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.

  • Opinion
  • Published:

Explaining microbial population genomics through phage predation

Nature Reviews Microbiology volume 7, pages 828–836 (2009)Cite this article

Abstract

The remarkable differences that have been detected by metagenomics in the genomes of strains of the same bacterial species are difficult to reconcile with the widely accepted paradigm that periodic selection within bacterial populations will regularly purge genomic diversity by clonal replacement. We have found that many of the genes that differ between strains affect regions that are potential phage recognition targets. We therefore propose the constant-diversity dynamics model, in which the diversity of prokaryotic populations is preserved by phage predation. We provide supporting evidence for this model from metagenomics, mathematical analysis and computer simulations. Periodic selection and phage predation dynamics are not mutually exclusive; we compare their predictions to shed light on the ecological circumstances under which each type of dynamics could predominate.

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: Metagenomic islands in selected bacteria identified by comparison with available metagenomes.
Figure 2: Population dynamics under constant-diversity and periodic-selection dynamics.
Figure 3: Cell density and microbial diversity under constant-diversity and periodic-selection dynamics.

Similar content being viewed by others

References

  1. Gupta, S. & Maiden, M. C. Exploring the evolution of diversity in pathogen populations. Trends Microbiol. 9, 181–185 (2001).

    Article  CAS  Google Scholar 

  2. Whitaker, R. J. & Banfield, J. F. Population genomics in natural microbial communities. Trends Ecol. Evol. 21, 508–516 (2006).

    Article  Google Scholar 

  3. Medini, D. et al. Microbiology in the post-genomic era. Nature Rev. Microbiol. 6, 419–430 (2008).

    Article  CAS  Google Scholar 

  4. Medini, D., Donati, C., Tettelin, H., Masignani, V. & Rappuoli, R. The microbial pan-genome. Curr. Opin. Genet. Dev. 15, 589–594 (2005).

    Article  CAS  Google Scholar 

  5. Liti, G. et al. Population genomics of domestic and wild yeasts. Nature 458, 337–341 (2009).

    Article  CAS  Google Scholar 

  6. Tettelin, H. et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc. Natl Acad. Sci. USA 102, 13950–13955 (2005).

    Article  CAS  Google Scholar 

  7. Konstantinidis, K. T. & Tiedje, J. M. Genomic insights that advance the species definition for prokaryotes. Proc. Natl Acad. Sci. USA 102, 2567–2572 (2005).

    Article  CAS  Google Scholar 

  8. Maharjan, R., Seeto, S., Notley-McRobb, L. & Ferenci, T. Clonal adaptive radiation in a constant environment. Science 313, 514–517 (2006).

    Article  CAS  Google Scholar 

  9. Atwood, K. C., Schneider, L. K. & Ryan, F. J. Periodic selection in Escherichia coli. Proc. Natl Acad. Sci. USA 37, 146–155 (1951).

    Article  CAS  Google Scholar 

  10. Atwood, K. C., Schneider, L. K. & Ryan, F. J. Selective mechanisms in bacteria. Cold Spring Harb. Symp. Quant. Biol. 16, 345–355 (1951).

    Article  CAS  Google Scholar 

  11. Feil, E. J. Small change: keeping pace with microevolution. Nature Rev. Microbiol. 2, 483–495 (2004).

    Article  CAS  Google Scholar 

  12. Hershberg, R. et al. high functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 6, e311 (2008).

    Article  Google Scholar 

  13. Cohan, F. M. & Koeppel, A. F. The origins of ecological diversity in prokaryotes. Curr. Biol. 18, R1024–R1034 (2008).

    Article  CAS  Google Scholar 

  14. Acinas, S. G. et al. Fine-scale phylogenetic architecture of a complex bacterial community. Nature 430, 551–554 (2004).

    Article  CAS  Google Scholar 

  15. Gevers, D. et al. Opinion: Re-evaluating prokaryotic species. Nature Rev. Microbiol. 3, 733–739 (2005).

    Article  CAS  Google Scholar 

  16. Koeppel, A. et al. Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics. Proc. Natl Acad. Sci. USA 105, 2504–2509 (2008).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  18. Wildschutte, H. & Lawrence, J. G. Differential Salmonella survival against communities of intestinal amoebae. Microbiology 153, 1781–1789 (2007).

    Article  CAS  Google Scholar 

  19. Zubkov, M. V. & Tarran, G. A. High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455, 224–226 (2008).

    Article  CAS  Google Scholar 

  20. Suttle, C. A. Marine viruses — major players in the global ecosystem. Nature Rev. Microbiol. 5, 801–812 (2007).

    Article  CAS  Google Scholar 

  21. Thingstad, T. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic ecosystems. Limnol. Oceanogr. 45, 1320–1328 (2000).

    Article  Google Scholar 

  22. Thingstad, T. F. & Lignell, R. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol. 13, 19–27 (1997).

    Article  Google Scholar 

  23. Coleman, M. L. et al. Genomic islands and the ecology and evolution of Prochlorococcus. Science 311, 1768–1770 (2006).

    CAS  Google Scholar 

  24. Legault, B. A. et al. Environmental genomics of “Haloquadratum walsbyi” in a saltern crystallizer indicates a large pool of accessory genes in an otherwise coherent species. BMC Genomics 7, 171 (2006).

    Article  Google Scholar 

  25. Coleman, M. L. & Chisholm, S. W. Code and context: Prochlorococcus as a model for cross-scale biology. Trends Microbiol. 15, 398–407 (2007).

    Article  CAS  Google Scholar 

  26. Wilhelm, L. J., Tripp, H. J., Givan, S. A., Smith, D. P. & Giovannoni, S. J. Natural variation in SAR11 marine bacterioplankton genomes inferred from metagenomic data. Biol. Direct 2, 27 (2007).

    Article  Google Scholar 

  27. Cuadros-Orellana, S. et al. Genomic plasticity in prokaryotes: the case of the square haloarchaeon. ISME J. 1, 235–245 (2007).

    Article  CAS  Google Scholar 

  28. Kettler, G. C. et al. Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet. 3, e231 (2007).

    Article  Google Scholar 

  29. Frias-Lopez, J. et al. Microbial community gene expression in ocean surface waters. Proc. Natl Acad. Sci. USA 105, 3805–3810 (2008).

    Article  CAS  Google Scholar 

  30. Garcia Martin, H. et al. Metagenomic analysis of two enhanced biological phosphorus removal (EBPR) sludge communities. Nature Biotechnol. 24, 1263–1269 (2006).

    Article  Google Scholar 

  31. Sharma, R. S., Mishra, V., Mohmmed, A. & Babu, C. R. Phage specificity and lipopolysaccarides of stem- and root-nodulating bacteria (Azorhizobium caulinodans, Sinorhizobium spp., and Rhizobium spp.) of Sesbania spp. Arch. Microbiol. 189, 411–418 (2008).

    Article  CAS  Google Scholar 

  32. Fitzgerald, C., Sherwood, R., Gheesling, L. L., Brenner, F. W. & Fields, P. I. Molecular analysis of the rfb O antigen gene cluster of Salmonella enterica serogroup O:6,14 and development of a serogroup-specific PCR assay. Appl. Environ. Microbiol. 69, 6099–6105 (2003).

    Article  CAS  Google Scholar 

  33. Ivars-Martinez, E. et al. Comparative genomics of two ecotypes of the marine planktonic copiotroph Alteromonas macleodii suggests alternative lifestyles associated with different kinds of particulate organic matter. ISME J. 2, 1194–1212 (2008).

    Article  CAS  Google Scholar 

  34. Reva, O. & Tummler, B. Think big — giant genes in bacteria. Environ. Microbiol. 10, 768–777 (2008).

    Article  CAS  Google Scholar 

  35. Leiman, P. G. et al. The structures of bacteriophages K1E and K1–5 explain processive degradation of polysaccharide capsules and evolution of new host specificities. J. Mol. Biol. 371, 836–849 (2007).

    Article  CAS  Google Scholar 

  36. Mizoguchi, K. et al. Coevolution of bacteriophage PP01 and Escherichia coli O157:H7 in continuous culture. Appl. Environ. Microbiol. 69, 170–176 (2003).

    Article  CAS  Google Scholar 

  37. Wilmes, P., Simmons, S. L., Denef, V. J. & Banfield, J. F. The dynamic genetic repertoire of microbial communities. FEMS Microbiol. Rev. 33, 109–132 (2009).

    Article  CAS  Google Scholar 

  38. Sorek, R., Kunin, V. & Hugenholtz, P. CRISPR — a widespread system that provides acquired resistance against phages in bacteria and archaea. Nature Rev. Microbiol. 6, 181–186 (2008).

    Article  CAS  Google Scholar 

  39. Kunin, V. et al. A bacterial metapopulation adapts locally to phage predation despite global dispersal. Genome Res. 18, 293–297 (2008).

    Article  CAS  Google Scholar 

  40. Cardinale, B. J. et al. Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443, 989–992 (2006).

    Article  CAS  Google Scholar 

  41. Tylianakis, J. M., Didham, R. K., Bascompte, J. & Wardle, D. A. Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11, 1351–1363 (2008).

    Article  Google Scholar 

  42. Thompson, J. R. et al. Genotypic diversity within a natural coastal bacterioplankton population. Science 307, 1311–1313 (2005).

    Article  CAS  Google Scholar 

  43. Brown, M. V., Schwalbach, M. S., Hewson, I. & Fuhrman, J. A. Coupling 16S-ITS rDNA clone libraries and automated ribosomal intergenic spacer analysis to show marine microbial diversity: development and application to a time series. Environ. Microbiol. 7, 1466–1479 (2005).

    Article  CAS  Google Scholar 

  44. Allen, E. E. et al. Genome dynamics in a natural archaeal population. Proc. Natl Acad. Sci. USA 104, 1883–1888 (2007).

    Article  CAS  Google Scholar 

  45. Hunt, D. E. et al. Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science 320, 1081–1085 (2008).

    Article  CAS  Google Scholar 

  46. Hennes, K. P., Suttle, C. A. & Chan, A. M. Fluorescently labeled virus probes show that natural virus populations can control the structure of marine microbial communities. Appl. Environ. Microbiol. 61, 3623–3627 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Wommack, K. E., Ravel, J., Hill, R. T. & Colwell, R. R. Hybridization analysis of Chesapeake Bay virioplankton. Appl. Environ. Microbiol. 65, 241–250 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Parada, V., Baudoux, A. C., Sintes, E., Weinbauer, M. G. & Herndl, G. J. Dynamics and diversity of newly produced virioplankton in the North Sea. ISME J. 2, 924–936 (2008).

    Article  CAS  Google Scholar 

  49. Golomidova, A., Kulikov, E., Isaeva, A., Manykin, A. & Letarov, A. The diversity of coliphages and coliforms in horse feces reveals a complex pattern of ecological interactions. Appl. Environ. Microbiol. 73, 5975–5981 (2007).

    Article  CAS  Google Scholar 

  50. Holmfeldt, K., Middelboe, M., Nybroe, O. & Riemann, L. Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts. Appl. Environ. Microbiol. 73, 6730–6739 (2007).

    Article  CAS  Google Scholar 

  51. Shoresh, N., Hegreness, M. & Kishony, R. Evolution exacerbates the paradox of the plankton. Proc. Natl Acad. Sci. USA 105, 12365–12369 (2008).

    Article  CAS  Google Scholar 

  52. Wittebolle, L. et al. Initial community evenness favours functionality under selective stress. Nature 458, 623–626 (2009).

    Article  CAS  Google Scholar 

  53. Benton, T. G., Solan, M., Travis, J. M. & Sait, S. M. Microcosm experiments can inform global ecological problems. Trends Ecol. Evol. 22, 516–521 (2007).

    Article  Google Scholar 

  54. Brockhurst, M. A., Fenton, A., Roulston, B. & Rainey, P. B. The impact of phages on interspecific competition in experimental populations of bacteria. BMC Ecol. 6, 19 (2006).

    Article  Google Scholar 

  55. Maynard-Smith, J. Evolution and the Theory of Games. (Cambridge Univ. Press, Cambridge, 1982).

    Book  Google Scholar 

  56. Simmons, S. L. et al. Population genomic analysis of strain variation in Leptospirillum group II bacteria involved in acid mine drainage formation. PLoS Biol. 6, e177 (2008).

    Article  Google Scholar 

  57. Strom, S. L. Microbial ecology of ocean biogeochemistry: a community perspective. Science 320, 1043–1045 (2008).

    Article  CAS  Google Scholar 

  58. Fraser, C., Hanage, W. P. & Spratt, B. G. Recombination and the nature of bacterial speciation. Science 315, 476–480 (2007).

    Article  CAS  Google Scholar 

  59. Schoenfeld, T. et al. Assembly of viral metagenomes from Yellowstone hot springs. Appl. Environ. Microbiol. 74, 4164–4174 (2008).

    Article  CAS  Google Scholar 

  60. Konstantinidis, K. T. & Tiedje, J. M. Towards a genome-based taxonomy for prokaryotes. J. Bacteriol. 187, 6258–6264 (2005).

    Article  CAS  Google Scholar 

  61. Ochman, H., Lerat, E. & Daubin, V. Examining bacterial species under the specter of gene transfer and exchange. Proc. Natl Acad. Sci. USA 102 (Suppl. 1), 6595–6599 (2005).

    Article  CAS  Google Scholar 

  62. Read, T. D. & Ussery, D. W. Opening the pan-genomics box. Curr. Opin. Microbiol. 9, 496–498 (2006).

    Article  Google Scholar 

  63. Stent, G. S. Molecular Biology of Bacterial Viruses. (W. H. Freeman & Co, San Francisco,1963).

    Google Scholar 

  64. Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol. 5, e77 (2007).

    Article  Google Scholar 

  65. Dinsdale, E. A. et al. Functional metagenomic profiling of nine biomes. Nature 452, 629–632 (2008).

    Article  CAS  Google Scholar 

  66. Qimron, U., Marintcheva, B., Tabor, S. & Richardson, C. C. Genomewide screens for Escherichia coli genes affecting growth of T7 bacteriophage. Proc. Natl Acad. Sci. USA 103, 19039–19044 (2006).

    Article  CAS  Google Scholar 

  67. Forde, S. E., Thompson, J. N., Holt, R. D. & Bohannan, B. J. Coevolution drives temporal changes in fitness and diversity across environments in a bacteria–bacteriophage interaction. Evolution 62, 1830–1839 (2008).

    PubMed  Google Scholar 

Download references

Acknowledgements

Work in the laboratory of F.R.-V. is supported by grant BIO2008-02444 from the Spanish Ministry of Science and Innovation. A.-B.M.-C. is supported by a Juan de la Cierva postdoctoral fellowship from the Spanish Ministry of Science and Innovation. A.M. is funded by the Centro Superior de Investigación en Salud Pública (CSISP) from Generalitat Valenciana. L.P. received a European Molecular Biology Laboratory (EMBO) short-term scholarship (ASTF366-2007) during her stay in the F.R.-V. laboratory. Funding for the F.R.-V. laboratory was received from the US National Science Foundation (NSF) (DEB-BE04-21955), the Gordon and Betty Moore Foundation, an Achievement Rewards for College Scientists Fellowship, NSF Postdoctoral Fellowship number DBI-0511948 and Advanced Technology Program/Kent Sea Tech.

Author information

Authors and Affiliations

  1. Francisco Rodriguez-Valera and Ana-Belen Martin-Cuadrado are at the Departmento de Producción Vegetal y Microbiología, Universidad Miguel Hernandez, Apartado 18 San Juan de Alicante, 03550 Spain.,

    Francisco Rodriguez-Valera & Ana-Belen Martin-Cuadrado

  2. Beltran Rodriguez-Brito and Forest Rohwer are at the Department of Biology, San Diego State University, San Diego, California 92182, USA.,

    Beltran Rodriguez-Brito & Forest Rohwer

  3. Lejla Pašić is at the Department of Biology, University of Ljubljana, Večna pot111, 1000 Ljubljana, Slovenia.,

    Lejla Pašić

  4. T. Frede Thingstad is at the Department of Microbiology, University of Bergen, 5020 Bergen, Norway.,

    T. Frede Thingstad

  5. Alex Mira is at the Genomics and Health Department, Center for Advanced Research in Public Health, Avda. Cataluña 21 Valencia, 46020 Spain.,

    Alex Mira

Authors
  1. Francisco Rodriguez-Valera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana-Belen Martin-Cuadrado
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Beltran Rodriguez-Brito
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lejla Pašić
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. Frede Thingstad
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Forest Rohwer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alex Mira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Francisco Rodriguez-Valera.

Supplementary information

Supplementary information S1 (figure)

Relative frequencies of different functional categories in metagenomic islands. (PDF 332 kb)

Supplementary information S2 (table)

Metagenomic Islands found in bacterial and archaeal genomes. (PDF 619 kb)

Supplementary information S3 (figure)

Relative frequencies of different functional categories in Metagenomic Islands (MGIs) compared to their frequency in the genome. (PDF 224 kb)

Related links

Related links

DATABASES

Entrez Genome Project

Candidatus Accumulibacter phosphatis

Candidatus Pelagibacter ubique

Escherichia coli

Haloquadratum walsbyi

FURTHER INFORMATION

Francisco Rodriguez-Valera's homepage

The Mathworks

Glossary

CRISPR

A widespread genetic system in bacteria and archaea that consists of multiple copies of palindromic repeats flanking short spacers of phage origin, which are believed to provide acquired resistance against viral infection.

Kill-the-winner dynamics

A model for the population dynamics of phage–bacteria interactions that postulates that an increase in a host population (the winner) is followed by an increase in its corresponding phage predator, resulting in an increase in the rate at which the winner is killed. It is analogous to classical Lotka–Volterra dynamics to explain predator–prey population dynamics.

Metagenome

The total genetic repertoire that exists in cells and viruses from a given environment. Metagenomes are often classified according to the predominant group of microorganisms that contribute to a sequence library, for example, viruses or bacteria.

Metagenomic island

A genomic region found in a bacterial genome that is absent or present at low frequency in the DNA pool of all microbes in the native environment of that bacterium.

Pan-genome

The total gene pool of a bacterial or archaeal taxon, a pan-genome is formed by the addition of all genes found in the different strains from a given species (species pan-genome) or from an ecologically distinct population (ecotype pan-genome).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rodriguez-Valera, F., Martin-Cuadrado, AB., Rodriguez-Brito, B. et al. Explaining microbial population genomics through phage predation. Nat Rev Microbiol 7, 828–836 (2009). https://doi.org/10.1038/nrmicro2235

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro2235

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