A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa

Molecular Microbiology

Volumn 79, Issue 1, 2011, Pages 166-179

  Xavier, Joao B ^a,b   Kim, Wook ^a   Foster, Kevin R ^a,c  

^a HARVARD UNIVERSITY   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSURFACTANT;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENETIC REGULATION; MOLECULAR DYNAMICS; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SECRETION; PROTEIN SYNTHESIS; PSEUDOMONAS AERUGINOSA; QUORUM SENSING;

GENE EXPRESSION REGULATION, BACTERIAL; GLYCOLIPIDS; LOCOMOTION; MUTATION; NITROGEN; PSEUDOMONAS AERUGINOSA;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 78650237493     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07436.x     Document Type: Article

References (57)

1. Alhede, M., Bjarnsholt, T., Jensen, P.O., Phipps, R.K., Moser, C., Christophersen, L., et al. (2009) Pseudomonas aeruginosa recognizes and responds aggressively to the presence of polymorphonuclear leukocytes. Microbiology 155: 3500-3508.
2. Arvidson, S. (2000) Extracellular enzymes. In Gram-positive Pathogens. Fischetti, R.P.N.V.A., Ferretti, J.J., Portnoy, D.A., and Rood, J.I. (eds). Washington, DC: ASM Press, pp. 379-385.
3. Bassler, B., and Losick, R. (2006) Bacterially speaking. Cell 125: 237-246.
4. Boles, B.R., Thoendel, M., and Singh, P.K. (2005) Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 57: 1210-1223.
5. Brockhurst, M., Buckling, A., Racey, D., and Gardner, A. (2008) Resource supply and the evolution of public-goods cooperation in bacteria. BMC Biol 6: 20.
6. Caiazza, N.C., Shanks, R.M.Q., and O'Toole, G.A. (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187: 7351-7361.
7. Caiazza, N.C., Merritt, J.H., Brothers, K.M., and O'Toole, G.A. (2007) Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189: 3603-3612.
8. Camilios Neto, D., Meira, J., de Araújo, J., Mitchell, D., and Krieger, N. (2008) Optimization of the production of rhamnolipids by Pseudomonas aeruginosa UFPEDA 614 in solid-state culture. Appl Microbiol Biotechnol 81: 441-448.
9. Cascales, E., Buchanan, S.K., Duche, D., Kleanthous, C., Lloubes, R., Postle, K., et al. (2007) Colicin biology. Microbiol Mol Biol Rev 71: 158-229.
10. Chuang, J.S., Rivoire, O., and Leibler, S. (2009) Simpson's paradox in a synthetic microbial system. Science 323: 272-275.
11. Clutton-Brock, T.H., Gaynor, D., Kansky, R., MacColl, A.D.C., McIlrath, G., Chadwick, P., et al. (1998) Costs of cooperative behaviour in suricates (Suricata suricatta). Proc Biol Sci 265: 185-190.
12. Clutton-Brock, T.H., O'Riain, M.J., Brotherton, P.N.M., Gaynor, D., Kansky, R., Griffin, A.S., and Manser, M. (1999) Selfish sentinels in cooperative mammals. Science 284: 1640-1644.
13. Costerton, J.W., Stewart, P.S., and Greenberg, E.P. (1999) Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322.
14. Crespi, B.J. (2001) The evolution of social behavior in microorganisms. Trends Ecol Evol 16: 178-183.
15. Deziel, E., Lepine, F., Milot, S., and Villemur, R. (2003) rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa: 3-(3-hydroxyalkanoyloxy)alkanoic acids (HAAs), the precursors of rhamnolipids. Microbiology 149: 2005-2013.
16. Diggle, S., Griffin, A., Campbell, G., and West, S. (2007) Cooperation and conflict in quorum-sensing bacterial populations. Nature 450: 411-414.
17. Dugatkin, L.A., Perlin, M., Lucas, J.S., and Atlas, R. (2005) Group-beneficial traits, frequency-dependent selection and genotypic diversity: an antibiotic resistance paradigm. Proc Biol Sci 272: 79-83.
18. Foster, K.R. (2005) Biomedicine. Hamiltonian medicine: why the social lives of pathogens matter. Science 308: 1269-1270.
19. Foster, K., Shaulsky, G., Strassmann, J., Queller, D., and Thompson, C. (2004) Pleiotropy as a mechanism to stabilize cooperation. Nature 431: 693-696.
20. Foster, K., Parkinson, K., and Thompson, C. (2006) What can microbial genetics teach sociobiology? Trends Genet 23: 74-80.
21. Gerstel, U., and Romling, U. (2001) Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ Microbiol 3: 638-648.
22. Glick, R., Gilmour, C., Tremblay, J., Satanower, S., Avidan, O., Deziel, E., et al. (2010) Increase in rhamnolipid synthesis under iron-limiting conditions influences surface motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol 192: 2973-2980.
23. Griffin, A.S., West, S.A., and Buckling, A. (2004) Cooperation and competition in pathogenic bacteria. Nature 430: 1024-1027.
24. Guerrasantos, L., Kappeli, O., and Fiechter, A. (1984) Pseudomonas-aeruginosa biosurfactant production in continuous culture with glucose as carbon source. Appl Environ Microbiol 48: 301-305.
25. Haba, E., Pinazo, A., Jauregui, O., Espuny, M.J., Infante, M.R., and Manresa, A. (2003) Physicochemical characterization and antimicrobial properties of rhamnolipids produced by Pseudomonas aeruginosa 47T2 NCBIM 40044. Biotechnol Bioeng 81: 316-322.
26. Harder, W., and Dijkhuizen, L. (1983) Physiological-responses to nutrient limitation. Annu Rev Microbiol 37: 1-23.
27. Harrison, F., and Buckling, A. (2009) Siderophore production and biofilm formation as linked social traits. ISME J 3: 632-634.
28. Heurlier, K., Williams, F., Heeb, S., Dormond, C., Pessi, G., Singer, D., et al. (2004) Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol 186: 2936-2945.
29. Horton, R.M., Cai, Z.L., Ho, S.N., and Pease, L.R. (1990) Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8: 528-535.
30. Johnson, N.L., Kotz, S., and Kemp, A.W. (1993) Univariate Discrete Distributions. Hoboken, NJ: Wiley-Interscience.
31. Kearns, D.B. (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 8: 634-644.
32. Kohler, T., Curty, L.K., Barja, F., van Delden, C., and Pechere, J.-C. (2000) Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 182: 5990-5996.
33. Korb, J., and Heinze, J. (2008) Ecology of Social Evolution. Heidelberg: Springer.
34. Kotte, O., Zaugg, J.B., and Heinemann, M. (2010) Bacterial adaptation through distributed sensing of metabolic fluxes. Mol Syst Biol 6: 355.
35. Kümmerli, R., Jiricny, N., Clarke, L.S., West, S.A., and Griffin, A.S. (2009) Phenotypic plasticity of a cooperative behaviour in bacteria. J Evol Biol 22: 589-598.
36. Lambertsen, L., Sternberg, C., and Molin, S. (2004) Mini-Tn7 transposons for site-specific tagging of bacteria with fluorescent proteins. Environ Microbiol 6: 726-732.
37. Latifi, A., Foglino, M., Tanaka, K., Williams, P., and Lazdunski, A. (1996) A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 21: 1137-1146.
38. Lequette, Y., and Greenberg, E.P. (2005) Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms. J Bacteriol 187: 37-44.
39. Medina, G., Juarez, K., and Soberon-Chavez, G. (2003) The Pseudomonas aeruginosa rhlAB operon is not expressed during the logarithmic phase of growth even in the presence of its activator RhlR and the autoinducer N-butyryl-homoserine lactone. J Bacteriol 185: 377-380.
40. Nadell, C.D., Xavier, J.B., and Foster, K.R. (2009) The sociobiology of biofilms. FEMS Microbiol Rev 33: 206-224.
41. Nadell, C.D., Foster, K.R., and Xavier, J.B. (2010) Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comput Biol 6: e1000716.
42. Ochsner, U.A., Koch, A.K., Fiechter, A., and Reiser, J. (1994) Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. J Bacteriol 176: 2044-2054.
43. Pennisi, E. (2005) How did cooperative behavior evolve. Science 309: 93-93.
44. Perkins, T.J., and Swain, P.S. (2009) Strategies for cellular decision-making. Mol Syst Biol 5: 326.
45. Rashid, M.H., and Kornberg, A. (2000) Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 97: 4885-4890.
46. Read, R.C., Roberts, P., Munro, N., Rutman, A., Hastie, A., Shryock, T., et al. (1992) Effect of Pseudomonas aeruginosa rhamnolipids on mucociliary transport and ciliary beating. J Appl Physiol 72: 2271-2277.
47. Sandoz, K.M., Mitzimberg, S.M., and Schuster, M. (2007) Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci USA 104: 15876-15881.
48. Tinbergen, N. (1963) On aims and methods of ethology. Z Tierpsychol 20: 410-433.
49. Venturi, V., Bertani, I., Kerényi, A., Netotea, S., and Pongor, S. (2010) Co-swarming and local collapse: quorum sensing conveys resilience to bacterial communities by localizing cheater mutants in Pseudomonas aeruginosa. PLoS ONE 5: e9998.
50. Verstraeten, N., Braeken, K., Debkumari, B., Fauvart, M., Fransaer, J., Vermant, J., and Michiels, J. (2008) Living on a surface: swarming and biofilm formation. Trends Microbiol 16: 496-506.
51. Visca, P., Imperi, F., and Lamont, I. (2007) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15: 22-30.
52. West, S.A., Griffin, A.S., Gardner, A., and Diggle, S.P. (2006) Social evolution theory for microorganisms. Nat Rev Microbiol 4: 597-607.
53. West, S.A., Diggle, S.P., Buckling, A., Gardner, A., and Griffins, A.S. (2007a) The social lives of microbes. Annu Rev Ecol Evol Syst 38: 53-77.
54. West, S.A., Griffin, A.S., and Gardner, A. (2007b) Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J Evol Biol 20: 415-432.
55. Yarwood, J.M., Volper, E.M., and Greenberg, E.P. (2005) Delays in Pseudomonas aeruginosa quorum-controlled gene expression are conditional. Proc Natl Acad Sci USA 102: 9008-9013.
56. Zhu, K., and Rock, C.O. (2008) RhlA converts {beta}-hydroxyacyl-acyl carrier protein intermediates in fatty acid synthesis to the {beta}-hydroxydecanoyl-{beta}-hydroxydecanoate component of rhamnolipids in Pseudomonas aeruginosa. J Bacteriol 190: 3147-3154.
57. Zulianello, L., Canard, C., Kohler, T., Caille, D., Lacroix, J.-S., and Meda, P. (2006) Rhamnolipids are virulence factors that promote early infiltration of primary human airway epithelia by Pseudomonas aeruginosa. Infect Immun 74: 3134-3147.