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.

  • Article
  • Published:

Diverse modes of eco-evolutionary dynamics in communities of antibiotic-producing microorganisms

Nature Ecology & Evolution volume 1, Article number: 0189 (2017) Cite this article

Subjects

Abstract

Whether and how toxin-mediated interactions contribute to diversity generation and maintenance has been a long-standing puzzle. A recent theoretical work has demonstrated that the interplay between antibiotic production and degradation can robustly maintain coexistence of several microbial strains with different antibiotic production and resistance capabilities. The questions, however, remain whether evolution can spontaneously arrive at such communities and whether this mechanism works when biologically realistic features are incorporated. Here I perform multi-scale eco-evolutionary simulations, in which microorganisms compete for a single resource in a two-dimensional environment and evolve their investment in reproduction, antibiotic production and degradation with respect to multiple antibiotics. I show that the dynamics can readily reach long-persistent diverse communities belonging to three different eco-evolutionary classes. First, the dynamics could settle into evolutionary stable states, which were in fact more diverse than those predicted by minimal models. Second, the eco-evolutionary dynamics could exhibit intermittency with prolonged periods of apparent community stability. Finally, communities could persist despite being ecologically unstable through stabilizing loss-of-function mutations. These findings demonstrate that the interplay between toxin production and degradation is a viable mechanism for explaining diversity, and they expand our understanding of the different possible types of eco-evolutionary dynamics in microbial communities.

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: Eco-evolutionary model of antibiotic production and degradation.
Figure 2: The eco-evolutionary dynamics with one antibiotic can rapidly reach an evolutionary stable state with three strains.
Figure 3: The dynamics with two antibiotics can reach evolutionary stable states.
Figure 4: The eco-evolutionary dynamics exhibit several qualitatively different regimes.
Figure 5: Ecologically stable but evolutionary unstable motifs reached by the dynamics.

Similar content being viewed by others

References

  1. Hardin, G. The competitive exclusion principle. Science 131, 1292–1297 (1960).

    Article  CAS  PubMed  Google Scholar 

  2. Kerr, B., Riley, M. A., Feldman, M. W. & Bohannan, B. J. M. Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors. Nature 418, 171–174 (2002).

    Article  CAS  PubMed  Google Scholar 

  3. Kassen, R. & Rainey, P. B. The ecology and genetics of microbial diversity. Annu. Rev. Microbiol. 58, 207–231 (2004).

    Article  CAS  PubMed  Google Scholar 

  4. Rainey, P. B., Buckling, A., Kassen, R. & Travisano, M. The emergence and maintenance of diversity: insights from experimental bacterial populations. Trends Ecol. Evol. 15, 243–247 (2000).

    Article  CAS  PubMed  Google Scholar 

  5. Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343– 366 (2000).

    Article  Google Scholar 

  6. Dieckmann, U. & Doebeli, M. On the origin of species by sympatric speciation. Nature 400, 354–357 (1999).

    Article  CAS  PubMed  Google Scholar 

  7. Doebeli, M. & Ispolatov, I. Complexity and Diversity. Science 328, 494–497 (2010).

    Article  CAS  PubMed  Google Scholar 

  8. Coyte, K. Z., Schluter, J. & Foster, K. R. The ecology of the microbiome: networks, competition, and stability. Science 350, 663–666 (2015).

    Article  CAS  PubMed  Google Scholar 

  9. Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998).

    Article  CAS  PubMed  Google Scholar 

  10. Traverse, C. C., Mayo-Smith, L. M., Poltak, S. R. & Cooper, V. S. Tangled bank of experimentally evolved Burkholderia biofilms reflects selection during chronic infections. Proc. Natl Acad. Sci. USA 110, E250–E259 (2013).

    Article  CAS  PubMed  Google Scholar 

  11. Kassen, R. Toward a general theory of adaptive radiation. Ann. NY Acad. Sci. 1168, 3–22 (2009).

    Article  PubMed  Google Scholar 

  12. Jasmin, J.-N. & Kassen, R. On the experimental evolution of specialization and diversity in heterogeneous environments. Ecol. Lett. 10, 272–281 (2007).

    Article  PubMed  Google Scholar 

  13. Odling-Smee, J., Erwin, D. H., Palkovacs, E. P., Feldman, M. W. & Laland, K. N. Niche construction theory: a practical guide for ecologists. Q. Rev. Biol. 88, 3–28 (2013).

    Article  Google Scholar 

  14. Callahan, B. J., Fukami, T. & Fisher, D. S. Rapid evolution of adaptive niche construction in experimental microbial populations. Evolution 68, 3307–3316 (2014).

    Article  PubMed  Google Scholar 

  15. Herron, M. D. & Doebeli, M. Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLoS Biol. 11, e1001490 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Rosenzweig, R. F., Sharp, R. R., Treves, D. S. & Adams, J. Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli . Genetics 137, 903–917 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Watve, M. G., Tickoo, R., Jog, M. M. & Bhole, B. D. How many antibiotics are produced by the genus Streptomyces? Arch. Microbiol. 176, 386–390 (2001).

    Article  CAS  PubMed  Google Scholar 

  18. Fischbach, M. A., Walsh, C. T. & Clardy, J. The evolution of gene collectives: how natural selection drives chemical innovation. Proc. Natl Acad. Sci. USA 105, 4601–4608 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Nett, M., Ikeda, H. & Moore, B. S. Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat. Prod. Rep. 26, 1362– 1384 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Hopwood, D. A. Soil to genomics: the Streptomyces chromosome. Annu. Rev. Genet. 40, 1– 23 (2006).

    Article  PubMed  Google Scholar 

  21. Wright, G. D. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat. Rev. Microbiol. 5, 175–186 (2007).

    Article  CAS  PubMed  Google Scholar 

  22. Vetsigian, K., Jajoo, R. & Kishony, R. Structure and evolution of Streptomyces interaction networks in soil and in silico . PLoS Biol. 9, e1001184 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  24. Abrudan, M. I. et al. Socially mediated induction and suppression of antibiosis during bacterial coexistence. Proc. Natl Acad. Sci. USA 112, 11054–11059 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Wright, E. S. & Vetsigian, K. H. Inhibitory interactions promote frequent bistability among competing bacteria. Nat. Commun. 7, 11274 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Cordero, O. X. et al. Ecological populations of bacteria act as socially cohesive units of antibiotic production and resistance. Science 337, 1228–1231 (2012).

    Article  CAS  PubMed  Google Scholar 

  27. Cornforth, D. M. & Foster, K. R. Antibiotics and the art of bacterial war. Proc. Natl Acad. Sci. USA 112, 10827–10828 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. van Dijk, B. & Hogeweg, P. In silico gene-level evolution explains microbial population diversity through differential gene mobility. Genome Biol. Evol. 8, 176–188 (2016).

    Article  CAS  Google Scholar 

  29. Durrett, R. & Levin, S. Allelopathy in spatially distributed populations. J. Theor. Biol. 185, 165–171 (1997).

    Article  CAS  PubMed  Google Scholar 

  30. 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 

  31. Kelsic, E. D., Zhao, J., Vetsigian, K. & Kishony, R. Counteraction of antibiotic production and degradation stabilizes microbial communities. Nature 521, 516–519 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Conlin, P. L., Chandler, J. R. & Kerr, B. Games of life and death: antibiotic resistance and production through the lens of evolutionary game theory. Curr. Opin. Microbiol. 21, 35–44 (2014).

    Article  CAS  PubMed  Google Scholar 

  33. Yurtsev, E. A., Chao, H. X., Datta, M. S., Artemova, T. & Gore, J. Bacterial cheating drives the population dynamics of cooperative antibiotic resistance plasmids. Mol. Syst. Biol. 9, 683 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Yurtsev, E. A., Conwill, A. & Gore, J. Oscillatory dynamics in a bacterial cross-protection mutualism. Proc. Natl Acad. Sci. USA 113, 6236–6241 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Vega, N. M. & Gore, J. Collective antibiotic resistance: mechanisms and implications. Curr. Opin. Microbiol. 21, 28–34 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Ochi, K., Tanaka, Y. & Tojo, S. Activating the expression of bacterial cryptic genes by rpoB mutations in RNA polymerase or by rare earth elements. J. Ind. Microbiol. Biotechnol. 41, 403–414 (2014).

    Article  CAS  PubMed  Google Scholar 

  37. Tanaka, Y. et al. Activation and products of the cryptic secondary metabolite biosynthetic gene clusters by rifampin resistance (rpoB) mutations in actinomycetes. J. Bacteriol. 195, 2959–2970 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Gao, C., Hindra, Mulder, D., Yin, C. & Elliot, M. A. Crp is a global regulator of antibiotic production in Streptomyces . mBio 3, e00407–12 (2012).

  39. Charusanti, P. et al. Exploiting adaptive laboratory evolution of Streptomyces clavuligerus for antibiotic discovery and overproduction. PLoS ONE 7, e33727 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Bibb, M. J. Regulation of secondary metabolism in streptomycetes. Curr. Opin. Microbiol. 8, 208–215 (2005).

    Article  CAS  PubMed  Google Scholar 

  41. Clardy, J., Fischbach, M. A. & Currie, C. R. The natural history of antibiotics. Curr. Biol. 19, R437–R441 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Kinkel, L. L., Schlatter, D. C., Xiao, K. & Baines, A. D. Sympatric inhibition and niche differentiation suggest alternative coevolutionary trajectories among Streptomycetes . ISME J. 8, 249–256 (2014).

    Article  CAS  PubMed  Google Scholar 

  43. Seipke, R. F., Kaltenpoth, M. & Hutchings, M. I. Streptomyces as symbionts: an emerging and widespread theme? FEMS Microbiol. Rev. 36, 862–876 (2011).

    Article  PubMed  Google Scholar 

  44. Xu, Y., Willems, A., Au-yeung, C., Tahlan, K. & Nodwell, J. R. A two-step mechanism for the activation of actinorhodin export and resistance in Streptomyces coelicolor . mBio 3, e00191–12 (2012).

  45. Christensen, K., Di Collobiano, S. A., Hall, M. & Jensen, H. J. Tangled nature: a model of evolutionary ecology. J. Theor. Biol. 216, 73–84 (2002).

    Article  PubMed  Google Scholar 

  46. Rikvold, P. A. & Zia, R. K. P. Punctuated equilibria and 1/f noise in a biological coevolution model with individual-based dynamics. Phys. Rev. E 68, 031913 (2003).

    Article  Google Scholar 

  47. Scheffer, M., Carpenter, S., Foley, J. A., Folke, C. & Walker, B. Catastrophic shifts in ecosystems. Nature 413, 591–596 (2001).

    Article  CAS  PubMed  Google Scholar 

  48. Williams, H. T. P. & Lenton, T. M. Evolutionary regime shifts in simulated ecosystems. Oikos 119, 1887–1899 (2010).

    Article  Google Scholar 

  49. Turner, C. B., Blount, Z. D. & Lenski, R. E. Replaying evolution to test the cause of extinction of one ecotype in an experimentally evolved population. PLoS ONE 10, e0142050 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Frenkel, E. M. et al. Crowded growth leads to the spontaneous evolution of semistable coexistence in laboratory yeast populations. Proc. Natl Acad. Sci. USA 112, 11306–11311 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

K.V. acknowledges support from the Simons Foundation, Targeted Grant in the Mathematical Modeling of Living Systems Award 342039 and the National Science Foundation Grant DEB 1457518. This research was performed using the compute resources and assistance of the UW-Madison Center For High Throughput Computing (CHTC) in the Department of Computer Sciences.

Author information

Authors and Affiliations

  1. Department of Bacteriology and Wisconsin Institute for Discovery, University of Wisconsin-Madison,

    Kalin Vetsigian

  2. 330 N Orchard Street, Madison, 53715, Wisconsin, USA

    Kalin Vetsigian

Authors
  1. Kalin Vetsigian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kalin Vetsigian.

Ethics declarations

Competing interests

The author declares no competing financial interests.

Supplementary information

Supplementary Information

Six Supplementary Figures (PDF 1926 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vetsigian, K. Diverse modes of eco-evolutionary dynamics in communities of antibiotic-producing microorganisms. Nat Ecol Evol 1, 0189 (2017). https://doi.org/10.1038/s41559-017-0189

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41559-017-0189

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