Chapter 2 : Multicellularity and Biofilms

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

Multicellularity and Biofilms, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817718/9781555818944_Chap02-1.gif /docserver/preview/fulltext/10.1128/9781555817718/9781555818944_Chap02-2.gif


The authors argue that multicellularity is chiefly characterized by extensive intercellular interactions that lead to coordination of the cells’ activities. They also argue that the evidence collected on biofilms thus far only partially supports the assertion that biofilms are multicellular organisms. In addition to extensive intercellular interactions, the classical examples of bacterial multicellularity also feature coordination of the activities of constituent cells. The chapter focuses on multicellularity of biofilms. Intercellular signaling is likely involved in establishing the division of labor, because quorum-sensing signals are known to be required for efficient sporulation. This division of labor could benefit the biofilm as a whole, because one can speculate that fruiting bodies play a role in spore dispersal, a function proposed for myxococcal fruiting bodies and the aerial hyphae of streptomycetes. In this way biofilms can be said to show all the features characteristic of multicellularity: intercellular interactions that lead to a coordination of cell activities that benefits the community. Perhaps the most daunting challenge in studies relating to bacterial multicellularity will be to determine whether an observed coordination of cell activities actually benefits the biofilm community as a whole. In large part, this is because biofilms typically lack an obvious function. A potential solution to this problem is suggested by the observation that terminal differentiation is a feature common to several of the examples of bacterial multicellularity discussed in this chapter (e.g., heterocysts, aerial hyphae, and myxobacterial fruiting bodies).

Citation: Branda S, Kolter R. 2004. Multicellularity and Biofilms, p 20-29. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch2
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


1. Adams, D. G., 2000. Cyanobacterial phylogeny and development: questions and challenges, p. 5181. In Y. V. Brun, and L. J. Shimkets (ed.), Prokaryotic Development. ASM Press, Washington, D.C.
2. Andersen, J. B.,, A. Heydorn,, M. Hentzer,, L. Eberl,, O. Geisenberger,, B. B. Christensen,, S. Molin,, and M. Givskov. 2001. gfp-based N-acyl homoserine-lactone sensor systems for detection of bacterial communication. Appl. Environ. Microbiol. 67:575585.
3. Arnold, J. W.,, and L. J. Shimkets. 1988. Cell surface properties correlated with cohesion in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 170:57715777.
4. Bassler, B. L. 1999. How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr. Opin. Microbiol. 2:582587.
5. Behmlander, R. M.,, and M. Dworkin. 1994. Biochemical and structural analyses of the extracellular matrix fibrils of Myxococcus xanthus. J. Bacteriol. 176:62956303.
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. Burchard, R. P. 1982. Trail following by gliding bacteria. J. Bacteriol. 152:495501.
8. Burkholder, W. F.,, and A. D. Grossman,. 2000. Regulation of the initiation of endospore formation in Bacillus subtilis, p. 151166. In Y. V. Brun, and L. J. Shimkets (ed.), Prokaryotic Development. ASM Press, Washington, D.C.
9. Champness, W., 2000. Actinomycete development, antibiotic production, and phylogeny: questions and challenges, p. 1131. In Y. V. Brun, and L. J. Shimkets (ed.), Prokaryotic Development. ASM Press, Washington, D.C.
10. Charlton, T. S.,, R. de Nys,, A. Netting,, N. Kumar,, M. Hentzer,, M. Givskov,, and S. Kjelleberg. 2000. A novel and sensitive method for the quantification of N-3-oxoacyl homoserine lactones using gas chromatography-mass spectrometry: application to a model bacterial biofilm. Environ. Microbiol. 2:530541.
11. Chater, K. F., 2000. Developmental decisions during sporulation in the aerial mycelium in Streptomyces, p. 3348. In Y. V. Brun, and L. J. Shimkets (ed.), Prokaryotic Development. ASM Press, Washington, D.C.
12. Costerton, J. W.,, Z. Lewandowski,, D. E. Caldwell,, D. R. Korber,, and H. M. Lappin-Scott. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711745.
13. Costerton, J. W.,, P. S. Stewart,, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:13181322.
14. Crespie, B. J. 2001. The evolution of social behavior in microorganisms. Trends Ecol. Evol. 16:178183.
15. Davey, M. E.,, and G. A. O’Toole. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64:847867.
16. Davies, D. G.,, M. R. Parsek,, J. P. Pearson,, B. H. Iglewski,, J. W. Costerton,, and E. P. Greenberg. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295298.
17. De Beer, D.,, P. Stoodley,, and Z. Lewandowski. 1994. Effects of biofilm structures on oxygen distribution and mass transport. Biotechnol. Bioeng. 43:11311138.
18. De Kievit, T. R.,, R. Gillis,, S. Marx,, C. Brown,, and B. H. Iglewski. 2001. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl. Environ. Microbiol. 67:18651873.
19. Dobson, W. J.,, H. D. McCurdy,, and T. H. MacRae. 1979. The function of fimbrae in Myxococcus xanthus. II. The role of fimbrae in cell-cell interactions. Can. J. Microbiol. 25:13591372.
20. Dworkin, M. 1999. Fibrils as extracellular appendages of bacteria: their role in contact-mediated cell-cell interactions in Myxococcus xanthus. Bioessays 20:590595.
21. Dworkin, M., 2000. Introduction to the myxobacteria, p. 221242. In Y. V. Brun, and L. J. Shimkets (ed.), Prokaryotic Development. ASM Press, Washington, D.C.
22. Fenchel, T. 2002. Microbial behavior in a heterogeneous world. Science 296:10681071.
23. Frank, S. A. 1998. Foundations of Social Evolution. Princeton University Press, Princeton, N.J.
24. Hentzer, M.,, K. Riedel,, T. B. Rasmussen,, A. Heydorn,, J. B. Anderson,, M. R. Parsek,, S. A. Rice,, L. Eberl,, S. Molin,, N. Hoiby,, S. Kjelleberg,, and M. Givskov. 2002. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148:87102.
25. Huber, B.,, K. Riedel,, M. Hentzer,, A. Heydorn,, A. Gotschlich,, M. Givskov,, S. Molin,, and L. Eberl. 2001. The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147:25172528.
26. Jelsbak, L.,, and L. Sogaard-Andersen. 2000. Pattern formation: fruiting body morphogenesis in Myxococcus xanthus. Curr. Opin. Microbiol. 3:637642.
27. Kaiser, D. 1979. Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 76:59525956.
28. Kaiser, D., 2000. Cell-interactive sensing of the environment, p. 263275. In Y. V. Brun, and L. J. Shimkets (ed.), Prokaryotic Development. ASM Press, Washington, D.C.
29. Kim, S. K.,, and D. Kaiser. 1991. C-factor has distinct aggregation and sporulation thresholds during Myxococcus development. J. Bacteriol. 173:17221728.
30. Kjelleberg, S.,, and S. Molin. 2002. Is there a role for quorum sensing signals in bacterial biofilms? Curr. Opin. Microbiol. 5:254258.
31. Kolenbrander, P. E. 2000. Oral microbial communities: biofilms, interactions, and genetic systems. Annu. Rev. Microbiol. 54:413437.
32. Kruse, T.,, S. Lobendanz,, N. M. S. Berthelsen,, and L. Sogaard-Andersen. 2001. C-signal: a cell surface-associated morphogen that induces and co-ordinates multicellular fruiting body morphogenesis and sporulation in Myxococcus xanthus. Mol.Microbiol. 40:156168.
33. Lewis, K. 2000. Programmed death in bacteria. Microbiol. Mol. Biol. Rev. 64:503514.
34. Li, S.,, B.-U. Lee,, and L. J. Shimkets. 1992. csgA expression entrains Myxococcus xanthus development. Genes Dev. 6:401410.
35. Li, Y.,, H. Sun,, X. Ma,, A. Lu,, R. Lux,, D. Zusman,, and W. Shi. 2003. Extracellular polysaccharides mediate pilus retraction during social motility of Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 100:54435448.
36. Li, Y.-H.,, N. Tang,, M. B. Aspiras,, P. C. Y. Lau,, J. H. Lee,, R. P. Ellen,, and D. G. Cvitkovitch. 2002. A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J. Bacteriol. 184:26992708.
37. Loo, C. Y.,, D. A. Corliss,, and N. Ganeshkumar. 2000. Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J. Bacteriol. 182:13741382.
38. Lynch, M. J.,, S. Swift,, D. F. Kirke,, C. W. Keevil,, C. E. R. Dodd,, and P. Williams. 2002. The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ. Microbiol. 4:1828.
39. MacNeil, S. D.,, F. Clara,, and P. L. Hartzell. 1994. Genes required for both gliding motility and development in Myxococcus xanthus. Mol. Microbiol. 14:785795.
40. Mattick, J. S. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56:289314.
41. McLean, R. J. C.,, M. Whiteley,, D. J. Stickler,, and C. Fuqua. 1997. Evidence of autoinducer activity in naturally occurring biofilms. FEMS Microbiol. Lett. 154:259263.
42. McNab, R.,, S. K. Ford,, A. El-Sabaeny,, B. Barbieri,, G. S. Cook,, and R. J. Lamont. 2003. LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J. Bacteriol. 185:274278.
43. Méndez, C.,, A. F. Braña,, M. B. Manzanal,, and C. Hardisson. 1985. Role of substrate mycelium in colony development in Streptomyces. Can. J. Microbiol. 31:446450.
44. Merritt, J.,, F. Qi,, S. D. Goodman,, M. H. Anderson,, and W. Shi. 2003. Mutation of luxS affects biofilm formation in Streptococcus mutans. Infect. Immun. 71:19721979.
45. Merz, A.,, M. Sheetz,, and M. So. 2000. Pilus retraction powers bacterial twitching motility. Nature 407:98102.
46. Michod, R. E.,, and D. Roze. 2001. Cooperation and conflict in the evolution of multicellularity. Heredity 86:17.
47. Moller, S.,, C. Sternberg,, J. B. Andersen,, B. B. Christensen,, J. L. Ramos,, M. Givskov,, and S. Molin. 1998. In situ gene expression in mixed-culture biofilms: evidence of metabolic interactions between community members. Appl. Environ. Microbiol. 64:721732.
48. Nielsen, A. T.,, T. Tolker-Nielsen,, K. B. Barken,, and S. Molin. 2000. Role of commensal relationships on the spatial structure of a surface-attached microbial consortium. Environ. Microbiol. 2:5968.
49. Nodwell, J. R.,, and R. Losick. 1998. Purification of an extracellular signaling molecule involved in production of aerial mycelium by Streptomyces coelicolor. J. Bacteriol. 180:13341337.
50. O’Toole, G.,, H. B. Kaplan,, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:4979.
51. O’Toole, G. A.,, and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295304.
52. Pierson, E. A.,, D. W. Wood,, J. A. Cannon,, F. M. Blachere,, and L. S. Pierson III. 1998. Interpopulation signaling via N-acyl-homoserine lactones among bacteria in the wheat rhizosphere. Mol. Plant-Microbe Interact. 11:10781084.
53. Pratten, J.,, S. J. Foster,, P. F. Chan,, M. Wilson,, and S. P. Nair. 2001. Staphylococcus aureus accessory regulators: expression within biofilms and effect on adhesion. Microb. Infect. 3:633637.
54. Prouty, A. M.,, W. H. Schwesinger,, and J. S. Gunn. 2002. Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect. Immun. 70:26402649.
55. Riedel, K.,, M. Hentzer,, O. Geisenberger,, B. Huber,, A. Steidle,, H. Wu,, N. Hoiby,, M. Givskov,, S. Molin,, and L. Eberl. 2001. N-Acylhomoserine- lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147:32493262.
56. Rosenbluh, A.,, and M. Eisenbach. 1992. Effect of mechanical removal of pili on gliding motility of Myxococcus xanthus. J. Bacteriol. 174:54065413.
57. Sauer, K.,, A. K. Camper,, G. D. Ehrlich,, J. W. Costerton,, and D. G. Davies. 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184:11401154.
58. Shapiro, J. A. 1998. Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52:81104.
59. Shapiro, J. A.,, and M. Dworkin. 1997. Bacteria as Multicellular Organisms. Oxford University Press, New York, N.Y.
60. Shimkets, L. J. 1990. Social and developmental biology of the myxobacteria. Microbiol. Rev. 54:473501.
61. Shimkets, L. J. 1999. Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu. Rev. Microbiol. 53:525549.
62. Skerker, J. M.,, and H. C. Berg. 2001. Direct observation of extension and retraction of type IV pili. Proc. Natl. Acad. Sci. USA 98:69016904.
63. Spormann, A. M. 1999. Gliding motility in bacteria: insights from studies of Myxococcus xanthus. Microbiol. Mol. Biol. Rev. 63:621641.
64. Steidle, A.,, K. Sigl,, R. Schuhegger,, A. Ihring,, M. Schmid,, S. Gantner,, M. Stoffels,, K. Riedel,, M. Givskov,, A. Hartmann,, C. Langebartels,, and L. Eberl. 2001. Visualization of N-acylhomoserine lactone-mediated cell-cell communication between bacteria colonizing the tomato rhizosphere. Appl. Environ. Microbiol. 67: 57615770.
65. Stickler, D. J.,, N. S. Morris,, R. J. C. McLean,, and C. Fuqua. 1998. Biofilms on indwelling urethral catheters produce quorum sensing signal molecules in situ and in vitro. Appl. Environ. Microbiol. 64:34863490.
66. Sun, H.,, Z. Yang,, and W. Shi. 1999. Effect of cellular filamentation on adventurous and social gliding motility of Myxococcus xanthus. Proc. Natl. Acad. Sci.USA 96:1517815183.
67. Sutherland, I. W. 2001. Exopolysaccharides in biofilms, flocs, and related structures. Water Sci. Technol. 43:7786.
68. Takano, E.,, R. Chakraburtty,, T. Nihira,, Y. Yamada,, and M. J. Bibb. 2001. A complex role for the gamma-butyrolactone SCB1 in regulating antibiotic production in Streptomyces coelicolor A3(2). Mol. Microbiol. 41:10151028.
69. Takano, E.,, T. Nihira,, Y. Hara,, J. J. Jones,, C. J. Gershater,, Y. Yamada,, and M. J. Bibb. 2000. Purification and structural determination of SCB1, a gamma-butyrolactone that elicits antibiotic production in Streptomyces coelicolor A3(2). J. Biol. Chem. 275:1101011016.
70. Velicier, G. J. 2003. Social strife in the microbial world. Trends Microbiol. 11:330337.
71. Vroom, J. M.,, K. J. De Grauw,, H. C. Gerritsen,, D. J. Bradshaw,, P. D. Marsh,, G. K. Watson,, J. J. Birmingham,, and C. Allison. 1999. Depth penetration and detection of pH gradients in biofilms by two-photon excitation microscopy. Appl. Environ. Microbiol. 65:35023511.
72. Webb, J. S.,, L. S. Thompson,, S. James,, T. S. Charlton,, T. Tolker-Nielsen,, B. Koch,, M. Givskov,, and S. Kjelleberg. 2003. Cell death in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 185:45854592.
73. Wimpenny, J.,, W. Manz,, and U. Szewzyk. 2000. Heterogeneity in biofilms. FEMS Microbiol. Rev. 24:661671.
74. Wolfaardt, G. M.,, J. R. Lawrence,, R. D. Robarts,, and D. E. Caldwell. 1994. Multicellular organization in a degradative biofilm community. Appl. Environ. Microbiol. 60:434446.
75. Wolk, C. P., 2000. Heterocyst formation in Anabaena, p. 83104. In Y. V. Brun, and L. J. Shimkets (ed.), Prokaryotic Development. ASM Press, Washington, D.C.
76. Wu, S. S.,, and D. Kaiser. 1995. Genetic and functional evidence that Type IV pili are required for social gliding motility in Myxococcus xanthus. Mol. Microbiol. 18:547558.
77. Yoon, H.-S.,, and J. W. Golden. 1998. Heterocyst pattern formation controlled by a diffusible peptide. Science 282:935938.
78. Yoon, H.-S.,, and J. W. Golden. 2001. PatS and products of nitrogen fixation control heterocyst pattern. J. Bacteriol. 183:26052613.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error