Quorum Sensing and Signal Transduction in Biofilms: the Impacts of Bacterial Social Behavior on Biofilm Ecology

Yung-Hua Li

doi:10.1128/9781555815479.ch7

Chapter 7 : Quorum Sensing and Signal Transduction in Biofilms: the Impacts of Bacterial Social Behavior on Biofilm Ecology

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Affiliations: 1: Department of Microbiology and Immunology and Department of Applied Oral Sciences, Dalhousie University, 5981 University Ave., Rm. 5215, Halifax, NS B3H 3J5, Canada

Content Type: Monograph

Publication Year: 2009

Category: Food Microbiology; Applied and Industrial Microbiology

Book DOI: 10.1128/9781555815479

Chapter DOI: 10.1128/9781555815479.ch7

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Abstract:

The advances from at least two major research areas, biofilms and bacterial quorum sensing, have led us to begin to appreciate the concept that bacteria can organize into groups, form well-organized communities, and communicate with each other for coordinated activities or social life that was once believed to be restricted to multicellular organisms. Bacteria with altered physiological activities (biofilm phenotypes) are known to result largely from bacterial social behaviors controlled by quorum sensing or other mechanisms when they are living in biofilms. Understanding bacterial social behaviors and their molecular mechanisms in the development of biofilms will greatly facilitate the development of novel strategies in the prevention and treatment of biofilm infections. In 1998, researchers first described the role of las quorum sensing in biofilm formation of Pseudomonas aeruginosa. The biofilms formed by the mutant were also dispersed by the addition of the detergent sodium dodecyl sulfate. This finding suggests that quorum sensing plays an important role in the development of bacterial biofilms. More importantly, this study suggests an inextricable connection between two bacterial social behaviors, quorum sensing and biofilm formation. In P. aeruginosa organism, quorum sensing is highly complex and consists of two interlinked N-acyl-homoserine lactone (AHL) dependent regulatory circuits, which are modulated by numerous regulators acting at both the transcriptional and posttranscriptional levels. The chapter discusses how might quorum sensing signal molecules function in biofilms. Quorum sensing is emerging as an integral component of bacterial global gene regulatory networks responsible for bacterial adaptation in biofilms.

Citation: Li Y. 2009. Quorum Sensing and Signal Transduction in Biofilms: the Impacts of Bacterial Social Behavior on Biofilm Ecology, p 117-133. In Jaykus L, Wang H, Schlesinger L (ed), Food-Borne Microbes. ASM Press, Washington, DC. doi: 10.1128/9781555815479.ch7

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Quorum Sensing and Signal Transduction in Biofilms: the Impacts of Bacterial Social Behavior on Biofilm Ecology

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FIGURE 1

LuxI/LuxR-type quorum sensing in gram-negative bacteria. The LuxI-like protein is an autoinducer synthase that catalyzes the formation of a specific AHL. The AHL freely diffuses through the cell membrane at high cell density. LuxR is a transcriptional regulator protein that binds to the diffusing AHL and, in turn, activates the transcription of its target genes.

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FIGURE 1

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FIGURE 2

Oligopeptide–two-component-type quorum sensing in gram-positive bacteria. Here is a hypothetical model of a quorum sensing system and its controlled phenotypes in Streptococcus mutans. ComD is the histidine kinase protein to sense CSP. ComE is the cognate response regulator to control the transcription of its target genes with the promoter containing a conserved 9-bp repeat element of accgttnag-12 bpaccgttnag (ComE binding site). ComX is an alternative sigma factor that is presumably regulated by ComE and directs RNA polymerase to drive transcription of the late competence genes, such as cinA, recA, and coiA, which contain the consensus sequence of tacgaata (cin-box). nlmAB and bip are the genes encoding CSP-dependent bacteriocin and bacteriocin immunity protein.

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FIGURE 2

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FIGURE 3

luxS-encoded AI-2 quorum sensing in both gram-negative and -positive bacteria. AI-2 is synthesized by the enzyme LuxS and chemically is a furanone. Many gram-negative and -positive bacteria have been found to harbor LuxS homologues in their genomes, but their cognate receptors are unknown with the exception of that in Vibrio harveyi, which uses the LuxPQ two-component-like system to sense and respond to AI-2 for bioluminescence emission. AI-2′ and AI-2″ stand for AI-2 homologues from different species, and they can be sensed by LuxPQ of V. harveyi.

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References

/content/book/10.1128/9781555815479.ch07

1. Ajdic, D.,, W. M. McShan,, R. E. McLaughlin,, G. Savic,, J. Chang,, M. B. Carson,, C. Primeaux,, R. Tian,, S. Kenton,, H. Jia,, S. Lin,, Y. Qian,, S. Li,, H. Zhu,, F. Najar,, H. Lai,, J. White,, B. A. Roe, and, J. J. Ferretti. 2002. Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc. Natl. Acad. Sci. USA 99: 14434– 14439.

2. Bassler, B. L. 2002. Small talk. Cell-to-cell communication in bacteria. Cell 109: 421– 424.

3. Chan, W. C.,, B. J. Coyle, and, P. Williams. 2004. Virulence regulation and quorum sensing in staphylococcal infections: competitive AgrC antagonists as quorum sensing inhibitors. J. Med. Chem. 47: 4633– 4641.

4. Chen, X.,, S. Schauder,, N. Potier,, A. Van Dorssealaer,, I. Pelczer,, B. L. Bassler, and, F. M. Hughson. 2002. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415: 545– 549.

5. Costerton, J. W.,, P. S. Stewart, and, E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284: 1318– 1322.

6. Costerton, W.,, R. Veeh,, M. Shirtliff,, M. Pasmore,, C. Post, and, G. Ehrlich. 2003. The application of biofilm science to the study and control of chronic bacterial infections. J. Clin. Investig. 112: 1466– 1477.

7. Cvitkovitch, D. G.,, Y. H. Li, and, R. P. Ellen. 2003. Quorum sensing and biofilm formation in streptococcal infections. J. Clin. Investig. 112: 1626– 1632.

8. Davey, M. E., and, G. A. O’Toole. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64: 847– 867.

9. 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: 295– 298.

10. de Kievit, T. R., and, B. H. Iglewski. 2000. Bacterial quorum sensing in pathogenic relationships. Infect. Immun. 68: 4839– 4849.

11. Dunny, G. M., and, B. A. Leonard. 1997. Cell-cell communication in Gram-positive bacteria. Annu. Rev. Microbiol. 51: 527– 564.

12. Federle, M. J., and, B. L. Bassler. 2003. Interspecies communication in bacteria. J. Clin. Investig. 112: 1291– 1299.

13. Fuqua, C., and, E. P. Greenberg. 2002. Listening in on bacteria: acyl-homoserine lactone signalling. Nat. Rev. Mol. Cell Biol. 3: 685– 695.

14. Fuqua, C.,, M. R. Parsek, and, E. P. Greenberg. 2001. Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu. Rev. Genet. 35: 439– 468.

15. Ghigo, J. M. 2001. Natural conjugative plasmids induce bacterial biofilm development. Nature 412: 442– 445.

16. Greenberg, E. P. 2003. Bacterial communication and group behavior. J. Clin. Investig. 112: 1288– 1290.

17. Guiral, S.,, T. J. Mitchell,, B. Martin, and, J. P. Claverys. 2005. Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: genetic requirements. Proc. Natl. Acad. Sci. USA 102: 8710– 8715.

18. Hense, B. A.,, C. Kuttler,, J. Müller,, M. Rothballer,, A. Hartmann, and, J. U. Kreft. 2007. Does efficiency sensing unify diffusion and quorum sensing? Nat. Rev. Microbiol. 5: 230– 239.

19. Hentzer, M., and, M. Givskov. 2003. Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J. Clin. Investig. 112: 1300– 1307.

20. Hogan, D., and, R. Kolter. 2002. Why are bacteria refractory to antimicrobials? Curr. Opin. Microbiol. 5: 472– 477.

21. Juhas, M.,, L. Eberl, and, B. Tümmler. 2005. Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ. Microbiol. 7: 459– 471.

22. Keller, L., and, M. G. Surette. 2006. Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol. 4: 249– 258.

23. Kirists, M. J., and, M. R. Parsek. 2006. Does Pseudomonas aeruginosa use intercellular signaling to build biofilm communities? Cell. Microbiol. 8: 1841– 1849.

24. Kolenbrander, P. E. 2000. Oral microbial communities: biofilms, interactions, and genetic systems. Annu. Rev. Microbiol. 54: 413– 437.

25. Kolenbrander, P. E.,, R. N. Andersen,, D. S. Blehert,, P. G. Egland,, J. S. Foster, and, R. J. Parmer, Jr. 2002. Communication among oral bacteria. Microbiol. Mol. Biol. Rev. 66: 486– 505.

26. Kreft, J. U. 2004. Biofilms promote altruism. Microbiology 150: 2751– 2760.

27. Kreth, J.,, J. Merritt,, W. Shi, and, F. Qi. 2005. Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm. J. Bacteriol. 187: 7193– 7203.

28. Kreth, J.,, J. Merritt,, W. Y. Shi, and, F. X. Qi. 2005. Coordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighbouring species. Mol. Microbiol. 57: 392– 404.

29. Li, Y.-H.,, P. C. Y. Lau,, J. H. Lee,, R. P. Ellen, and, D. G. Cvitkovitch. 2001. Natural genetic transformation of Streptococcus mutans growing in biofilms. J. Bacteriol. 183: 897– 908.

30. Li, Y.-H.,, M. N. Hanna,, G. Svensäter,, R. P. Ellen, and, D. G. Cvitkovitch. 2001. Cell density modulates acid adaptation in Streptococcus mutans: implications for survival in biofilms. J. Bacteriol. 183: 6875– 6884.

31. 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: 2699– 2708.

32. Luo, H.,, K. Wan, and, H. H. Wang. 2005. High-frequency conjugation system facilitates biofilm formation and pAMβ1 transmission by Lactococcus lactis. Appl. Environ. Microbiol. 71: 2970– 2978.

33. Lyon, G. J.,, P. Mayville,, T. W. Muir, and, R. P. Novick. 2000. Rational design of a global inhibitor of the virulence response in Staphylococcus aureus, based in part on localization of the site of inhibition to the receptor-histidine kinase, AgrC. Proc. Natl. Acad. Sci. USA 97: 13330– 13335.

34. Marsh, P. D. 1994. Microbial ecology of dental plaque and its significance in health and disease. Adv. Dent. Res. 8: 263– 271.

35. Mayville, P.,, G. Ji,, R. Beavis,, H. Yang,, M. Goger,, R. P. Novick, and, T. W. Muir. 1999. Structure-activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc. Natl. Acad. Sci. USA 96: 1218– 1223.

36. 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: 1972– 1979.

37. Miller, M. B., and, B. L. Bassler. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55: 165– 199.

38. Miller, S. D.,, S. D. Haddock,, C. D. Elvidge, and, T. F. Lee. 2005. Detection of a bioluminescent milky sea from space. Proc. Natl. Acad. Sci. USA 102: 14181– 14184.

39. Mitchell, T. J. 2003. The pathogenesis of streptococcal infections: from tooth decay to meningitis. Nat. Rev. Microbiol. 1: 219– 230.

40. Novick, R. P. 2003. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48: 1429– 1449.

41. Parsek, M. R., and, E. P. Greenberg. 2005. Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol. 13: 27– 33.

42. Parsek, M. R.,, D. L. Val,, B. L. Hanzelka,, J. E. Cronan, Jr., and, E. P. Greenberg. 1999. Acyl homoserine-lactone quorum-sensing signal generation. Proc. Natl. Acad. Sci. USA 96: 4360– 4365.

43. Petersen, F. C., and, A. A. Scheie. 2004. Biofilm mode of growth of Streptococcus intermedius favored by a competence-stimulating signaling peptide. J. Bacteriol. 186: 6327– 6331.

44. Petersen, F. C.,, L. Tao, and, A. A. Scheie. 2005. DNA binding-uptake system: a link between cell-to-cell communication and biofilm formation. J. Bacteriol. 187: 4392– 4400.

45. Rickard, A. H.,, R. J. Palmer, Jr.,, D. S. Blehert,, S. R. Campagna,, M. F. Semmelhack,, P. G. Egland,, B. L. Bassler, and, P. E. Kolenbrander. 2006. Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol. Microbiol. 60: 1446– 1456.

46. Schauder, S., and, B. L. Bassler. 2001. The languages of bacteria. Genes Dev. 15: 1468– 1480.

47. Shirtliff, M. E.,, J. T. Mader, and, A. K. Camper. 2002. Molecular interactions in biofilms. Chem. Biol. 9: 859– 871.

48. Singh, P. K.,, A. L. Schaefer,, M. R. Parsek,, T. O. Moninger,, M. J. Welsh, and, E. P. Greenberg. 2000. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407: 762– 764.

49. Smith, R. S., and, B. H. Iglewski. 2003. Pseudomonas aeruginosa quorum sensing as a potential antimicrobial target. J. Clin. Investig. 112: 1460– 1465.

50. Sponering, A. L., and, M. S. Gilmore. 2006. Quorum sensing and DNA release in bacterial biofilms. Curr. Opin. Microbiol. 9: 133– 137.

51. Syvitski, R. T.,, X.-L. Tian,, K. Sampara,, A. Salman,, S. F. Lee,, D. L. Jakeman, and, Y.-H. Li. 2007. Structure-activity analysis of quorum-sensing signaling peptides from Streptococcus mutans. J. Bacteriol. 189: 1441– 1450.

52. Taga, M. E., and, B. L. Bassler. 2003. Chemical communication among bacteria. Proc. Natl. Acad. Sci. USA 100: 14549– 14554.

53. van der Ploeg, J. R. 2005. Regulation of bacteriocin production in Streptococcus mutans by the quorum-sensing system required for development of genetic competence. J. Bacteriol. 187: 3980– 3989.

54. Watnick, P., and, R. Kolter. 2000. Biofilm, city of microbes. J. Bacteriol. 182: 2675– 2679.

55. Withers, H.,, S. Swift, and, P. Williams. 2001. Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria. Curr. Opin. Microbiol. 4: 186– 193.

56. Yarwood, J. M.,, D. J. Bartels,, E. M. Volper, and, E. P. Greenberg. 2004. Quorum sensing in Staphylococcus aureus biofilms. J. Bacteriol. 186: 1838– 1850.

57. Yoshida, A.,, T. Ansai,, T. Takehara, and, H. K. Kuramitsu. 2005. LuxS-based signaling affects Streptococcus mutans biofilm formation. Appl. Environ. Microbiol. 71: 2372– 2380.

58. Zhang, L.-H., and, Y.-H. Dong. 2004. Quorum sensing and signal interference: diverse implications. Mol. Microbiol. 53: 1563– 1571.