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Bacterial competition: surviving and thriving in the microbial jungle

Key Points

  • As has been studied extensively for macroorganisms, competition between and within microbial species constitutes a crucial facet of microbial life in the environment.

  • Individuals in a population of a single bacterial species will be in competition with each other when nutrients are limiting. If the ecological opportunity arises (such as when populations are grown in a spatially structured environment, providing multiple niches), intraspecies competition can lead to selection for the diversification of a bacterial population.

  • Under some conditions, cooperation among individuals in a bacterial population can facilitate competition between groups. However, cooperation can be vulnerable to cheating.

  • Bacteria engage in diverse active competitive strategies. These include: accumulating and storing specific nutrients, thereby depriving potential competitors; blocking access to favourable habitats (such as binding sites on a surface) or forcing the dispersal of competitors; motility, especially when directed (chemotaxis); producing antimicrobial toxins; and interfering with competitors' signalling.

  • Microbial systems should be exploited further for testing ecological theories of competition. Additionally, new technologies should aid in moving the study of bacterial competition from the test tube to the natural habitats of microorganisms.

Abstract

Most natural environments harbour a stunningly diverse collection of microbial species. In these communities, bacteria compete with their neighbours for space and resources. Laboratory experiments with pure and mixed cultures have revealed many active mechanisms by which bacteria can impair or kill other microorganisms. In addition, a growing body of theoretical and experimental population studies indicates that the interactions within and between bacterial species can have a profound impact on the outcome of competition in nature. The next challenge is to integrate the findings of these laboratory and theoretical studies and to evaluate the predictions that they generate in more natural settings.

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Figure 1: Examples of interference competition between bacterial species.
Figure 2: Non-transitive competition networks.
Figure 3: Simplified models of siderophore-mediated bacterial competition.

References

  1. Schluter, D. Ecological causes of adaptive radiation. Am. Nat. 148, S40 (1996).

    Article  Google Scholar 

  2. Connell, J. H. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42, 710–723 (1961).

    Article  Google Scholar 

  3. Sogin, M. L. et al. Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc. Natl Acad. Sci. USA 103, 12115–12120 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol. 5, e77 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Monod, J. The growth of bacterial cultures. Annu. Rev. Microbiol. 3, 371–394 (1949).

    Article  CAS  Google Scholar 

  6. Monod, J. La technique de culture continue; theorie et applications. Ann. Inst. Pasteur (Paris) 79, 390–410 (1950).

    CAS  Google Scholar 

  7. Tilman, D. Resource competition between planktonic algae: experimental and theoretical approach. Ecology 58, 338–348 (1977).

    Article  CAS  Google Scholar 

  8. Tilman, D. The resource-ratio hypothesis of plant succession. Am. Nat. 125, 827–852 (1985).

    Article  Google Scholar 

  9. Murray, M. G. & Baird, D. R. Resource-ratio theory applied to large herbivores. Ecology 89, 1445–1456 (2008).

    Article  PubMed  Google Scholar 

  10. Smith, V. Effects of resource supplies on the structure and function of microbial communities. Antonie Van Leeuwenhoek 81, 99–106 (2002).

    Article  CAS  PubMed  Google Scholar 

  11. Cherif, M. & Loreau, M. Stoichiometric constraints on resource use, competitive interactions, and elemental cycling in microbial decomposers. Am. Nat. 169, 709–724 (2007).

    Article  PubMed  Google Scholar 

  12. Kassen, R., Llewellyn, M. & Rainey, P. B. Ecological constraints on diversification in a model adaptive radiation. Nature 431, 984–988 (2004).

    Article  CAS  PubMed  Google Scholar 

  13. Boles, B. R., Thoendel, M. & Singh, P. K. Self-generated diversity produces “insurance effects” in biofilm communities. Proc. Natl Acad. Sci. USA 101, 16630–16635 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kirisits, M. J., Prost, L., Starkey, M. & Parsek, M. R. Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 71, 4809–4821 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998). This study shows that providing P. fluorescens with ecological opportunity (growth in spatially structured, static liquid cultures) results in predictable diversification.

    Article  CAS  PubMed  Google Scholar 

  16. Czárán, T. L., Hoekstra, R. F. & Pagie, L. Chemical warfare between microbes promotes biodiversity. Proc. Natl Acad. Sci. USA 99, 786–790 (2002).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  17. Kerr, B., Riley, M. A., Feldman, M. W. & Bohannan, B. J. Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature 418, 171–174 (2002). Using a model system with colicin-producing, colicin-sensitive and colicin-resistant E. coli , this work elegantly shows the ability of this combination of strains to establish a non-transitive competitive network, as predicted by a model that is elaborated in this paper, and also illustrates the importance of spatial structure in establishing and maintaining the network.

    Article  CAS  PubMed  Google Scholar 

  18. Reichenbach, T., Mobilia, M. & Frey, E. Mobility promotes and jeopardizes biodiversity in rock-paper-scissors games. Nature 448, 1046–1049 (2007).

    Article  CAS  PubMed  Google Scholar 

  19. Narisawa, N., Haruta, S., Arai, H., Ishii, M. & Igarashi, Y. Coexistence of antibiotic-producing and antibiotic-sensitive bacteria in biofilms is mediated by resistant bacteria. Appl. Environ. Microbiol. 74, 3887–3894 (2008). The authors demonstrate the ability of three species isolated from the same sediment to establish a non-transitive competitive network that shares many features of the model network that is described in reference 17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Coleman, M. L. & Chisholm, S. W. Code and context: Prochlorococcus as a model for cross-scale biology. Trends Microbiol. 15, 398–407 (2007).

    Article  CAS  PubMed  Google Scholar 

  21. Garcia-Fernandez, J. M., de Marsac, N. T. & Diez, J. Streamlined regulation and gene loss as adaptive mechanisms in Prochlorococcus for optimized nitrogen utilization in oligotrophic environments. Microbiol. Mol. Biol. Rev. 68, 630–638 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Sullivan, M. B., Waterbury, J. B. & Chisholm, S. W. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424, 1047–1051 (2003).

    Article  CAS  PubMed  Google Scholar 

  23. Coleman, M. L. et al. Genomic islands and the ecology and evolution of Prochlorococcus. Science 311, 1768–1770 (2006).

    Article  CAS  PubMed  Google Scholar 

  24. Hense, B. A. et al. Does efficiency sensing unify diffusion and quorum sensing? Nature Rev. Microbiol. 5, 230–239 (2007).

    Article  CAS  Google Scholar 

  25. West, S. A., Diggle, S. P., Buckling, A., Gardner, A. & Griffin, A. S. The social lives of microbes. Annu. Rev. Ecol. Evol. Syst. 38, 53–77 (2007).

    Article  Google Scholar 

  26. Velicer, G. J. Social strife in the microbial world. Trends Microbiol. 11, 330–337 (2003).

    Article  CAS  PubMed  Google Scholar 

  27. Sandoz, K. M., Mitzimberg, S. M. & Schuster, M. Social cheating in Pseudomonas aeruginosa quorum sensing. Proc. Natl Acad. Sci. USA 104, 15876–15881 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Diggle, S. P., Griffin, A. S., Campbell, G. S. & West, S. A. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450, 411–414 (2007). This study and that described in reference 27 delineate conditions under which social cheaters of P. aeruginosa (that is, mutants that no longer respond to a quorum-sensing signal) accumulate.

    Article  CAS  PubMed  Google Scholar 

  29. Rainey, P. B. & Rainey, K. Evolution of cooperation and conflict in experimental bacterial populations. Nature 425, 72–74 (2003).

    Article  CAS  PubMed  Google Scholar 

  30. Smith, E. E. et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl Acad. Sci. USA 103, 8487–8492 (2006). This work documents the accumulation of mutations in P. aeruginosa populations that live in the lungs of patients with cystic fibrosis and finds a high rate of mutation in the gene encoding the quorum-sensing regulator, lasR.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. D'Argenio, D. A. et al. Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol. Microbiol. 64, 512–533 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Platt, T. G. & Bever, J. D. Kin competition and the evolution of cooperation. Trends Ecol. Evol. 24, 370–377 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Travisano, M. & Velicer, G. J. Strategies of microbial cheater control. Trends Microbiol. 12, 72–78 (2004).

    Article  CAS  PubMed  Google Scholar 

  34. Fiegna, F. & Velicer, G. J. Competitive fates of bacterial social parasites: persistence and self-induced extinction of Myxococcus xanthus cheaters. Proc. R. Soc. Lond. B 270, 1527–1534 (2003).

    Article  Google Scholar 

  35. Griffin, A. S., West, S. A. & Buckling, A. Cooperation and competition in pathogenic bacteria. Nature 430, 1024–1027 (2004).

    Article  CAS  PubMed  Google Scholar 

  36. Chisholm, S. T., Coaker, G., Day, B. & Staskawicz, B. J. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803–814 (2006).

    Article  CAS  PubMed  Google Scholar 

  37. Hansen, S. K., Rainey, P. B., Haagensen, J. A. & Molin, S. Evolution of species interactions in a biofilm community. Nature 445, 533–536 (2007). Describes the interaction of two nutritionally dependent bacteria and the short-term development of mechanisms to enhance their physical association.

    Article  CAS  PubMed  Google Scholar 

  38. Christensen, B. B., Haagensen, J. A. J., Heydorn, A. & Molin, S. Metabolic commensalism and competition in a two-species microbial consortium. Appl. Environ. Microbiol. 68, 2495–2502 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Tong, H. et al. Streptococcus oligofermentans inhibits Streptococcus mutans through conversion of lactic acid into inhibitory H2O2: a possible counteroffensive strategy for interspecies competition. Mol. Microbiol. 63, 872–880 (2007). This paper depicts a particularly intriguing competitive interaction that may have resulted from co-evolution of two species living in the human oral cavity.

    Article  CAS  PubMed  Google Scholar 

  40. Loesche, W. J. Role of Streptococcus mutans in human dental decay. Microbiol. Rev. 50, 353–380 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Nicholson, A. J. An outline of the dynamics of animal populations. Aust. J. Zool. 2, 9–65 (1954).

    Article  Google Scholar 

  42. Wilson, E. O. Sociobiology: The New Synthesis (The Belknap Press, Cambridge, Massachusetts, 2000).

    Google Scholar 

  43. Oehmen, A. et al. Advances in enhanced biological phosphorus removal: from micro to macro scale. Water Res. 41, 2271–2300 (2007).

    Article  CAS  PubMed  Google Scholar 

  44. Wandersman, C. & Delepelaire, P. Bacterial iron sources: from siderophores to hemophores. Annu. Rev. Microbiol. 58, 611–647 (2004).

    Article  CAS  PubMed  Google Scholar 

  45. Khan, A. et al. Differential cross-utilization of heterologous siderophores by nodule bacteria of Cajanus cajan and its possible role in growth under iron-limited conditions. Agric. Ecosyst. Environ. Appl. Soil Ecol. 34, 19–26 (2006).

    Article  Google Scholar 

  46. Joshi, F., Archana, G. & Desai, A. Siderophore cross-utilization amongst rhizospheric bacteria and the role of their differential affinities for Fe3+ on growth stimulation under iron-limited conditions. Curr. Microbiol. 53, 141–147 (2006).

    Article  CAS  PubMed  Google Scholar 

  47. Weaver, V. B. & Kolter, R. Burkholderia spp. alter Pseudomonas aeruginosa physiology through iron sequestration. J. Bacteriol. 186, 2376–2384 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. West, S. A. & Buckling, A. Cooperation, virulence and siderophore production in bacterial parasites. Proc. R. Soc. Lond. B 270, 37–44 (2003).

    Article  Google Scholar 

  49. Harrison, F., Paul, J., Massey, R. C. & Buckling, A. Interspecific competition and siderophore-mediated cooperation in Pseudomonas aeruginosa. ISME J. 2, 49–55 (2008). One of the few studies that seeks to integrate research on the requirements for maintaining intraspecies cooperation with that on the pressure that is imposed by competition from another species.

    Article  PubMed  Google Scholar 

  50. Mashburn, L. M., Jett, A. M., Akins, D. R. & Whiteley, M. Staphylococcus aureus serves as an iron source for Pseudomonas aeruginosa during in vivo coculture. J. Bacteriol. 187, 554–566 (2005). This study uses expression analysis to examine the antagonistic behaviour of P. aeruginosa when it kills S. aureus to access its iron in a rat peritoneal cavity: a true example of a rumble in the microbial jungle.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Rickard, A. H., Gilbert, P., High, N. J., Kolenbrander, P. E. & Handley, P. S. Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol. 11, 94–100 (2003).

    Article  CAS  PubMed  Google Scholar 

  52. Irie, Y., O'Toole, G. A. & Yuk, M. H. Pseudomonas aeruginosa rhamnolipids disperse Bordetella bronchiseptica biofilms. FEMS Microbiol. Lett. 250, 237–243 (2005).

    Article  CAS  PubMed  Google Scholar 

  53. Davies, D. G. & Marques, C. N. A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J. Bacteriol. 191, 1393–1403 (2009). This paper presents the identification and characterization of a specific fatty acid produced by P. aeruginosa that, at nanomolar concentrations, stimulates the dispersal of biofilms of a number of other microbial species.

    Article  CAS  PubMed  Google Scholar 

  54. Golowczyc, M. A., Mobili, P., Garrote, G. L., Abraham, A. G. & De Antoni, G. L. Protective action of Lactobacillus kefir carrying S-layer protein against Salmonella enterica serovar Enteritidis. Int. J. Food Microbiol. 118, 264–273 (2007).

    Article  CAS  PubMed  Google Scholar 

  55. Johnson-Henry, K. C., Hagen, K. E., Gordonpour, M., Tompkins, T. A. & Sherman, P. M. Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157: H7 adhesion to epithelial cells. Cell. Microbiol. 9, 356–367 (2007).

    Article  CAS  PubMed  Google Scholar 

  56. Horie, M. et al. Inhibition of the adherence of Escherichia coli strains to basement membrane by Lactobacillus crispatus expressing an S-layer. J. Appl. Microbiol. 92, 396–403 (2002).

    Article  CAS  PubMed  Google Scholar 

  57. Xavier, J. B. & Foster, K. R. Cooperation and conflict in microbial biofilms. Proc. Natl Acad. Sci. USA 104, 876–881 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. An, D. D., Danhorn, T., Fuqua, C. & Parsek, M. R. Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa and Agrobacterium tumefaciens in biofilm cocultures. Proc. Natl Acad. Sci. USA 103, 3828–3833 (2006). This study identified quorum sensing as an important mechanism that controls the interaction of two bacterial species in several different cultivation formats and that dictates the relative competitive advantage of each species.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Klausen, M., Aaes-Jorgensen, A., Molin, S. & Tolker-Nielsen, T. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol. Microbiol. 50, 61–68 (2003).

    Article  CAS  PubMed  Google Scholar 

  60. Flannagan, R. S., Valvano, M. A. & Koval, S. F. Downregulation of the motA gene delays the escape of the obligate predator Bdellovibrio bacteriovorus 109J from bdelloplasts of bacterial prey cells. Microbiology 150, 649–656 (2004).

    Article  CAS  PubMed  Google Scholar 

  61. Pham, V. D., Shebelut, C. W., Diodati, M. E., Bull, C. T. & Singer, M. Mutations affecting predation ability of the soil bacterium Myxococcus xanthus. Microbiology 151, 1865–1874 (2005).

    Article  CAS  PubMed  Google Scholar 

  62. Verstraeten, N. et al. Living on a surface: swarming and biofilm formation. Trends Microbiol. 16, 496–506 (2008).

    Article  CAS  PubMed  Google Scholar 

  63. McBride, M. J. Bacterial gliding motility: multiple mechanisms for cell movement over surfaces. Annu. Rev. Microbiol. 55, 49–75 (2001).

    Article  CAS  PubMed  Google Scholar 

  64. Chao, L. & Levin, B. R. Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc. Natl Acad. Sci. USA 78, 6324–6328 (1981).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Uroz, S. et al. N-Acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 151, 3313–3322 (2005).

    Article  CAS  PubMed  Google Scholar 

  66. Dong, Y. H., Wang, L. H. & Zhang, L. H. Quorum-quenching microbial infections: mechanisms and implications. Proc. R. Soc. Lond. B 362, 1201–1211 (2007).

    CAS  Google Scholar 

  67. Wang, Y. J. & Leadbetter, J. R. Rapid acyl-homoserine lactone quorum signal biodegradation in diverse soils. Appl. Environ. Microbiol. 71, 1291–1299 (2005). The authors provide a first glimpse of the prevalence and potential importance of biologically mediated degradation of acyl homoserine lactone signal molecules in the environment.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Leadbetter, J. R. & Greenberg, E. P. Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax paradoxus. J. Bacteriol. 182, 6921–6926 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Taga, M. E., Semmelhack, J. L. & Bassler, B. L. The LuxS-dependent autoinducer Al-2 controls the expression of an ABC transporter that functions in Al-2 uptake in Salmonella typhimurium. Mol. Microbiol. 42, 777–793 (2001).

    Article  CAS  PubMed  Google Scholar 

  70. Taga, M. E. & Bassler, B. L. Chemical communication among bacteria. Proc. Natl Acad. Sci. USA 100, 14549–14554 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Taga, M. E. Bacterial signal destruction. ACS Chem. Biol. 2, 89–92 (2007).

    Article  CAS  PubMed  Google Scholar 

  72. Xavier, K. B. & Bassler, B. L. Interference with Al-2-mediated bacterial cell-cell communication. Nature 437, 750–753 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Lyon, G. J. & Novick, R. P. Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria. Peptides 25, 1389–1403 (2004).

    Article  CAS  PubMed  Google Scholar 

  74. Ji, G. Y., Beavis, R. & Novick, R. P. Bacterial interference caused by autoinducing peptide variants. Science 276, 2027–2030 (1997).

    Article  CAS  PubMed  Google Scholar 

  75. Jarraud, S. et al. Exfoliatin-producing strains define a fourth agr specificity group in Staphylococcus aureus. J. Bacteriol. 182, 6517–6522 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Geisinger, E., George, E. A., Muir, T. W. & Novick, R. P. Identification of ligand specificity determinants in AgrC, the Staphylococcus aureus quorum-sensing receptor. J. Biol. Chem. 283, 8930–8938 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Wang, B. Y. & Kuramitsu, H. K. Interactions between oral bacteria: inhibition of Streptococcus mutans bacteriocin production by Streptococcus gordonii. Appl. Environ. Microbiol. 71, 354–362 (2005). This work provides evidence to support a role for signal degradation in mediating competition between Gram-positive residents of the human oral cavity.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Amarasekare, P. Interference competition and species coexistence. Proc. Biol. Sci. 269, 2541–2550 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  79. Kuramitsu, H. K., He, X., Lux, R., Anderson, M. H. & Shi, W. Interspecies interactions within oral microbial communities. Microbiol. Mol. Biol. Rev. 71, 653–670 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Simu, K. & Hagstrom, A. Oligotrophic bacterioplankton with a novel single-cell life strategy. Appl. Environ. Microbiol. 70, 2445–2451 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Stocker, R., Seymour, J. R., Samadani, A., Hunt, D. E. & Polz, M. F. Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc. Natl Acad. Sci. USA 105, 4209–4214 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Prosser, J. I. et al. The role of ecological theory in microbial ecology. Nature Rev. Microbiol. 5, 384–392 (2007).

    Article  CAS  Google Scholar 

  83. Yim, G., Wang, H. M. H. & Davies, J. Antibiotics as signalling molecules. Proc. R. Soc. Lond. B 362, 1195–1200 (2007).

    CAS  Google Scholar 

  84. Goh, E. B. et al. Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proc. Natl Acad. Sci. USA 99, 17025–17030 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Davies, J., Spiegelman, G. B. & Yim, G. The world of subinhibitory antibiotic concentrations. Curr. Opin. Microbiol. 9, 445–453 (2006).

    Article  CAS  PubMed  Google Scholar 

  86. Shank, E. A. & Kolter, R. New developments in microbial interspecies signaling. Curr. Opin. Microbiol. 12, 205–214 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Hoffman, L. R., D'Argenio, D. A., Bader, M. & Miller, S. I. Microbial recognition of antibiotics: ecological, physiological, and therapeutic implications. Microbe 2, 175–182 (2007).

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  89. Price-Whelan, A., Dietrich, L. E. P. & Newman, D. K. Rethinking 'secondary' metabolism: physiological roles for phenazine antibiotics. Nature Chem. Biol. 2, 71–78 (2006).

    Article  CAS  Google Scholar 

  90. López, D., Fischbach, M. A., Chu, F., Losick, R. & Kolter, R. Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc. Natl Acad. Sci. USA 106, 280–285 (2009). A range of small molecules, many of them previously characterized for their antimicrobial activity, are shown to influence B. subtilis biofilm development through a mechanism that involves the triggering of K+ leakage, which is in turn sensed by a particular membrane protein kinase.

    Article  PubMed  Google Scholar 

  91. Dietrich, L. E. P., Teal, T. K., Price-Whelan, A. & Newman, D. K. Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321, 1203–1206 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Schloss, P. D. & Handelsman, J. Toward a census of bacteria in soil. PLoS Comput. Biol. 2, e92 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Challis, G. L. & Hopwood, D. A. Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc. Natl Acad. Sci. USA 100 (Suppl. 2), 14555–14561 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Reader, J. S. et al. Major biocontrol of plant tumors targets tRNA synthetase. Science 309, 1533 (2005).

    Article  CAS  PubMed  Google Scholar 

  95. Kim, J. G. et al. Bases of biocontrol: Sequence predicts synthesis and mode of action of agrocin 84, the Trojan Horse antibiotic that controls crown gall. Proc. Natl Acad. Sci. USA 103, 8846–8851 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Cotter, P. D., Hill, C. & Ross, R. P. Bacteriocins: developing innate immunity for food. Nature Rev. Microbiol. 3, 777–788 (2005).

    Article  CAS  Google Scholar 

  97. Ryan, M., Rea, M., Hill, C. & Ross, R. An application in cheddar cheese manufacture for a strain of Lactococcus lactis producing a novel broad-spectrum bacteriocin, lacticin 3147. Appl. Environ. Microbiol. 62, 612–619 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Pierson, L. S. 3rd, Keppenne, V. D. & Wood, D. W. Phenazine antibiotic biosynthesis in Pseudomonas aureofaciens 30–84 is regulated by PhzR in response to cell density. J. Bacteriol. 176, 3966–3974 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Wood, D. W. & Pierson, L. S. 3rd. The phzI gene of Pseudomonas aureofaciens 30–84 is responsible for the production of a diffusible signal required for phenazine antibiotic production. Gene 168, 49–53 (1996).

    Article  CAS  PubMed  Google Scholar 

  100. Barnard, A. M. et al. Quorum sensing, virulence and secondary metabolite production in plant soft-rotting bacteria. Phil. Trans. R. Soc. Lond. B 362, 1165–1183 (2007).

    Article  CAS  Google Scholar 

  101. Pessi, G. & Haas, D. Transcriptional control of the hydrogen cyanide biosynthetic genes hcnABC by the anaerobic regulator ANR and the quorum-sensing regulators LasR and RhlR in Pseudomonas aeruginosa. J. Bacteriol. 182, 6940–6949 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Ochsner, U. A. & Reiser, J. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 92, 6424–6428 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Brint, J. M. & Ohman, D. E. Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. J. Bacteriol. 177, 7155–7163 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Duerkop, B. A. et al. Quorum-sensing control of antibiotic synthesis in Burkholderia thailandensis. J. Bacteriol. 191, 3909–3918 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Horinouchi, S. A microbial hormone, A-factor, as a master switch for morphological differentiation and secondary metabolism in Streptomyces griseus. Front. Biosci. 7, d2045–d2057 (2002).

    CAS  PubMed  Google Scholar 

  106. Corre, C., Song, L., O'Rourke, S., Chater, K. F. & Challis, G. L. 2-Alkyl-4-hydroxymethylfuran-3-carboxylic acids, antibiotic production inducers discovered by Streptomyces coelicolor genome mining. Proc. Natl Acad. Sci. USA 105, 17510–17515 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Choi, S., Lee, C., Hwang, Y., Kinoshita, H. & Nihira, T. Cloning and functional analysis by gene disruption of a gene encoding a γ-butyrolactone autoregulator receptor from Kitasatospora setae. J. Bacteriol. 186, 3423–3430 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Fontaine, L. et al. Quorum-sensing regulation of the production of Blp bacteriocins in Streptococcus thermophilus. J. Bacteriol. 189, 7195–7205 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Kuipers, O. P., Beerthuyzen, M. M., de Ruyter, P. G., Luesink, E. J. & de Vos, W. M. Autoregulation of nisin biosynthesis in Lactococcus lactis by signal transduction. J. Biol. Chem. 270, 27299–27304 (1995).

    Article  CAS  PubMed  Google Scholar 

  110. Stein, T. et al. Dual control of subtilin biosynthesis and immunity in Bacillus subtilis. Mol. Microbiol. 44, 403–416 (2002).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank L. Hoffman, E. P. Greenberg, G. Velicer and T. Platt for comments that improved the manuscript. Research in the Fuqua laboratory is supported by the US National Institutes of Health (NIH) (GM080546) and the US National Science Foundation (NSF) (MCB-0703467 and DEB-0326842). M.E.H. was a trainee on the Indiana University Genetics, Cellular and Molecular Sciences Training Grant (GM007757). Research in the Parsek laboratory is supported by the NSF (MCB0822405), the NIH (R01 AI061396 and 1R01 AI077628-01A1) and the Cystic Fibrosis Foundation (CFF) (CFR565-CR07), and S.B.P. is supported by a Postdoctoral Research Fellowship from the CFF.

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Correspondence to Matthew R. Parsek or S. Brook Peterson.

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Glossary

Competitive exclusion

When competition between species results in the elimination of one species from a given habitat or region.

Resource ratio model of competition

A theory that predicts the relationship between species' abilities to use resources, resource availability and the outcome of competitive interactions.

Niche

The set of environmental parameters that define the extent of a species habitat.

Negative frequency-dependent selection

Selection that favours individuals only when they are rare in a population.

Colicins

A group of bacteriocins that are produced by and toxic to some strains of Escherichia coli and other enteric bacteria. Colicin-producing strains are immune to the colicin that they produce, owing to their synthesis of an immunity protein.

Kin selection

The accumulation of behaviours that may be detrimental to the fitness of the individual that performs them but that favour the survival of close relatives likely to harbour similar (or identical, in the case of a clonal bacterial population) alleles conferring the cooperative traits.

Social cheaters

Individuals in a population that benefit from the cooperative behaviour of other individuals without themselves contributing to cooperation.

Co-evolution

The process by which two or more species contribute to the selective pressures that lead to adaptation of the interacting species.

Scramble competition

Competition in which one competitor deprives another of a resource (such as a nutrient or habitable space) by depleting that resource.

Contest competition

Competition in which one competitor actively harms the other, such as by fighting or by the production of toxins.

Public goods

In evolutionary biology, any resource produced by one individual that is then available for exploitation by other individuals. An example would be extracellular proteases secreted by a bacterium.

Bacteriocin

A proteinaceous toxin produced by bacteria, with antimicrobial toxicity. Most bacteriocins target other strains of the same species as the producing organism, but some have a broader spectrum of activity.

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Hibbing, M., Fuqua, C., Parsek, M. et al. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8, 15–25 (2010). https://doi.org/10.1038/nrmicro2259

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