Ecological suicide in microbes

Abstract

The growth and survival of organisms often depend on interactions between them. In many cases, these interactions are positive and caused by a cooperative modification of the environment. Examples are the cooperative breakdown of complex nutrients in microbes or the construction of elaborate architectures in social insects, in which the individual profits from the collective actions of her peers. However, organisms can similarly display negative interactions by changing the environment in ways that are detrimental for them, for example by resource depletion or the production of toxic byproducts. Here we find an extreme type of negative interactions, in which Paenibacillus sp. bacteria modify the environmental pH to such a degree that it leads to a rapid extinction of the whole population, a phenomenon that we call ecological suicide. Modification of the pH is more pronounced at higher population densities, and thus ecological suicide is more likely to occur with increasing bacterial density. Correspondingly, promoting bacterial growth can drive populations extinct whereas inhibiting bacterial growth by the addition of harmful substances—such as antibiotics—can rescue them. Moreover, ecological suicide can cause oscillatory dynamics, even in single-species populations. We found ecological suicide in a wide variety of microbes, suggesting that it could have an important role in microbial ecology and evolution.

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Fig. 1: Microbial acidification can cause ecological suicide.
Fig. 2: Ecological suicide can cause oscillations in the population size over time.
Fig. 3: Inhibiting growth of the bacteria can save the population.
Fig. 4: Ecological suicide is a common phenomenon in microbes.

References

  1. 1.

    Celiker, H. & Gore, J. Cellular cooperation: insights from microbes. Trends Cell Biol. 23, 9–15 (2013).

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Ratzke, C. & Gore, J. Self-organized patchiness facilitates survival in a cooperatively growing Bacillus subtilis population. Nat. Microbiol. 1, 16022 (2016).

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Drescher, K., Nadell, C. D., Stone, H. A., Wingreen, N. S. & Bassler, B. L. Solutions to the public goods dilemma in bacterial biofilms. Curr. Biol. 24, 50–55 (2014).

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Celiker, H. & Gore, J. Competition between species can stabilize public‐goods cooperation within a species. Mol. Syst. Biol. 8, 621 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Anderson, D. E., Becktel, W. J. & Dahlquist, F. W. pH-induced denaturation of proteins: a single salt bridge contributes 3-5 kcal/mol to the free energy of folding of T4 lysozyme. Biochemistry 29, 2403–2408 (1990).

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Träuble, H., Teubner, M., Woolley, P. & Eibl, H. Electrostatic interactions at charged lipid membranes: I. Effects of ph and univalent cations on membrane structure. Biophys. Chem. 4, 319–342 (1976).

    Article  Google Scholar 

  7. 7.

    Jones, R. T. et al. A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J. 3, 442–453 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Rousk, J., Brookes, P. C. & Bååth, E. Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl. Environ. Microbiol. 75, 1589–1596 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Ratzke, C. & Gore, J. Modifying and reacting to the environmental pH can drive bacterial interactions. PLoS Biol. 16, e2004248 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Russell, J. B. & Dombrowski, D. B. Effect of pH on the efficiency of growth by pure cultures of rumen bacteria in continuous culture. Appl. Environ. Microbiol. 39, 604–610 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Raven, J. A. & Smith, F. A. The evolution of chemiosmotic energy coupling. J. Theor. Biol. 57, 301–312 (1976).

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Safařík, I. V. O. & Šantrůčková, H. Direct determination of total soil carbohydrate content. Plant Soil 143, 109–114 (1992).

    Article  Google Scholar 

  13. 13.

    Mehta, N. C., Dubach, P. & Deuel, H. in Advances in Carbohydrate Chemistry (ed. Wolfrom, M. L.) 335–355 (Academic, Amsterdam, 1962).

  14. 14.

    Li, C. H., Ma, B. L. & Zhang, T. Q. Soil bulk density effects on soil microbial populations and enzyme activities during the growth of maize (Zea mays L.) planted in large pots under field exposure. Can. J. Soil Sci. 82, 147–154 (2002).

    CAS  Article  Google Scholar 

  15. 15.

    Raynaud, X. & Nunan, N. Spatial ecology of bacteria at the microscale in soil. PLoS ONE 9, e87217 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Seviour, R. & Nielsen, P. H. Microbial Ecology of Activated Sludge (IWA Publishing, London, 2010).

  17. 17.

    Seviour, E. M. et al. Studies on filamentous bacteria from Australian activated sludge plants. Water Res. 28, 2335–2342 (1994).

    Article  Google Scholar 

  18. 18.

    Allee, W. C. et al. Principles of Animal Ecology (W. B. Saunders, Philadelphia, 1965).

  19. 19.

    Courchamp, F., Clutton-Brock, T. & Grenfell, B. Inverse density dependence and the Allee effect. Trends Ecol. Evol. 14, 405–410 (1999).

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Stephens, P. A., Sutherland, W. J. & Freckleton, R. P. What is the Allee effect? Oikos 87, 185–190 (1999).

    Article  Google Scholar 

  21. 21.

    Stebbing, A. R. D. Hormesis — the stimulation of growth by low levels of inhibitors. Sci. Total Environ. 22, 213–234 (1982).

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Higgins, L. M., Friedman, J., Shen, H. & Gore, J. Co-occurring soil bacteria exhibit a robust competitive hierarchy and lack of non-transitive interactions. Preprint at https://www.biorxiv.org/content/early/2017/08/16/175737 (2017).

  23. 23.

    Paczia, N. et al. Extensive exometabolome analysis reveals extended overflow metabolism in various microorganisms. Microb. Cell Factor. 11, 122 (2012).

    CAS  Article  Google Scholar 

  24. 24.

    Fujita, Y., Ferris, F. G., Lawson, R. D., Colwell, F. S. & Smith, R. W. Subscribed content calcium carbonate precipitation by ureolytic subsurface bacteria. Geomicrobiol. J. 17, 305–318 (2000).

    CAS  Article  Google Scholar 

  25. 25.

    Finkel, S. E. Long-term survival during stationary phase: evolution and the GASP phenotype. Nat. Rev. Microbiol. 4, 113–120 (2006).

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Burtner, C. R., Murakami, C. J., Kennedy, B. K. & Kaeberlein, M. A molecular mechanism of chronological aging in yeast. Cell Cycle 8, 1256–1270 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Goo, E. et al. Bacterial quorum sensing, cooperativity, and anticipation of stationary-phase stress. Proc. Natl Acad. Sci. USA 109, 19775–19780 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    An, J. H., Goo, E., Kim, H., Seo, Y.-S. & Hwang, I. Bacterial quorum sensing and metabolic slowing in a cooperative population. Proc. Natl Acad. Sci. USA 111, 14912–14917 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Cotter, P. D. & Hill, C. Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiol. Mol. Biol. Rev. 67, 429–453 (2003).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Klein, D. R. The introduction, increase, and crash of reindeer on St. Matthew Island. J. Wildl. Manage. 32, 350–367 (1968).

    Article  Google Scholar 

  31. 31.

    Scheffer, V. B. The rise and fall of a reindeer herd. Sci. Mon. 73, 356–362 (1951).

    Google Scholar 

  32. 32.

    Hindell, M. A. Some life-history parameters of a declining population of southern elephant seals, Mirounga leonina. J. Anim. Ecol. 60, 119–134 (1991).

    Article  Google Scholar 

  33. 33.

    Wackernagel, M. et al. Tracking the ecological overshoot of the human economy. Proc. Natl Acad. Sci. USA 99, 9266–9271 (2002).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Malthus, T. R. An Essay on the Principle of Population, as it Affects the Future Improvement of Society: With Remarks on the Speculations of Mr. Godwin, Mr. Condorcet, and Other Writers (J. Johnson, London, 1798).

  35. 35.

    Meadows, D., Randers, J. & Meadows, D. Limits to Growth: The 30-Year Update (Chelsea Green Publishing, White River Junction, 2004).

  36. 36.

    Diamond, J. Collapse: How Societies Choose to Fail or Succeed (Penguin, London, 2005).

  37. 37.

    Tainter, J. A. Archaeology of overshoot and collapse. Annu. Rev. Anthropol. 35, 59–74 (2006).

    Article  Google Scholar 

  38. 38.

    Shennan, S. et al. Regional population collapse followed initial agriculture booms in mid-Holocene Europe. Nat. Commun. 4, 2486 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Fussmann, G. F., Ellner, S. P., Shertzer, K. W. & Hairston, N. G. Jr. Crossing the Hopf bifurcation in a live predator–prey system. Science 290, 1358–1360 (2000).

    CAS  Article  PubMed  Google Scholar 

  40. 40.

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Tu, B. P., Kudlicki, A., Rowicka, M. & McKnight, S. L. Logic of the yeast metabolic cycle: temporal compartmentalization of cellular processes. Science 310, 1152–1158 (2005).

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    Liu, J. et al. Coupling between distant biofilms and emergence of nutrient time-sharing. Science 365, 638–642 (2017).

  43. 43.

    Collos, Y. et al. Phased oscillations in cell numbers and nitrate in batch cultures of Alexandrium tamarense (Dinophyceae). J. Phycol. 47, 1057–1062 (2011).

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Cornejo, O. E., Rozen, D. E., May, R. M. & Levin, B. R. Oscillations in continuous culture populations of Streptococcus pneumoniae: population dynamics and the evolution of clonal suicide. Proc. R. Soc. B 276, 999–1008 (2009).

    Article  PubMed  Google Scholar 

  45. 45.

    Parvinen, K. Evolutionary suicide. Acta Biotheor. 53, 241–264 (2005).

    Article  PubMed  Google Scholar 

  46. 46.

    Wang, X., Meier, R. J. & Wolfbeis, O. S. Fluorescent pH-sensitive nanoparticles in an agarose matrix for imaging of bacterial growth and metabolism. Angew. Chem. Int. Ed. 52, 406–409 (2013).

    CAS  Article  Google Scholar 

  47. 47.

    Rein, J. et al. Fluorescence measurements of serotonin-induced V-ATPase-dependent pH changes at the luminal surface in salivary glands of the blowfly Calliphora vicina. J. Exp. Biol. 209, 1716–1724 (2006).

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

We thank L. Higgins for providing us with the collection of bacterial soil isolates. J.D. is supported by a DFG fellowship through the Graduate School of Quantitative Biosciences Munich. We thank all members of the Gore lab for reading and discussing the manuscript. This work was funded by an Allen Distinguished Investigator Award and a NIH R01 grant.

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C.R., J.D. and J.G. designed the research. J.D., C.R. and J.G. carried out the experiments and performed the mathematical analysis. C.R., J.D. and J.G discussed and interpreted the results, and wrote the manuscript.

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Correspondence to Christoph Ratzke or Jeff Gore.

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Ratzke, C., Denk, J. & Gore, J. Ecological suicide in microbes. Nat Ecol Evol 2, 867–872 (2018). https://doi.org/10.1038/s41559-018-0535-1

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