Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Opinion
  • Published:

Competition sensing: the social side of bacterial stress responses

Nature Reviews Microbiology volume 11, pages 285–293 (2013)Cite this article

Subjects

Abstract

The field of ecology has long recognized two types of competition: exploitative competition, which occurs indirectly through resource consumption, and interference competition, whereby one individual directly harms another. Here, we argue that these two forms of competition have played a dominant role in the evolution of bacterial regulatory networks. In particular, we argue that several of the major bacterial stress responses detect ecological competition by sensing nutrient limitation (exploitative competition) or direct cell damage (interference competition). We call this competition sensing: a physiological response that detects harm caused by other cells and that evolved, at least in part, for that purpose. A key prediction of our hypothesis is that bacteria will counter-attack when they sense ecological competition but not when they sense abiotic stress. In support of this hypothesis, we show that bacteriocins and antibiotics are frequently upregulated by stress responses to nutrient limitation and cell damage but very rarely upregulated by stress responses to heat or osmotic stress, which typically are not competition related. We argue that stress responses, in combination with the various mechanisms that sense secretions, enable bacteria to infer the presence of ecological competition and navigate the 'microbe-kill-microbe' world in which they live.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The correlated information provided by competition sensing and quorum sensing.
Figure 2: Cladogram of bacteria that induce toxin secretion as a result of stress response activation.

Similar content being viewed by others

References

  1. Birch, L. C. The meanings of competition. Am. Nat. 91, 5–18 (1957).

    Article  Google Scholar 

  2. Case, T. J. & Gilpin, M. E. Interference competition and niche theory. Proc. Natl Acad. Sci. USA 71, 3073–3077 (1974).

    Article  CAS  Google Scholar 

  3. Hansen, S. K., Rainey, P. B., Haagensen, J. A. J. & Molin, S. Evolution of species interactions in a biofilm community. Nature 445, 533–536 (2007).

    Article  CAS  Google Scholar 

  4. Nadell, C. D., Xavier, J. B. & Foster, K. R. The sociobiology of biofilms. FEMS Microbiol. Rev. 33, 206–224 (2009).

    Article  CAS  Google Scholar 

  5. Gans, J., Wolinsky, M. & Dunbar, J. Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309, 1387–1390 (2005).

    Article  CAS  Google Scholar 

  6. Burns, B. P., Goh, F., Allen, M. & Neilan, B. A. Microbial diversity of extant stromatolites in the hypersaline marine environment of Shark Bay, Australia. Environ. Microbiol. 6, 1096–1101 (2004).

    Article  CAS  Google Scholar 

  7. Dethlefsen, L., Eckburg, P. B., Bik, E. M. & Relman, D. A. Assembly of the human intestinal microbiota. Trends Ecol. Evol. 21, 517–523 (2006).

    Article  Google Scholar 

  8. Foster, K. R. & Wenseleers, T. A general model for the evolution of mutualisms. J. Evol. Biol. 19, 1283–1293 (2006).

    Article  CAS  Google Scholar 

  9. Little, A. E. F., Robinson, C. J., Peterson, S. B., Raffa, K. F. & Handelsman, J. Rules of engagement: interspecies interactions that regulate microbial communities. Annu. Rev. Microbiol. 62, 375–401 (2008).

    Article  CAS  Google Scholar 

  10. Hibbing, M. E., Fuqua, C., Parsek, M. R. & Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle. Nature Rev. Microbiol. 8, 15–25 (2009).

    Article  Google Scholar 

  11. Foster, K. R. & Bell, T. Competition, not cooperation, dominates interactions among culturable microbial species. Curr. Biol. 22, 1845–1850 (2012).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Nadell, C. D. & Bassler, B. L. A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. Proc. Natl Acad. Sci. USA 108, 14181–14185 (2011).

    Article  CAS  Google Scholar 

  14. 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).

    Article  CAS  Google Scholar 

  15. D'Costa, V. M. et al. Antibiotic resistance is ancient. Nature 477, 457–461 (2011).

    Article  CAS  Google Scholar 

  16. Fuqua, W. C., Winans, S. C. & Greenberg, E. P. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176, 269–275 (1994).

    Article  CAS  Google Scholar 

  17. Diggle, S. P., Gardner, A., West, S. A. & Griffin, A. S. Evolutionary theory of bacterial quorum sensing: when is a signal not a signal? Philos. Trans. R. Soc. B. 362, 1241–1249 (2007).

    Article  CAS  Google Scholar 

  18. Waters, C. M. & Bassler, B. L. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319–346 (2005).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  21. Storz, G. & Hengge, R. (eds) Bacterial Stress Responses 2nd edn (American Society for Microbiology Press, 2011).

    Google Scholar 

  22. Poole, K. Stress responses as determinants of antimicrobial resistance in Gram-negative bacteria. Trends Microbiol. 20, 227–234 (2012).

    Article  CAS  Google Scholar 

  23. Bagge, N. et al. Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and β-lactamase and alginate production. Antimicrob. Agents Chemother. 48, 1175–1187 (2004).

    Article  CAS  Google Scholar 

  24. 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 

  25. Chavan, M. & Riley, M. in Bacteriocins: Ecology and Evolution (eds Riley, M. A. & Chavan, M. A.) 19–43 (Springer, 2007).

    Book  Google Scholar 

  26. Staron´, A. et al. The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) σ factor protein family. Mol. Microbiol. 74, 557–581 (2009).

    Article  Google Scholar 

  27. Brazas, M. D. & Hancock, R. E. W. Ciprofloxacin induction of a susceptibility determinant in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 49, 3222–3227 (2005).

    Article  CAS  Google Scholar 

  28. Majeed, H., Gillor, O., Kerr, B. & Riley, M. A. Competitive interactions in Escherichia coli populations: the role of bacteriocins. ISME J. 5, 71–81 (2010).

    Article  Google Scholar 

  29. Cao, M. et al. Defining the Bacillus subtilis σW regulon: a comparative analysis of promoter consensus search, run-off transcription/macroarray analysis (ROMA), and transcriptional profiling approaches. J. Mol. Biol. 316, 443–457 (2002).

    Article  CAS  Google Scholar 

  30. Walker, D. et al. Transcriptional profiling of colicin-induced cell death of Escherichia coli MG1655 identifies potential mechanisms by which bacteriocins promote bacterial diversity. J. Bacteriol. 186, 866–869 (2004).

    Article  CAS  Google Scholar 

  31. Cavard, D. Effects of temperature and of heat shock on the expression and action of the colicin A lysis protein. J. Bacteriol. 177, 5189–5192 (1995).

    Article  CAS  Google Scholar 

  32. Wood, J. in Bacterial Stress Responses 2nd edn (eds Storz, G. & Hengge, R.) 133–156 (American Society for Microbiology Press, 2011).

    Google Scholar 

  33. Liras, P., Gomez-Escribano, J. P. & Santamarta, I. Regulatory mechanisms controlling antibiotic production in Streptomyces clavuligerus. J. Ind. Microbiol. Biotechnol. 35, 667–676 (2008).

    Article  CAS  Google Scholar 

  34. Sanchez, S. et al. Carbon source regulation of antibiotic production. J. Antibiot. 63, 442–459 (2010).

    Article  CAS  Google Scholar 

  35. Jensen, V. et al. RhlR expression in Pseudomonas aeruginosa is modulated by the Pseudomonas quinolone signal via PhoB-dependent and -independent pathways. J. Bacteriol. 188, 8601–8606 (2006).

    Article  CAS  Google Scholar 

  36. Xavier, J., Kim, W. & Foster, K. A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa. Mol. Microbiol. 79, 166–179 (2011).

    Article  CAS  Google Scholar 

  37. Perkins, T. J. & Swain, P. S. Strategies for cellular decision-making. Mol. Syst. Biol. 5, 326 (2009).

    Article  Google Scholar 

  38. Gardner, A. Adaptation as organism design. Biol. Lett. 5, 861–864 (2009).

    Article  Google Scholar 

  39. Hindré, T., Pennec, J. P., Haras, D. & Dufour, A. Regulation of lantibiotic lacticin 481 production at the transcriptional level by acid pH. FEMS Microbiol. Lett. 231, 291–298 (2004).

    Article  Google Scholar 

  40. Darch, S. E., West, S. A., Winzer, K. & Diggle, S. P. Density-dependent fitness benefits in quorum-sensing bacterial populations. Proc. Natl Acad. Sci. USA 109, 8259–8263 (2012).

    Article  CAS  Google Scholar 

  41. Hayes, C. S., Aoki, S. K. & Low, D. A. Bacterial contact-dependent delivery systems. Annu. Rev. Genet. 44, 71–90 (2010).

    Article  CAS  Google Scholar 

  42. Gibbs, K. A., Urbanowski, M. L. & Greenberg, E. P. Genetic determinants of self identity and social recognition in bacteria. Science 321, 256–259 (2008).

    Article  CAS  Google Scholar 

  43. Garbeva, P., Silby, M. W., Raaijmakers, J. M., Levy, S. B. & de Boer, W. Transcriptional and antagonistic responses of Pseudomonas fluorescens Pf0-1 to phylogenetically different bacterial competitors. ISME J. 5, 973–985 (2011).

    Article  CAS  Google Scholar 

  44. Laub, M. T. in Bacterial Stress Responses 2nd edn (eds Storz, G. & Hengge, R.) 45–58 (American Society for Microbiology Press, 2011).

    Google Scholar 

  45. Korgaonkar, A. K. & Whiteley, M. Pseudomonas aeruginosa enhances production of an antimicrobial in response to N-acetylglucosamine and peptidoglycan. J. Bacteriol. 193, 909–917 (2011).

    Article  CAS  Google Scholar 

  46. Braun, V., Patzer, S. I. & Hantke, K. Ton-dependent colicins and microcins: modular design and evolution. Biochimie 84, 365–380 (2002).

    Article  CAS  Google Scholar 

  47. Maynard Smith, J. & Price, G. R. The logic of animal conflict. Nature 246, 15–18 (1973).

    Article  Google Scholar 

  48. McGannon, C. M., Fuller, C. A. & Weiss, A. A. Different classes of antibiotics differentially influence Shiga toxin production. Antimicrob. Agents Chemother. 54, 3790–3798 (2010).

    Article  CAS  Google Scholar 

  49. Kültz, D. Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function. J. Exp. Biol. 206, 3119–3124 (2003).

    Article  Google Scholar 

  50. Chopin, M.-C., Chopin, A. & Bidnenko, E. Phage abortive infection in lactococci: variations on a theme. Curr. Opin. Microbiol. 8, 473–479 (2005).

    Article  CAS  Google Scholar 

  51. Marraffini, L. A. & Sontheimer, E. J. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nature Rev. Genet. 11, 181–190 (2010).

    Article  CAS  Google Scholar 

  52. Hayes, F. & Van Melderen, L. Toxins-antitoxins: diversity, evolution and function. Crit. Rev. Biochem. Mol. Biol. 46, 386–408 (2011).

    Article  CAS  Google Scholar 

  53. Roth, J. R., Kugelberg, E., Reams, A. B., Kofoid, E. & Andersson, D. I. Origin of mutations under selection: the adaptive mutation controversy. Annu. Rev. Microbiol. 60, 477–501 (2006).

    Article  CAS  Google Scholar 

  54. Hoffman, L. R. et al. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436, 1171–1175 (2005).

    Article  CAS  Google Scholar 

  55. Collet, A. et al. Impact of rpoS deletion on the proteome of Escherichia coli grown planktonically and as biofilm. J. Proteome Res. 7, 4659–4669 (2008).

    Article  CAS  Google Scholar 

  56. Pfeiffer, T., Schuster, S. & Bonhoeffer, S. Cooperation and competition in the evolution of ATP-producing pathways. Science 292, 504–507 (2001).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  58. Gillor, O. in Bacteriocins: Ecology and Evolution (eds Riley, M. A. & Chavan, M. A.) 135–145 (Springer, 2007).

    Book  Google Scholar 

  59. Gardner, A., West, S. A. & Buckling, A. Bacteriocins, spite and virulence. Proc. Biol. Sci. 271, 1529–1535 (2004).

    Article  CAS  Google Scholar 

  60. Frank, S. A. Spatial polymorphism of bacteriocins and other allelopathic traits. Evol. Ecol. 8, 369–386 (1994).

    Article  Google Scholar 

  61. Wloch-Salamon, D. M., Gerla, D., Hoekstra, R. F. & de Visser, J. A. G. M. Effect of dispersal and nutrient availability on the competitive ability of toxin-producing yeast. Proc. Biol. Sci. 275, 535–541 (2008).

    Article  Google Scholar 

  62. Gough, J., Karplus, K., Hughey, R. & Chothia, C. Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J. Mol. Biol. 313, 903–919 (2001).

    Article  CAS  Google Scholar 

  63. Dauga, C. Evolution of the gyrB gene and the molecular phylogeny of Enterobacteriaceae: a model molecule for molecular systematic studies. Int. J. Syst. Evol. Microbiol. 52, 531–547 (2002).

    Article  CAS  Google Scholar 

  64. Labeda, D. et al. Phylogenetic study of the species within the family Streptomycetaceae. Antonie Van Leeuwenhoek 101, 73–104 (2012).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  66. Inaoka, T., Takahashi, K., Ohnishi-Kameyama, M., Yoshida, M. & Ochi, K. Guanine nucleotides guanosine 5′-diphosphate 3′-diphosphate and GTP co-operatively regulate the production of an antibiotic bacilysin in Bacillus subtilis. J. Biol. Chem. 278, 2169–2176 (2003).

    Article  CAS  Google Scholar 

  67. Jerman, B., Butala, M. & Žgur-Bertok, D. Sublethal concentrations of ciprofloxacin induce bacteriocin synthesis in Escherichia coli. Antimicrob. Agents Chemother. 49, 3087–3090 (2005).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank S. Brown, N. Davies, N. Oliveira, C. Kleanthous, J. Schluter, C. Maclean, P. Swain, R. Popat, D. Newman, W. Kim, S. Mitri, Z. Frankel, S. Diggle and the anonymous referees. D.M.C. acknowledges a Clarendon Fund Scholarship (University of Oxford, UK) and the University of Edinburgh School of Biological Sciences (UK) for support. K.R.F. is supported by European Research Council grant 242670.

Author information

Authors and Affiliations

  1. Daniel M. Cornforth and Kevin R. Foster are at the Department of Zoology, University of Oxford, Oxford, UK.,

    Daniel M. Cornforth & Kevin R. Foster

  2. Daniel M. Cornforth is also at the Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh, UK.,

    Daniel M. Cornforth

  3. Kevin R. Foster is also at the Oxford Centre for Integrative Systems Biology, University of Oxford, Oxford, UK.,

    Kevin R. Foster

Authors
  1. Daniel M. Cornforth
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kevin R. Foster
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Daniel M. Cornforth or Kevin R. Foster.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information S1 (table)

Survey of the regulation of bacterial antibiotics. (PDF 403 kb)

Supplementary information S2 (box)

Parameters and equations for the toxin production model in box 2. (PDF 450 kb)

Supplementary information S3 (figure)

Simulation to evaluate correlations in the information provided by nutrient levels, cell damage and quorum related information. (PDF 414 kb)

Related links

Related links

FURTHER INFORMATION

Kevin R. Foster's homepage

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cornforth, D., Foster, K. Competition sensing: the social side of bacterial stress responses. Nat Rev Microbiol 11, 285–293 (2013). https://doi.org/10.1038/nrmicro2977

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro2977

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing