA, Parsek MR (2003) Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms. Proc Natl Acad Sci USA 100:7907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yala JF, Thebault P, Héquet A, Humblot V, Pradier CM, Berjeaud JM (2010) Elaboration of antibiofilm materials by chemical grafting of an antimicrobial peptide. Appl Micro Biotechnol 89:623–634

    Article  CAS  Google Scholar 

  • Yuan SJ, Liu CK, Pehkonen SO, Bai RB, Neoh KG, Ting YP, Kang ET (2009) Surface functionalization of Cu–Ni alloys via grafting of a bactericidal polymer for inhibiting biocorrosion by Desulfovibrio desulfuricans in anaerobic seawater. Biofouling 25:109–125

    Article  CAS  PubMed  Google Scholar 

  • Zobell CE (1943) The effect of solid surfaces upon bacterial activity. J Bact 46:39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zogaj X, Nimtz M, Rohde M, Bokranz W, Romling U (2001) The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39:1452–1463

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to acknowledge the UK Engineering and Physical Sciences Research Council (EPSRC) for a studentship for Karunakaran, Advanced Research Fellowship for Biggs (EP/E053556/01) and further project funding (EP/E053556/01 and EP/E036252/1) and The University of Sheffield for a fee scholarship for Karunakaran and Ramalingam. The authors declare that they have no conflicts of interest.

Author information

Authors and Affiliations

  1. Department of Chemical and Biological Engineering, ChELSI Institute, The University of Sheffield, Sheffield, S1 3JD, UK

    Esther Karunakaran, Joy Mukherjee, Bharathi Ramalingam & Catherine A. Biggs

Authors
  1. Esther Karunakaran
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joy Mukherjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bharathi Ramalingam
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Catherine A. Biggs
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Catherine A. Biggs.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karunakaran, E., Mukherjee, J., Ramalingam, B. et al. “Biofilmology”: a multidisciplinary review of the study of microbial biofilms. Appl Microbiol Biotechnol 90, 1869–1881 (2011). https://doi.org/10.1007/s00253-011-3293-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-011-3293-4

Keywords

Search

Navigation