Chapter 21 : Biofilms

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This chapter discusses specific triggers of biofilm formation and how survival in these multicellular communities affects the physiology of the constituent cells. The ability of bacteria to adhere to and form biofilms on virtually every surface makes it particularly important that we understand the mechanisms underlying this sedentary lifestyle. The molecular mechanisms necessary for the formation of biofilms varies from species to species. There is a vast array of research on biofilm communities, but this chapter focuses on a few model organisms to illustrate major similarities and differences between species. Biofilms contain large numbers of cells and, quite importantly, these populations are phenotypically heterogeneous. Cells within the biofilm are constantly consuming available resources and can form structures with a depth of hundreds of microns or more. Stochastic gene expression inherent to individual bacterial cells also adds to the complex distribution of phenotypes of individual cells within a biofilm. Cyclic di-guanosine monophosphate (c-di-GMP) is a second messenger that is important in regulating the transition from a planktonic to biofilm lifestyle in many organisms. Secondary metabolites include most antibiotics and/or pigments and are generally produced during stationary phase as nutrients become depleted. Phenazine mutant colonies have been shown to bind the dye congo red, which is known to specifically interact with the Pel exopolysaccharide in .

Citation: Vlamakis H, Kolter R. 2011. Biofilms, p 365-373. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch21
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Image of Figure 1.
Figure 1.

Side view of a vertically thin sectioned colony biofilm from strain NCIB 3610 cells harboring transcriptional reporters for cell type-specific promoters. Shown are overlays of transmitted light and fluorescence images. Top panel: motility (P-, colored blue) and sporulation (P-, colored yellow). Bottom panel: matrix production (P-, colored red) and sporulation (P-, colored green). The edge of the colony is on the left and the agar is at the bottom of the image. Colonies were initiated from single cells and grown on an agar surface for 72 hours at 30°C prior to sectioning. Bar is 50 µm.

Citation: Vlamakis H, Kolter R. 2011. Biofilms, p 365-373. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch21
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1. An, D., and, M.R. Parsek. 2007. The promise and peril of transcriptional profiling in biofilm communities. Curr. Opin. Microbiol. 10: 292296.
2. Anderson, G. G., and, G.A. O’Toole. 2008. Innate and induced resistance mechanisms of bacterial biofilms, P. 85105. In T. Romeo (ed.), Bacterial Biofilms. Springer, Heidelberg, Germany.
3. Bagge, N.,, M. Schuster,, M. Hentzer,, O. Ciofu,, M. Givskov,, E. P. Greenberg,, and N. Hoiby. 2004. Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and beta-lactamase and alginate production. Anti-microb. Agents Chemother. 48: 11751187.
4. Barken, K. B.,, S.J. Pamp,, L. Yang,, M. Gjermansen,, J. J. Bertrand,, M. Klausen,, M. Givskov,, C. B. Whitchurch,, J. N. Engel,, and T. Tolker-Nielsen. 2008. Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environ. Microbiol. 10: 23312343.
5. Beloin, C., A. Roux, and, J.M. Ghigo. 2008. Escherichia coli biofilms, P. 249289. In T. Romeo (ed.), Bacterial Biofilms. Springer, Heidelberg, Germany.
6. Branda, S. S.,, J.E. Gonzalez-Pastor,, S. Ben-Yehuda,, R. Losick,, and R. Kolter. 2001. Fruiting body formation by Bacillus subtilis. Proc. Natl. Acad. Sci. USA 98: 1162111626.
7. Branda, S. S.,, S. Vik,, L. Friedman, and, R. Kolter. 2005. Biofilms: the matrix revisited. Trends Microbiol. 13: 2026.
8. Cotter, P. A., and, S. Stibitz. 2007. c-di-GMP-mediated regulation of virulence and biofilm formation. Curr. Opin. Microbiol. 10: 1723.
9. Currie, C. R. 2001. A community of ants, fungi, and bacteria: a multilateral approach to studying symbiosis. Annu. Rev. Microbiol. 55: 357380.
10. Danhorn, T., and, C. Fuqua. 2007. Biofilm formation by plantassociated bacteria. Annu. Rev. Microbiol. 61: 401422.
11. de Beer, D.,, P. Stoodley,, F. Roe, and, Z. Lewandowski. 1994. Effects of biofilm structures on oxygen distribution and mass transport. Biotechnol. Bioeng. 43: 11311138.
12. de Carvalho, C. C. 2007. Biofilms: recent developments on an old battle. Recent Pat. Biotechnol. 1: 4957.
13. Dietrich, L. E.,, A. Price-Whelan, A. Petersen,, M. Whiteley, and, D.K. Newman. 2006. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol. Microbiol. 61: 13081321.
14. Dietrich, L. E.,, T.K. Teal,, A. Price-Whelan, and, D.K. Newman. 2008. Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321: 12031206.
15. Donlan, R. M. 2008. Biofilms on central venous catheters: is eradication possible? Curr. Top. Microbiol. Immunol. 322: 133161.
16. Dubnau, D., and, R. Losick. 2006. Bistability in bacteria. Mol. Microbiol. 61: 564572.
17. Dupraz, C., and, P.T. Visscher. 2005. Microbial lithification in marine stromatolites and hypersaline mats. Trends Microbiol. 13: 429438.
18. Friedman, L., and, R. Kolter. 2004. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J. Bacteriol. 186: 44574465.
19. Fujita, M.,, J.E. Gonzalez-Pastor, and, R. Losick. 2005. High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J. Bacteriol. 187: 13571368.
20. Fux, C. A.,, J.W. Costerton,, P.S. Stewart,, and P. Stoodley. 2005. Survival strategies of infectious biofilms. Trends Microbiol. 13: 3440.
21. Goller, C. C., and, T. Romeo. 2008. Environmental influences on biofilm development, P. 3766. In T. Romeo (ed.), Bacterial Biofilms. Springer, Heidelberg, Germany.
22. Hall-Stoodley, L.,, J.W. Costerton, and, P. Stoodley. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2: 95108.
23. Hall-Stoodley, L., and, P. Stoodley. 2009. Evolving concepts in biofilm infections. Cell. Microbiol. 11: 10341043.
24. Hatt, J. K., and, P.N. Rather. 2008. Role of bacterial biofilms in urinary tract infections, P. 163192. In T. Romeo (ed.), Bactarial Biofilms. Springer, Heidelberg, Germany.
25. Hengge, R. 2009. Principles of c-di-GMP signalling in bacteria. Nat. Rev. Microbiol. 7: 263273.
26. Hernandez, M. E., and, D.K. Newman. 2001. Extracellular electron transfer. Cell. Mol. Life Sci. 58: 15621571.
27. Hickman, J. W., and, C.S. Harwood. 2008. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol. Microbiol. 69: 376389.
28. Hoffman, L. R.,, D.A. D’Argenio,, M.J. MacCoss, Z., Zhang, R., A. Jones, and, S.I. Miller. 2005. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436: 11711175.
29. Jackson, D. W.,, K. Suzuki,, L. Oakford,, J.W. Simecka,, M. E. Hart,, and T. Romeo. 2002. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J. Bacteriol. 184: 290301.
30. Jenal, U., and, J. Malone. 2006. Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet. 40: 385407.
31. Jiang, M.,, W. Shao,, M. Perego, and, J.A. Hoch. 2000. Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol. Microbiol. 38: 535542.
32. Kearns, D. B.,, F. Chu,, S. S. Branda,, R. Kolter,, and R. Losick. 2005. A master regulator for biofilm formation by Bacillus subtilis. Mol. Microbiol. 55: 739749.
33. Klausen, M.,, A. Heydorn,, P. Ragas,, L. Lambertsen,, A. Aaes-Jorgensen,, S. Molin,, and T. Tolker-Nielsen. 2003. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol. Microbiol. 48: 15111524.
34. Kulasakara, H.,, V. Lee,, A. Brencic,, N. Liberati,, J. Urbach,, S. Miyata,, D. G. Lee,, A. N. Neely,, M. Hyodo,, Y. Hayakawa,, F. M. Ausubel,, and S. Lory. 2006. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3'-5')-cyclic-GMP in virulence. Proc. Natl. Acad. Sci. USA 103: 28392844.
35. Landini, P. 2009. Cross-talk mechanisms in biofilm formation and responses to environmental and physiological stress in Escherichia coli. Res. Microbiol. 160: 259266.
36. Lasa, I., and, J.R. Penades. 2006. Bap: a family of surface proteins involved in biofilm formation. Res. Microbiol. 157: 99107.
37. Lee, V. T.,, J.M. Matewish,, J.L. Kessler,, M. Hyodo,, Y. Hayakawa,, and S. Lory. 2007. A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol. Microbiol. 65: 14741484.
38. Lemon, K. P.,, A.M. Earl,, H.C. Vlamakis,, C. Aguilar,, and R. Kolter. 2008. Biofilm development with an emphasis on Bacillus subtilis, P. 116. In T. Romeo (ed.), Bacterial Biofilms. Springer, Heidelberg, Germany.
39. Lenz, A. P.,, K.S. Williamson,, B. Pitts,, P. S. Stewart, and, M.J. Franklin. 2008. Localized gene expression in Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 74: 44634471.
40. Lewis, K. 2005. Persister cells and the riddle of biofilm survival. Biochemistry (Moscow) 70: 267274.
41. Lopez, D., H. Vlamakis, and, R. Kolter. 2009a. Generation of multiple cell types in Bacillus subtilis. FEMS Microbiol. Rev. 33: 152163.
42. Lopez, D.,, M.A. Fischbach,, F. Chu,, R. Losick,, and R. Kolter. 2009b. Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 106: 280285.
43. Mack, D.,, P. Becker,, I. Chatterjee,, S. Dobinsky,, J.K. Knobloch,, G. Peters,, H. Rohde,, and M. Herrmann. 2004. Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: functional molecules, regulatory circuits, and adaptive responses. Int. J. Med. Microbiol. 294: 203212.
44. Mah, T. F., and, G.A. O’Toole. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9: 3439.
45. Matz, C., and, S. Kjelleberg. 2005. Off the hook—how bacteria survive protozoan grazing. Trends Microbiol. 13: 302307.
46. Monds, R. D., and, G.A. O’Toole. 2009. The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol. 17: 7387.
47. O’Gara, J. P. 2007. ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol. Lett. 270: 179188.
48. O’Gara, J. P., and, H. Humphreys. 2001. Staphylococcus epidermidis biofilms: importance and implications. J. Med. Microbiol. 50: 582587.
49. O’Toole, G. A., and, R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30: 295304.
50. Otto, M. 2008. Staphylococcal biofilms, P. 207228. In T. Romeo (ed.), Bacterial Biofilms. Springer, Heidelberg, Germany.
51. Phillips, Z. E., and, M.A. Strauch. 2002. Bacillus subtilis sporulation and stationary phase gene expression. Cell. Mol. Life Sci. 59: 392402.
52. Piggot, P. J., and, D.W. Hilbert. 2004. Sporulation of Bacillus subtilis. Curr. Opin. Microbiol. 7: 579586.
53. Pratt, L. A., and, R. Kolter. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 30: 285293.
54. Price-Whelan, A.,, L. E. Dietrich, and, D.K. Newman. 2006. Rethinking ‘secondary’ metabolism: physiological roles for phenazine antibiotics. Nat. Chem. Biol. 2: 7178.
55. Rani, S. A.,, B. Pitts,, H. Beyenal,, R.A. Veluchamy,, Z. Lewandowski,, W.M. Davison,, K. Buckingham-Meyer, and, P.S. Stewart. 2007. Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J. Bacteriol. 189: 42234233.
56. Rice, K. C.,, E.E. Mann,, J.L. Endres, E. C., Weiss, J.E., Cassat, M., S. Smeltzer, and, K.W. Bayles. 2007. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 104: 81138118.
57. Ryder, C., M. Byrd, and, D.J. Wozniak. 2007. Role of polysaccharides in Pseudomonas aeruginosa biofilm development. Curr. Opin. Microbiol. 10: 644648.
58. Spormann, A. M. 2008. Physiology of microbes in biofilms, P. 1736. In T. Romeo (ed.), Bacterial Biofilms. Springer, Heidelberg, Germany.
59. Stein, T. 2005. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol. Microbiol. 56: 845857.
60. Stewart, P. S., and, M.J. Franklin. 2008. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6: 199210.
61. Sudarsan, N.,, E.R. Lee,, Z. Weinberg, R. H. Moy,, J.N. Kim, K. H. Link, and, R.R. Breaker. 2008. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321: 411413.
62. Tart, A. H., and, D.J. Wozniak. 2008. Shifting paradigms in Pseudomonas aeruginosa biofilm research, P. 193206. In T. Romeo (ed.), Bacterial Biofilms. Springer, Heidelberg, Germany.
63. Vallet, I.,, J.W. Olson,, S. Lory, A. Lazdunski, and, A. Filloux. 2001. The chaperone/usher pathways of Pseudomonas aeruginosa: identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proc. Natl. Acad. Sci. USA 98: 69116916.
64. Veening, J. W.,, O.P. Kuipers,, S. Brul,, K. J. Hellingwerf,, and R. Kort. 2006. Effects of phosphorelay perturbations on architecture, sporulation, and spore resistance in biofilms of Bacillus subtilis. J. Bacteriol. 188: 30993109.
65. Vlamakis, H.,, C. Aguilar,, R. Losick, and, R. Kolter. 2008. Control of cell fate by the formation of an architecturally complex bacterial community. Genes Dev. 22: 945953.
66. Wang, X.,, J.F. Preston 3rd, and, T. Romeo. 2004. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J. Bacteriol. 186: 27242734.
67. Watnick, P. I.,, C.M. Lauriano,, K.E. Klose,, L. Croal,, and R. Kolter. 2001. The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Mol. Microbiol. 39: 223235.
68. Weinberg, Z.,, J.E. Barrick,, Z. Yao,, A. Roth,, J.N. Kim,, J. Gore,, J. X. Wang,, E. R. Lee,, K. F. Block,, N. Sudarsan,, S. Neph,, M. Tompa,, W. L. Ruzzo, and, R.R. Breaker. 2007. Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Res. 35: 48094819.
69. Wood, T. K. 2009. Insights on Escherichia coli biofilm formation and inhibition from whole-transcriptome profiling. Environ. Microbiol. 11: 115.
70. Xu, K. D.,, P.S. Stewart,, F. Xia, C. T. Huang, and, G.A. McFeters. 1998. Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl. Environ. Microbiol. 64: 40354039.
71. Yildiz, F. H., and, K.L. Visick. 2009. Vibrio biofilms: so much the same yet so different. Trends Microbiol. 17: 109118.
72. Yim, G.,, H.H. Wang, and, J. Davies. 2007. Antibiotics as signalling molecules. Philos. Trans. R. Soc. Lond. B 362: 11951200.


Generic image for table
Table 1.

Features of biofilms for model organisms

Citation: Vlamakis H, Kolter R. 2011. Biofilms, p 365-373. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch21

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