Skip to main content
Log in

Alternative stable states in host–phage dynamics

  • Original Paper
  • Published:
Theoretical Ecology Aims and scope Submit manuscript

Abstract

Bacteriophage are ubiquitous in nature, yet many central aspects of host–phage biology have not been integrated into mathematical models. We propose a novel model of host–phage population dynamics that accounts for the decreased ability of phages to lyse hosts as hosts approach their carrying capacity. In contrast to existing predator–prey-like models, we find a parameter regime in which phages cannot invade a host-only system but, nonetheless, can stably coexist with hosts at lower densities. The finding of alternative stable states suggests clear linkages with observed life history strategies of phages. In addition, we solve a limiting case of the proposed model and show that conservative predator-prey like systems do not inevitably exhibit population cycles. Finally, we discuss possible extensions of the present model and scenarios for experimental testing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abedon ST, Yin J (2006) Bacteriophage plaques: theory and analysis. In: Kropinski M (ed) Bacteriophages: methods and protocols. Humana Press, Totowa, NJ

    Google Scholar 

  • Beretta E, Kuang Y (2001) Modeling and analysis of a marine bacteriophage infection with latency period. Nonlinear Anal Real World Appl 2:35–74

    Article  Google Scholar 

  • Bohannan BJM, Lenski RE (1997) Effect of resource enrichment on a chemostat community of bacteria and bacteriophage. Ecology 78:2303–2315

    Article  Google Scholar 

  • Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM, Mead D, Azam F, Rohwer, F (2002) Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci USA 99:14250–14255

    Article  PubMed  CAS  Google Scholar 

  • Bull JJ, Millstein J, Orcutt J, Wichman HA (2006) Evolutionary feedback mediated through population density, illustrated with viruses in chemostats. Am Nat 167:E39–E51

    Article  PubMed  CAS  Google Scholar 

  • Burch CL, Chao L (2004) Epistasis and its relationship to canalization in the RNA virus ϕ6. Genetics 167:559–567

    Article  PubMed  Google Scholar 

  • Chao L, Levin BR, Stewart FM (1977) A complex community in a simple habitat: an experimental study with bacteria and phage. Ecology 58:369–378

    Article  Google Scholar 

  • Cohen SS (1949) Growth requirements of bacterial viruses. Bacteriol Rev 13:1–24

    CAS  Google Scholar 

  • Culley AI, Chan AM, Suttle CA (2006) Metagenomic analysis of coastal RNA virus communities. Science 312:1795–1798

    Article  PubMed  CAS  Google Scholar 

  • De Paepe M, Taddei F (2006) Viruses’ life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages. PLoS Biol 4:e193

    Article  PubMed  CAS  Google Scholar 

  • Edwards RA, Rohwer F (2005) Viral metagenomics. Nat Rev Microbiol 3:504–510

    Article  PubMed  CAS  Google Scholar 

  • Faruque SM, Islam MJ, Ahmad QA, Faruque ASG, Sack DA, Nair GB, Mekalanos JJ (2005a) Self-limiting nature of aseasonal cholera epidemics: Role of host-mediated amplification of phage. Proc Natl Acad Sci USA 102:6119–6124

    Article  CAS  Google Scholar 

  • Faruque SM, Naser IB, Islam MJ, Faruque ASG, Ghosh AN, Nair GB, Sack DA, Mekalanos JJ (2005b) Seasonal epidemics of cholera inversely correlate with the prevalence of environmental cholera phages. Proc Natl Acad Sci USA 102:1702–1707

    Article  CAS  Google Scholar 

  • Forde SE, Thompson JN, Bohannan BJM (2004) Adaptation varies through space and time in a coevoling host–parasitoid interaction. Nature 431:841–844

    Article  PubMed  CAS  Google Scholar 

  • Fort J, Méndez V (2002) Time-delayed spread of viruses in growing plaques. Phys Rev Lett 89:178101

    Article  PubMed  CAS  Google Scholar 

  • Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399:541–548

    Article  PubMed  CAS  Google Scholar 

  • Haywood AM (1974) Lysis of RNA phage-infected cells depends upon culture conditions. J Gen Virol 22:431–435

    Article  Google Scholar 

  • Lenski RE (1988) Dynamics of interactions between bacteria and virulent bacteriophage. Adv Microb Ecol 10:1–44

    CAS  Google Scholar 

  • Levin BR, Stewart FM, Chao L (1977) Resource-limited growth, competition, and predation: a model and experimental studies with bacteria and bacteriophage. Am Nat 111:3–24

    Article  Google Scholar 

  • Lindell DL, Sullivan MB, Johnson ZI, Tolonen A, Rohwer F, Chisholm SW (2004) Transfer of photosnthetic genes to and from Prochlorococcus viruses. Proc Natl Acad Sci USA 101:11013–11018

    Article  PubMed  CAS  Google Scholar 

  • Lythgoe KA, Chao L (2003) Mechanisms of coexistence of a bacteria and a bacteriophage in a spatially homogeneous environment. Ecol Lett 6:326–334

    Article  Google Scholar 

  • McAdams HH, Arkin A (1997) Stochastic mechanisms in gene expression. Proc Natl Acad Sci USA 94:814–819

    Article  PubMed  CAS  Google Scholar 

  • Middleboe M (2000) Bacterial growth rate and marine virus-host dynamics. Microb Ecol 40:114–124

    Google Scholar 

  • Moebus K (1996) Marine bacteriophage reproductiong under nutrient-limited growth of host bacteria. I. Investigations with six phage-host systems. Mar Ecol Prog Ser 144:1–12

    Article  Google Scholar 

  • Murray JD (2002) Mathematical biology I. An introduction, 3rd edn. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Ricciuti CP (1972) Host-virus interactions in Escherichia coli: effect of stationary phase on viral release from MS2-infected bacteria. J Virol 10:162–165

    PubMed  CAS  Google Scholar 

  • Sano E, Carlson S, Wegley L, Rohwer F (2004) Movement of viruses between biomes. Appl Environ Microbiol 70: 5842–5846

    Article  PubMed  CAS  Google Scholar 

  • Silander OK, Weinrich DM, Wright KM, O’Keefe KJ, Rang CU, Turner PE, Chao L (2005) Widespread genetic exchange among terrestrial bacteriophages. Proc Natl Acad Sci USA 102: 19009–19014

    Article  PubMed  CAS  Google Scholar 

  • Sillankorva S, Oliveira R, Vieira MJ, Sutherland I, Azeredo J (2004) Pseudomonas flourescens infection by bacteriophage ΦS1: the influence of temperature, host growth phase and media. FEMS Microbiol Lett 241:13–20

    Article  PubMed  CAS  Google Scholar 

  • Sullivan MB, Coleman M, Weigele P, Rohwer F, Chisholm SW (2005) Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3:e144

    Article  PubMed  CAS  Google Scholar 

  • Suttle CA (1994) The significance of viruses to mortality in aquatic microbial communities. Microb Ecol 28:237–243

    Article  Google Scholar 

  • Turner PE, Chao L (1999) Prisoner’s dilemma in an RNA virus. Nature 398:441–443

    Article  PubMed  CAS  Google Scholar 

  • Wang I, Dykhuizen DE, Slobodkin LB (1996) The evolution of phage lysis timing. Evol Ecol 10:545–558

    Article  Google Scholar 

  • Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181

    Article  PubMed  CAS  Google Scholar 

  • Weitz JS, Hartman H, Levin SA (2005) Coevolutionary arms races between bacteria and bacteriophage. Proc Natl Acad Sci USA 102:9535–9540

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are pleased to acknowledge the support of the Defense Advanced Research Projects Agency under grant HR0011-05-1-0057 to Princeton University. Joshua S. Weitz, Ph.D., holds a Career Award at the Scientific Interface from the Burroughs Wellcome Fund. The authors would like to thank Simon Levin, Steve Pacala, and the members of the Theoretical Ecology Lab at Princeton University, where this work was initiated, for many inspiring discussions. The authors acknowledge A. Handel, A. Rabinovitch, F. Rohwer, P. Salamon, and two anonymous reviewers for helpful suggestions on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joshua S. Weitz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weitz, J.S., Dushoff, J. Alternative stable states in host–phage dynamics. Theor Ecol 1, 13–19 (2008). https://doi.org/10.1007/s12080-007-0001-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12080-007-0001-1

Keywords

Navigation