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.

Community context matters for bacteria-phage ecology and evolution

Abstract

Bacteria-phage symbioses are ubiquitous in nature and serve as valuable biological models. Historically, the ecology and evolution of bacteria-phage systems have been studied in either very simple or very complex communities. Although both approaches provide insight, their shortcomings limit our understanding of bacteria and phages in multispecies contexts. To address this gap, here we synthesize the emerging body of bacteria-phage experiments in medium-complexity communities, specifically those that manipulate bacterial community presence. Generally, community presence suppresses both focal bacterial (phage host) and phage densities, while sometimes altering bacteria-phage ecological interactions in diverse ways. Simultaneously, community presence can have an array of evolutionary effects. Sometimes community presence has no effect on the coevolutionary dynamics of bacteria and their associated phages, whereas other times the presence of additional bacterial species constrains bacteria-phage coevolution. At the same time, community context can alter mechanisms of adaptation and interact with the pleiotropic consequences of (co)evolution. Ultimately, these experiments show that community context can have important ecological and evolutionary effects on bacteria-phage systems, but many questions still remain unanswered and ripe for additional investigation.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Effects of community context on focal bacterial and phage ecology and evolution.

References

  1. 1.

    Crick FHC, Barnett FRSL, Brenner S, Watts-Tobin RJ. General Nature of the Genetic Code for Proteins. Nature. 1961;192:1227–32.

    CAS  PubMed  Article  Google Scholar 

  2. 2.

    Hershey AD, Chase M. Independent functions of viral protein and nucleic acid in growth of bacteriophage. J Gen Physiol. 1952;36:39–56.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  3. 3.

    Luria S, Delbrück M. Mutations of Bacteria from Virus Sensitivity to Virus Resistance. Genetics. 1943;28:491–511.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  4. 4.

    Kortright KE, Chan BK, Koff JL, Turner PE. Phage Therapy: a Renewed Approach to Combat Antibiotic-Resistant Bacteria. Cell Host Microbe. 2019;25:219–32.

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Mushegian AR. Are there 10^31 virus particles on Earth, or more, or less? J Bacteriol. 2020;202:e00052–20.

    PubMed  PubMed Central  Article  Google Scholar 

  6. 6.

    Dennehy JJ. What Can Phages Tell Us about Host-Pathogen Coevolution? Int J Evol Biol. 2012;2012:1–12.

    Article  Google Scholar 

  7. 7.

    Jessup CM, Kassen R, Forde SE, Kerr B, Buckling A, Rainey PB, et al. Big questions, small worlds: microbial model systems in ecology. Trends Ecol Evol. 2004;19:189–97.

    PubMed  Article  Google Scholar 

  8. 8.

    Tecon R, Mitri S, Ciccarese D, Or D, Meer JR, van der, Johnson DR. Bridging the Holistic-Reductionist Divide in Microbial Ecology. MSystems. 2019;4:e00265–18.

    PubMed  PubMed Central  Article  Google Scholar 

  9. 9.

    Bohannan BJM, Lenski RE. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol Lett. 2000;3:362–77.

    Article  Google Scholar 

  10. 10.

    Buckling A, Brockhurst MA. Bacteria-Virus Coevolution. In: Orkun S Soyer, editor. Evolutionary Systems Biology. 2012. New York, NY: Springer; 2012. p. 347–70.

  11. 11.

    Koskella B, Brockhurst MA. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol Rev. 2014;38:1–16.

    Article  CAS  Google Scholar 

  12. 12.

    De Sordi L, Lourenço M, Debarbieux L. The Battle Within: interactions of Bacteriophages and Bacteria in the Gastrointestinal Tract. Cell Host Microbe. 2019;25:210–8.

    PubMed  Article  CAS  Google Scholar 

  13. 13.

    Scanlan PD. Bacteria–Bacteriophage Coevolution in the Human Gut: implications for Microbial Diversity and Functionality. Trends Microbiol. 2017;25:614–23.

    CAS  PubMed  Article  Google Scholar 

  14. 14.

    Breitbart M. Marine viruses: truth or dare. Annu Rev Mar Sci. 2012;4:425–48.

    Article  Google Scholar 

  15. 15.

    Pratama AA, van Elsas JD. The ‘neglected’ soil virome–potential role and impact. Trends Microbiol. 2018;26:649–62.

    CAS  PubMed  Article  Google Scholar 

  16. 16.

    Lourenço M, De Sordi L, Debarbieux L. The diversity of bacterial lifestyles hampers bacteriophage tenacity. Viruses. 2018;10:1–11.

    Article  CAS  Google Scholar 

  17. 17.

    Martiny JBH, Riemann L, Marston MF, Middelboe M. Antagonistic Coevolution of Marine Planktonic Viruses and Their Hosts. Annu Rev Mar Sci. 2014;6:393–414.

    Article  Google Scholar 

  18. 18.

    Díaz-Muñoz SL, Koskella B. Bacteria–Phage Interactions in Natural Environments. In: Sariaslani S, Gadd GM, editors. Advances in Applied Microbiology. Cambridge, MA:Academic Press; 2014. p.135–83.

  19. 19.

    Avrani S, Schwartz DA, Lindell D. Virus-host swinging party in the oceans. Mob Genet Elem. 2012;2:88–95.

    Article  Google Scholar 

  20. 20.

    Winter C, Bouvier T, Weinbauer MG, Thingstad TF. Trade-Offs between Competition and Defense Specialists among Unicellular Planktonic Organisms: the “Killing the Winner” Hypothesis Revisited. Microbiol Mol Biol Rev. 2010;74:42–57.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  21. 21.

    Hansen MF, Svenningsen SL, Røder HL, Middelboe M, Burmølle M. Big Impact of the Tiny: bacteriophage–bacteria Interactions in Biofilms. Trends Microbiol. 2019;27:739–52.

    CAS  PubMed  Article  Google Scholar 

  22. 22.

    O’Brien S, Hodgson DJ, Buckling A. The interplay between microevolution and community structure in microbial populations. Curr Opin Biotechnol. 2013;24:821–5.

    PubMed  Article  CAS  Google Scholar 

  23. 23.

    Brockhurst MA, Koskella B. Experimental coevolution of species interactions. Trends Ecol Evol. 2013;28:367–75.

    PubMed  Article  Google Scholar 

  24. 24.

    Geredew Kifelew L, Mitchell JG, Speck P. Mini-review: efficacy of lytic bacteriophages on multispecies biofilms. Biofouling. 2019;35:472–81.

    CAS  PubMed  Article  Google Scholar 

  25. 25.

    Miki T, Jacquet S. Complex interactions in the microbial world: Underexplored key links between viruses, bacteria and protozoan grazers in aquatic environments. Aquat Micro Ecol. 2008;51:195–208.

    Article  Google Scholar 

  26. 26.

    Johnke J, Cohen Y, de Leeuw M, Kushmaro A, Jurkevitch E, Chatzinotas A. Multiple micro-predators controlling bacterial communities in the environment. Curr Opin Biotechnol. 2014;27:185–90.

    CAS  PubMed  Article  Google Scholar 

  27. 27.

    Hall AR, Ashby B, Bascompte J, King KC. Measuring Coevolutionary Dynamics in Species-Rich Communities. Trends Ecol Evol. 2020;35:539–50.

    PubMed  Article  Google Scholar 

  28. 28.

    Strauss SY. Ecological and evolutionary responses in complex communities: implications for invasions and eco-evolutionary feedbacks. Oikos. 2014;123:257–66.

    Article  Google Scholar 

  29. 29.

    Strauss SY, Irwin RE. Ecological and evolutionary consequences of multispecies plant-animal interactions. Annu Rev Ecol Evol Syst. 2004;35:435–66.

    Article  Google Scholar 

  30. 30.

    Inouye B, Stinchcombe JR. Relationships between ecological interaction modifications and diffuse coevolution: similarities, differences, and causal links. Oikos. 2011;95:353–60.

    Article  Google Scholar 

  31. 31.

    Barraclough TG. How Do Species Interactions Affect Evolutionary Dynamics Across Whole Communities? Annu Rev Ecol Evol Syst. 2015;46:25–48.

    Article  Google Scholar 

  32. 32.

    Bottery MJ, Pitchford JW, Friman V-P. Ecology and evolution of antimicrobial resistance in bacterial communities. ISME J. 2021;15:939–48.

    PubMed  Article  PubMed Central  Google Scholar 

  33. 33.

    Gómez P, Bennie J, Gaston KJ, Buckling A. The Impact of Resource Availability on Bacterial Resistance to Phages in Soil. PLoS ONE. 2015;10:e0123752.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  34. 34.

    Gorter FA, Scanlan PD, Buckling A. Adaptation to abiotic conditions drives local adaptation in bacteria and viruses coevolving in heterogeneous environments. Biol Lett. 2016;12:20150879.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  35. 35.

    Scanlan JG, Hall AR, Scanlan PD. Impact of bile salts on coevolutionary dynamics between the gut bacterium Escherichia coli and its lytic phage PP01. Infect Genet Evol. 2019;73:425–32.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  36. 36.

    Gómez P, Buckling A. Bacteria-phage antagonistic coevolution in soil. Science. 2011;332:106–9.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  37. 37.

    Weinbauer MG, Rassoulzadegan F. Are viruses driving microbial diversification and diversity? Environ Microbiol. 2004;6:1–11.

    PubMed  Article  PubMed Central  Google Scholar 

  38. 38.

    Johnke J, Baron M, de Leeuw M, Kushmaro A, Jurkevitch E, Harms H, et al. A generalist protist predator enables coexistence in multitrophic predator-prey systems containing a phage and the bacterial predator Bdellovibrio. Front Ecol Evol. 2017;5:1–12.

    Article  Google Scholar 

  39. 39.

    R Core Team. R: a Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2020.

  40. 40.

    Mumford R, Friman VP. Bacterial competition and quorum-sensing signalling shape the eco-evolutionary outcomes of model in vitro phage therapy. Evol Appl. 2017;10:161–9.

    CAS  PubMed  Article  Google Scholar 

  41. 41.

    Connell JH. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology. 1961;42:710–23.

    Article  Google Scholar 

  42. 42.

    Vellend M. Conceptual Synthesis in Community Ecology. Q Rev Biol. 2010;85:183–206.

    PubMed  Article  Google Scholar 

  43. 43.

    Alseth EO, Pursey E, Lujan AM, McLeod I, Rollie C, Westra ER. Bacterial biodiversity drives the evolution of CRISPR-based phage resistance in Pseudomonas aeruginosa. Nature. 2019;574:549–74.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  44. 44.

    Goldhill DH, Turner PE. The evolution of life history trade-offs in viruses. Curr Opin Virol. 2014;8:79–84.

    PubMed  Article  Google Scholar 

  45. 45.

    Keen EC. Tradeoffs in bacteriophage life histories. Bacteriophage. 2014;4:e28365.

    PubMed  PubMed Central  Article  Google Scholar 

  46. 46.

    Gómez P, Buckling A. Real-time microbial adaptive diversification in soil. Ecol Lett. 2013;16:650–5.

    PubMed  Article  Google Scholar 

  47. 47.

    Houte S, van, Buckling A, Westra ER. Evolutionary Ecology of Prokaryotic Immune Mechanisms. Microbiol Mol Biol Rev. 2016;80:745–63.

    PubMed  PubMed Central  Article  Google Scholar 

  48. 48.

    Middelboe M, Hagström A, Blackburn N, Sinn B, Fischer U, Borch NH, et al. Effects of bacteriophages on the population dynamics of four strains of pelagic marine bacteria. Micro Ecol. 2001;42:395–406.

    CAS  Article  Google Scholar 

  49. 49.

    Gómez P, Buckling A. Coevolution with phages does not influence the evolution of bacterial mutation rates in soil. ISME J. 2013;7:2242–4.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  50. 50.

    De Sordi L, Khanna V, Debarbieux L. The Gut Microbiota Facilitates Drifts in the Genetic Diversity and Infectivity of Bacterial Viruses. Cell Host Microbe. 2017;22:801–8.e3.

    CAS  PubMed  Article  Google Scholar 

  51. 51.

    De Sordi L, Lourenço M, Debarbieux L. “I will survive”: A tale of bacteriophage-bacteria coevolution in the gut. Gut Microbes. 2019;10:92–9.

    CAS  PubMed  Article  Google Scholar 

  52. 52.

    Landsberger M, Gandon S, Meaden S, Chabas H, Buckling A, Westra ER, et al. Anti-CRISPR phages cooperate to overcome CRISPR-Cas immunity. Cell. 2018;174:908–16.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  53. 53.

    Westra ER, van Houte S, Oyesiku-Blakemore S, Makin B, Broniewski JM, Best A, et al. Parasite exposure drives selective evolution of constitutive versus inducible defense. Curr Biol. 2015;25:1043–9.

    CAS  PubMed  Article  Google Scholar 

  54. 54.

    Dy RL, Richter C, Salmond GP, Fineran PC. Remarkable mechanisms in microbes to resist phage infections. Annu Rev Virol. 2014;1:307–31.

    PubMed  Article  CAS  Google Scholar 

  55. 55.

    Rostøl JT, Marraffini L. (Ph)ighting phages: how bacteria resist their parasites. Cell Host Microbe. 2019;25:184–94.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  56. 56.

    Burmeister AR, Turner PE. Trading-off and trading-up in the world of bacteria–phage evolution. Curr Biol. 2020;30:R1120–R1124.

    CAS  PubMed  Article  Google Scholar 

  57. 57.

    Plummer M. JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. Vienna, Austria: Proc. 3rd Int. Workshop Distrib. Stat. Comput; 2003. p. 1–10.

  58. 58.

    Wickham H. ggplot2: elegant Graphics for Data Analysis. Verlag New York: Springer; 2016.

  59. 59.

    Wickham H. tidyr: Tidy Messy Data. 2020.

  60. 60.

    Plummer M. rjags: Bayesian Graphical Models using MCMC. 2019.

  61. 61.

    Wickham H, François R, Henry L, Müller K. dplyr: A Grammar of Data Manipulation. 2020.

  62. 62.

    Gandon S, Buckling A, Decaestecker E, Day T. Host-parasite coevolution and patterns of adaptation across time and space. J Evol Biol. 2008;21:1861–6.

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgements

We thank the authors of [38,43] for their willingness to share their data, and the authors of [40] for making their data publicly available. Three anonymous reviewers provided valuable comments on this study. Alita Burmeister provided feedback on drafts of the paper, and the members of the Turner lab provided feedback on the paper ideas. Our work was supported by NSF Cooperative Agreement DBI-0939454 through the BEACON Center for the Study of Evolution in Action, and by NIH Grant #R21AI144345 from the National Institute of Allergy and Infectious Diseases.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Michael Blazanin.

Ethics declarations

Conflict of interest

MB declares no competing interests. PET is a co-founder of Felix Biotechnology Inc., and declares a financial interest in this company that seeks to commercially develop phages for use as therapeutics.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Blazanin, M., Turner, P.E. Community context matters for bacteria-phage ecology and evolution. ISME J 15, 3119–3128 (2021). https://doi.org/10.1038/s41396-021-01012-x

Download citation

Search

Quick links