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.
Subscribe to Journal
Get full journal access for 1 year
only $9.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Crick FHC, Barnett FRSL, Brenner S, Watts-Tobin RJ. General Nature of the Genetic Code for Proteins. Nature. 1961;192:1227–32.
Hershey AD, Chase M. Independent functions of viral protein and nucleic acid in growth of bacteriophage. J Gen Physiol. 1952;36:39–56.
Luria S, Delbrück M. Mutations of Bacteria from Virus Sensitivity to Virus Resistance. Genetics. 1943;28:491–511.
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.
Mushegian AR. Are there 10^31 virus particles on Earth, or more, or less? J Bacteriol. 2020;202:e00052–20.
Dennehy JJ. What Can Phages Tell Us about Host-Pathogen Coevolution? Int J Evol Biol. 2012;2012:1–12.
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.
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.
Bohannan BJM, Lenski RE. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol Lett. 2000;3:362–77.
Buckling A, Brockhurst MA. Bacteria-Virus Coevolution. In: Orkun S Soyer, editor. Evolutionary Systems Biology. 2012. New York, NY: Springer; 2012. p. 347–70.
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.
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.
Scanlan PD. Bacteria–Bacteriophage Coevolution in the Human Gut: implications for Microbial Diversity and Functionality. Trends Microbiol. 2017;25:614–23.
Breitbart M. Marine viruses: truth or dare. Annu Rev Mar Sci. 2012;4:425–48.
Pratama AA, van Elsas JD. The ‘neglected’ soil virome–potential role and impact. Trends Microbiol. 2018;26:649–62.
Lourenço M, De Sordi L, Debarbieux L. The diversity of bacterial lifestyles hampers bacteriophage tenacity. Viruses. 2018;10:1–11.
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.
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.
Avrani S, Schwartz DA, Lindell D. Virus-host swinging party in the oceans. Mob Genet Elem. 2012;2:88–95.
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.
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.
O’Brien S, Hodgson DJ, Buckling A. The interplay between microevolution and community structure in microbial populations. Curr Opin Biotechnol. 2013;24:821–5.
Brockhurst MA, Koskella B. Experimental coevolution of species interactions. Trends Ecol Evol. 2013;28:367–75.
Geredew Kifelew L, Mitchell JG, Speck P. Mini-review: efficacy of lytic bacteriophages on multispecies biofilms. Biofouling. 2019;35:472–81.
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.
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.
Hall AR, Ashby B, Bascompte J, King KC. Measuring Coevolutionary Dynamics in Species-Rich Communities. Trends Ecol Evol. 2020;35:539–50.
Strauss SY. Ecological and evolutionary responses in complex communities: implications for invasions and eco-evolutionary feedbacks. Oikos. 2014;123:257–66.
Strauss SY, Irwin RE. Ecological and evolutionary consequences of multispecies plant-animal interactions. Annu Rev Ecol Evol Syst. 2004;35:435–66.
Inouye B, Stinchcombe JR. Relationships between ecological interaction modifications and diffuse coevolution: similarities, differences, and causal links. Oikos. 2011;95:353–60.
Barraclough TG. How Do Species Interactions Affect Evolutionary Dynamics Across Whole Communities? Annu Rev Ecol Evol Syst. 2015;46:25–48.
Bottery MJ, Pitchford JW, Friman V-P. Ecology and evolution of antimicrobial resistance in bacterial communities. ISME J. 2021;15:939–48.
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.
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.
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.
Gómez P, Buckling A. Bacteria-phage antagonistic coevolution in soil. Science. 2011;332:106–9.
Weinbauer MG, Rassoulzadegan F. Are viruses driving microbial diversification and diversity? Environ Microbiol. 2004;6:1–11.
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.
R Core Team. R: a Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2020.
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.
Connell JH. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology. 1961;42:710–23.
Vellend M. Conceptual Synthesis in Community Ecology. Q Rev Biol. 2010;85:183–206.
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.
Goldhill DH, Turner PE. The evolution of life history trade-offs in viruses. Curr Opin Virol. 2014;8:79–84.
Keen EC. Tradeoffs in bacteriophage life histories. Bacteriophage. 2014;4:e28365.
Gómez P, Buckling A. Real-time microbial adaptive diversification in soil. Ecol Lett. 2013;16:650–5.
Houte S, van, Buckling A, Westra ER. Evolutionary Ecology of Prokaryotic Immune Mechanisms. Microbiol Mol Biol Rev. 2016;80:745–63.
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.
Gómez P, Buckling A. Coevolution with phages does not influence the evolution of bacterial mutation rates in soil. ISME J. 2013;7:2242–4.
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.
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.
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.
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.
Dy RL, Richter C, Salmond GP, Fineran PC. Remarkable mechanisms in microbes to resist phage infections. Annu Rev Virol. 2014;1:307–31.
Rostøl JT, Marraffini L. (Ph)ighting phages: how bacteria resist their parasites. Cell Host Microbe. 2019;25:184–94.
Burmeister AR, Turner PE. Trading-off and trading-up in the world of bacteria–phage evolution. Curr Biol. 2020;30:R1120–R1124.
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.
Wickham H. ggplot2: elegant Graphics for Data Analysis. Verlag New York: Springer; 2016.
Wickham H. tidyr: Tidy Messy Data. 2020.
Plummer M. rjags: Bayesian Graphical Models using MCMC. 2019.
Wickham H, François R, Henry L, Müller K. dplyr: A Grammar of Data Manipulation. 2020.
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.
We thank the authors of [38,43] for their willingness to share their data, and the authors of  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.
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.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Blazanin, M., Turner, P.E. Community context matters for bacteria-phage ecology and evolution. ISME J (2021). https://doi.org/10.1038/s41396-021-01012-x