Skip to main content

Short Time-Scale Bacterial Adhesion Dynamics

  • Chapter
  • First Online:
Bacterial Adhesion

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 715))

Abstract

In natural conditions many bacterial populations are found as surface-attached communities exhibiting features distinct from those of planktonic cells. We focus here on the question of initial adhesion, the mechanisms of which are still far from being fully understood. Recently, the frontier between microbiologists and physicists has become increasingly permeable, boosting implementation of new methodological approaches for better elucidating the intricate aspects of initial bacterial adhesion. After discussing briefly the main sources of complexity that confuse the understanding of the early steps of cell-surface attachment, we present a selection of physical methods enabling real-time measurement of early adhesion kinetics in live cells. We also discuss the limitations and pitfalls that might appear when applying such methodologies – initially designed for studying physically ideal systems – to analysis of these, more complex, living systems. We address mainly on the use of dispersed-surfaces flow cytometry (DS-FCM), quartz microbalance (QCM) and surface plasmon resonance (SPR) approaches, and give a brief survey of new perspectives in optical microscopy. We conclude that the use of combined and multiparametric technical approaches will lead to significant advances in providing a comprehensive understanding of the early events in bacterial adhesion.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 179.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 229.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agladze K, Jackson D, Romeo T (2003) Periodicity of cell attachment patterns during Escherichia coli biofilm development. J Bacteriol 185:5632–5638

    Article  PubMed  CAS  Google Scholar 

  • Agladze K, Wang X, Romeo T (2005) Spatial periodicity of Escherichia coli K-12 biofilm microstructure initiates during a reversible, polar attachment phase of development and requires the polysaccharide adhesin PGA. J Bacteriol 187:8237–8246

    Article  PubMed  CAS  Google Scholar 

  • Amblard F, Cantin C, Durand J, Fischer A, Sekaly R, Auffray C (1992) New chamber for flow cytometric analysis over an extended range of stream velocity and application to cell adhesion measurements. Cytometry 13:15–22

    Article  PubMed  CAS  Google Scholar 

  • Andersen TE, Kingshott P, Palarasah Y, Benter M, Alei M, Kolmos HJ (2010) A flow chamber assay for quantitative evaluation of bacterial surface colonization used to investigate the influence of temperature and surface hydrophilicity on the biofilm forming capacity of uropathogenic Escherichia coli. J Microbiol Meth 81:135–140

    Article  CAS  Google Scholar 

  • Barnhart MM, Chapman MR (2006) Curli biogenesis and function. Annu Rev Microbiol 60:131–147

    Article  PubMed  CAS  Google Scholar 

  • Beloin C, Houry A, Froment M, Ghigo JM, Henry N (2008) A short-time scale colloidal system reveals early bacterial adhesion dynamics. PLoS Biol 6:e167

    Article  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

    PubMed  CAS  Google Scholar 

  • Bos R, van der Mei HC, Gold J, Busscher HJ (2000) Retention of bacteria on a substratum surface with micro-patterned hydrophobicity. FEMS Microbiol Lett 189:311–315

    Article  PubMed  CAS  Google Scholar 

  • Brehm-Stecher BF, Johnson EA (2004) Single-cell microbiology: tools, technologies, and applications. Microbiol Mol Biol Rev 68:538–559

    Article  PubMed  CAS  Google Scholar 

  • Breznak JA (1984) Activity on surfaces: group report, Dahlem Conference. In: Marshall KC (ed) Microbial adhesion and aggregation. Springer, Berlin, pp 203–221

    Google Scholar 

  • Brooks DE, Trust TJ (1983) Enhancement of bacterial adhesion by shear forces: characterization of the haemagglutination induced by Aeromonas salmonicida strain 438. J Gen Microbiol 129:3661–3669

    PubMed  CAS  Google Scholar 

  • Busscher HJ, van der Mei HC (2006) Microbial adhesion in flow displacement systems. Clin Microbiol Rev 19:127–141

    Article  PubMed  Google Scholar 

  • Chamberlain AHL (1992) The role of adsorbed layers in bacterial adhesion. In: Melo LF, Bott TR, Fletcher M, Capdeville B (eds) Biofilms-science and technology. Kluwer, The Netherlands, pp 59–67

    Google Scholar 

  • Czechowska K, Johnson DR, van der Meer JR (2008) Use of flow cytometric methods for single-cell analysis in environmental microbiology. Curr Opin Microbiol 11:205–212

    Article  PubMed  CAS  Google Scholar 

  • Davey HM, Kell DB (1996) Flow cytometry and cell sorting of heterogeneous microbial populations: the importance of single-cell analyses. Microbiol Rev 60:641–696

    PubMed  CAS  Google Scholar 

  • Davies DG, Geesey GG (1995) Regulation of the alginate biosynthesis gene algC in Pseudomonas aeruginosa during biofilm development in continuous culture. Appl Environ Microbiol 61: 860–867

    PubMed  CAS  Google Scholar 

  • Decher G (1997) Fuzzy nanoassemblies: toward layered polymeric multicomposites. Science 277:1232–1237

    Article  CAS  Google Scholar 

  • Dixon MC (2008) Quartz crystal microbalance with dissipation monitoring: enabling real-time characterization of biological materials and their interactions. J Biomol Tech 19:151–158

    PubMed  Google Scholar 

  • Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881–890

    PubMed  Google Scholar 

  • Dufrêne YF (2003) Recent progress in the application of atomic force microscopy imaging and force spectroscopy to microbiology. Curr Opin Microbiol 6:317–323

    Article  PubMed  Google Scholar 

  • Dunne WM Jr. (2002) Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15:155–166

    Article  PubMed  CAS  Google Scholar 

  • Ebersbach G, Jacobs-Wagner C (2007) Exploration into the spatial and temporal mechanisms of bacterial polarity. Trends Microbiol 15:101–108

    Article  PubMed  CAS  Google Scholar 

  • Ferreira GN, da-Silva AC, Tome B (2009) Acoustic wave biosensors: physical models and biological applications of quartz crystal microbalance. Trends Biotechnol 27:689–697

    Article  PubMed  CAS  Google Scholar 

  • Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP (2009) The bacterial species challenge: making sense of genetic and ecological diversity. Science 323:741–746

    Article  PubMed  CAS  Google Scholar 

  • Frymier PD, Ford RM, Berg HC, Cummings PT (1995) Three-dimensional tracking of motile bacteria near a solid planar surface. Proc Natl Acad Sci USA 92:6195–6199

    Article  PubMed  CAS  Google Scholar 

  • Garland PB (1996) Optical evanescent wave methods for the study of biomolecular interactions. Q Rev Biophys 29:91–117

    Article  PubMed  CAS  Google Scholar 

  • Geesey GG (2001) Bacterial behavior at surfaces. Curr Opin Microbiol 4:296–300

    Article  PubMed  CAS  Google Scholar 

  • Ghigo JM (2003) Are there biofilm-specific physiological pathways beyond a reasonable doubt? Res Microbiol 154:1–8

    Article  PubMed  CAS  Google Scholar 

  • Giepmans BN, Adams SR, Ellisman MH, Tsien RY (2006) The fluorescent toolbox for assessing protein location and function. Science 312:217–224

    Article  PubMed  CAS  Google Scholar 

  • Girard V, Cote JP, Charbonneau ME, Campos M, Berthiaume F, Hancock MA, Siddiqui N, Mourez M (2010) Conformation change in a self-recognizing autotransporter modulate bacterial cell-cell interaction. J Biol Chem 285:10616–10626

    Article  PubMed  CAS  Google Scholar 

  • Gitai Z (2009) New fluorescence microscopy methods for microbiology: sharper, faster, and quantitative. Curr Opin Microbiol 12:341–346

    Article  PubMed  CAS  Google Scholar 

  • Golding I, Paulsson J, Zawilski SM, Cox EC (2005) Real-time kinetics of gene activity in individual bacteria. Cell 123:1025–1036

    Article  PubMed  CAS  Google Scholar 

  • Goller CC, Romeo T (2008) Environmental influences on biofilm development. Curr Top Microbiol Immunol 322:37–66

    Article  PubMed  CAS  Google Scholar 

  • Hoa XD, Kirk AG, Tabrizian M (2007) Towards integrated and sensitive surface plasmon resonance biosensors: a review of recent progress. Biosens Bioelectron 23:151–160

    Article  PubMed  CAS  Google Scholar 

  • Jefferson KK (2004) What drives bacteria to produce a biofilm? FEMS Microbiol Lett 236: 163–173

    PubMed  CAS  Google Scholar 

  • Jenkins AT, Buckling A, McGhee M, Ffrench-Constant RH (2005) Surface plasmon resonance shows that type IV pili are important in surface attachment by Pseudomonas aeruginosa. J R Soc Interface 2:255–259

    Article  PubMed  Google Scholar 

  • Jones TR, Carpenter AE, Lamprecht MR, Moffat J, Silver SJ, Grenier JK, Castoreno AB, Eggert US, Root DE, Golland P, Sabatini DM (2009) Scoring diverse cellular morphologies in image-based screens with iterative feedback and machine learning. Proc Natl Acad Sci USA 106:1826–1831

    Article  PubMed  CAS  Google Scholar 

  • Kaiser D, Yu R (2005) Reversing cell polarity: evidence and hypothesis. Curr Opin Microbiol 8:216–221

    Article  PubMed  CAS  Google Scholar 

  • Kanazawa KK (1997) Mechanical behaviour of films on the quartz microbalance. Faraday Disc 107:77–90

    Article  Google Scholar 

  • Kjaergaard K, Schembri MA, Hasman H, Klemm P (2000) Antigen 43 from Escherichia coli induces inter- and intraspecies cell aggregation and changes in colony morphology of Pseudomonas fluorescens. J Bacteriol 182:4789–4796

    Article  PubMed  CAS  Google Scholar 

  • Klemm P, Schembri MA (2000) Bacterial adhesins: function and structure. Int J Med Microbiol 290:27–35

    PubMed  CAS  Google Scholar 

  • Kogure K, Ikemoto E, Morisaki H (1998) Attachment of Vibrio alginolyticus to glass surfaces is dependent on swimming speed. J Bacteriol 180:932–937

    PubMed  CAS  Google Scholar 

  • Kretschmann E, Raether H (1968) Radiative decay of non-radiative surface plasmons excited by light. Z Naturforsch A 23:2135–2136

    CAS  Google Scholar 

  • Lauga E, Brenner MP, Stone HA (2007) Microfluidics: the no-slip boundary condition. In: Tropea C, Yarin A, Foss JF (eds) Handbook of experimental fluid dynamics. Springer, The Netherlands, isbn: 978-3-540-25141-5. Chap 19:1219–1240

    Google Scholar 

  • Lauga E, DiLuzio WR, Whitesides GM, Stone HA (2006) Swimming in circles: motion of bacteria near solid boundaries. Biophys J 90:400–412

    Article  PubMed  CAS  Google Scholar 

  • Lecuyer S, Rusconi R, Shen Y, Forsyth A, Stone HA (2010) Shear-enhanced adhesion of Pseudomonas aeruginosa. American Physics Society annual meeting, Portland, OR

    Google Scholar 

  • Li ZJ, Mohamed N, Ross JM (2000) Shear stress affects the kinetics of Staphylococcus aureus adhesion to collagen. Biotechnol Prog 16:1086–1090

    Article  PubMed  CAS  Google Scholar 

  • Li G, Tam LK, Tang JX (2008) Amplified effect of Brownian motion in bacterial near-surface swimming. Proc Natl Acad Sci USA 105:18355–18359

    Article  PubMed  CAS  Google Scholar 

  • Ljosa V, Carpenter AE (2009) Introduction to the quantitative analysis of two-dimensional fluorescence microscopy images for cell-based screening. PLoS Comput Biol 5:e1000603

    Article  PubMed  Google Scholar 

  • Locke JC, Elowitz MB (2009) Using movies to analyse gene circuit dynamics in single cells. Nat Rev Microbiol 7:383–392

    Article  PubMed  CAS  Google Scholar 

  • McClaine JW, Ford RM (2002) Reversal of flagellar rotation is important in initial attachment of Escherichia coli to glass in a dynamic system with high- and low-ionic-strength buffers. Appl Environ Microbiol 68:1280–1289

    Article  PubMed  CAS  Google Scholar 

  • Merritt PM, Danhorn T, Fuqua C (2007) Motility and chemotaxis in Agrobacterium tumefaciens surface attachment and biofilm formation. J Bacteriol 189:8005–8014

    Article  PubMed  CAS  Google Scholar 

  • Mohamed N, Teeters MA, Patti JM, Hook M, Ross JM (1999) Inhibition of Staphylococcus aureus adherence to collagen under dynamic conditions. Infect Immun 67:589–594

    PubMed  CAS  Google Scholar 

  • Morisaki H, Nagai S, Ohshima H, Ikemoto E, Kogure K (1999) The effect of motility and cell-surface polymers on bacterial attachment. Microbiology 145(Pt 10):2797–2802

    PubMed  CAS  Google Scholar 

  • Neu TR (1996) Significance of bacterial surface-active compounds in interaction of bacteria with interfaces. Microbiol Rev 60:151–166

    PubMed  CAS  Google Scholar 

  • Oli MW, McArthur WP, Brady LJ (2006) A whole cell BIAcore assay to evaluate P1-mediated adherence of Streptococcus mutans to human salivary agglutinin and inhibition by specific antibodies. J Microbiol Methods 65:503–511

    Article  PubMed  CAS  Google Scholar 

  • Olofsson AC, Hermansson M, Elwing H (2005) Use of a quartz crystal microbalance to investigate the antiadhesive potential of N-acetyl-L-cysteine. Appl Environ Microbiol 71:2705–2712

    Article  PubMed  CAS  Google Scholar 

  • Olsson AL, van der Mei HC, Busscher HJ, Sharma PK (2009) Influence of cell surface appendages on the bacterium-substratum interface measured real-time using QCM-D. Langmuir 25: 1627–1632

    Article  PubMed  CAS  Google Scholar 

  • Otto K (2008) Considering the first steps toward a stable and orderly way of bacterial life. PLoS Biol 6:e180

    Article  PubMed  Google Scholar 

  • Otto K, Elwing H, Hermansson M (1999) Effect of ionic strength on initial interactions of Escherichia coli with surfaces, studied on-line by a novel quartz crystal microbalance technique. J Bacteriol 181:5210–5218

    PubMed  CAS  Google Scholar 

  • Otto K, Hermansson M (2004) Inactivation of ompX causes increased interactions of type 1 fimbriated Escherichia coli with abiotic surfaces. J Bacteriol 186:226–234

    Article  PubMed  CAS  Google Scholar 

  • O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79

    Article  PubMed  Google Scholar 

  • Palmer J, Flint S, Brooks J (2007) Bacterial cell attachment, the beginning of a biofilm. J Ind Microbiol Biotechnol 34:577–588

    Article  PubMed  CAS  Google Scholar 

  • Pourshafie MR, Marklund BI, Ohlson S (2004) Binding interactions of Escherichia coli with globotetraosylceramide (globoside) using a surface plasmon resonance biosensor. J Microbiol Methods 58:313–320

    Article  PubMed  CAS  Google Scholar 

  • Prigent-Combaret C, Vidal O, Dorel C, Lejeune P (1999) Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J Bacteriol 181:5993–6002

    PubMed  CAS  Google Scholar 

  • Radcliff G, Jaroszeski MJ (1998) Basics of flow cytometry. Meth Mol Biol 91:1–24

    CAS  Google Scholar 

  • Salminen A, Loimaranta V, Joosten JA, Khan AS, Hacker J, Pieters RJ, Finne J (2007) Inhibition of P-fimbriated Escherichia coli adhesion by multivalent galabiose derivatives studied by a live-bacteria application of surface plasmon resonance. J Antimicrob Chemother 60:495–501

    Article  PubMed  CAS  Google Scholar 

  • Sasahara K, Zottola C, EA (1993) Biofilm formation by Listeria monocytogenes utilizes a primary colonizing microorganism in flowing systems. J. Food Protect 56:1022–1028

    Google Scholar 

  • Sauerbrey GZ (1959) Use of quartz vibrator for weighing thin films on a microbalance. Z Phys 155:206–222

    Article  CAS  Google Scholar 

  • Schembri MA, Hjerrild L, Gjermansen M, Klemm P (2003) Differential expression of the Escherichia coli autoaggregation factor antigen 43. J Bacteriol 185:2236–2242

    Article  PubMed  CAS  Google Scholar 

  • Schuck P (1997) Reliable determination of binding affinity and kinetics using surface plasmon resonance biosensors. Curr Opin Biotechnol 8:498–502

    Article  PubMed  CAS  Google Scholar 

  • Shapiro HM (2000) Microbial analysis at the single-cell level: tasks and techniques. J Microbiol Methods 42:3–16

    Article  PubMed  CAS  Google Scholar 

  • Shen Z, Huang M, Xiao C, Zhang Y, Zeng X, Wang PG (2007) Nonlabeled quartz crystal microbalance biosensor for bacterial detection using carbohydrate and lectin recognitions. Anal Chem 79:2312–2319

    Article  PubMed  CAS  Google Scholar 

  • Sherlock O, Schembri MA, Reisner A, Klemm P (2004) Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: cell aggregation and biofilm formation. J Bacteriol 186:8058–8065

    Google Scholar 

  • Shive MS, Hasan SM, Anderson JM (1999) Shear stress effects on bacterial adhesion, leukocyte adhesion, and leukocyte oxidative capacity on a polyetherurethane. J Biomed Mater Res 46:511–519

    Article  PubMed  CAS  Google Scholar 

  • Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358:135–138

    Article  PubMed  CAS  Google Scholar 

  • Thomas WE, Nilsson LM, Forero M, Sokurenko EV, Vogel V (2004) Shear-dependent ‘stick-and-roll’ adhesion of type 1 fimbriated Escherichia coli. Mol Microbiol 53:1545–1557

    Article  PubMed  CAS  Google Scholar 

  • Thomas WE, Trintchina E, Forero M, Vogel V, Sokurenko EV (2002) Bacterial adhesion to target cells enhanced by shear force. Cell 109:913–923

    Article  PubMed  CAS  Google Scholar 

  • Thomas WE, Vogel V, Sokurenko E (2008) Biophysics of catch bonds. Annu Rev Biophys 37: 399–416

    Article  PubMed  CAS  Google Scholar 

  • Trache A, Meininger GA (2008) Total internal reflection fluorescence (TIRF) microscopy. Curr Protoc Microbiol Chapter 2:Unit 2A 2 1–2A 2 22

    PubMed  Google Scholar 

  • Valle J, Da Re S, Henry N, Fontaine T, Balestrino D, Latour-Lambert P, Ghigo JM (2006) Broad-spectrum biofilm inhibition by a secreted bacterial polysaccharide. Proc Natl Acad Sci USA 103:12558–12563

    Article  PubMed  CAS  Google Scholar 

  • van Loosdrecht MC, Lyklema J, Norde W, Zehnder AJ (1990) Influence of interfaces on microbial activity. Microbiol Rev 54:75–87

    PubMed  Google Scholar 

  • Vigeant MA, Ford RM (1997) Interactions between motile Escherichia coli and glass in media with various ionic strengths, as observed with a three-dimensional-tracking microscope. Appl Environ Microbiol 63:3474–3479

    PubMed  CAS  Google Scholar 

  • Vigeant MA, Ford RM, Wagner M, Tamm LK (2002) Reversible and irreversible adhesion of motile Escherichia coli cells analyzed by total internal reflection aqueous fluorescence microscopy. Appl Environ Microbiol 68:2794–2801

    Article  PubMed  CAS  Google Scholar 

  • Vigeant MA, Wagner M, Tamm LK, Ford RM (2001) Nanometer distances between swimming bacteria and surfaces measured by total internal reflection aqueous fluorescence microscopy. Langmuir 17:2235–2242

    Article  CAS  Google Scholar 

  • Wang IW, Anderson JM, Jacobs MR, Marchant RE (1995) Adhesion of Staphylococcus epidermidis to biomedical polymers: contributions of surface thermodynamics and hemodynamic shear conditions. J Biomed Mater Res 29:485–493

    Article  PubMed  CAS  Google Scholar 

  • Watnick P, Kolter R (2000) Biofilm, city of microbes. J Bacteriol 182:2675–2679

    Article  PubMed  CAS  Google Scholar 

  • Zobell CE (1943) The effect of solid surfaces upon bacterial activity. J Bacteriol 46:39–56

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nelly Henry .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Geng, J., Henry, N. (2011). Short Time-Scale Bacterial Adhesion Dynamics. In: Linke, D., Goldman, A. (eds) Bacterial Adhesion. Advances in Experimental Medicine and Biology, vol 715. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0940-9_20

Download citation

Publish with us

Policies and ethics