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Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution

Nature volume 449, pages 83–86 (2007)Cite this article

Abstract

Interactions between bacterial hosts and their viruses (phages) lead to reciprocal genome evolution through a dynamic co-evolutionary process1,2,3,4,5. Phage-mediated transfer of host genes—often located in genome islands—has had a major impact on microbial evolution1,4,6. Furthermore, phage genomes have clearly been shaped by the acquisition of genes from their hosts2,3,5. Here we investigate whole-genome expression of a host and phage, the marine cyanobacterium Prochlorococcus MED4 and the T7-like cyanophage P-SSP7, during lytic infection, to gain insight into these co-evolutionary processes. Although most of the phage genome was linearly transcribed over the course of infection, four phage-encoded bacterial metabolism genes formed part of the same expression cluster, even though they are physically separated on the genome. These genes—encoding photosystem II D1 (psbA), high-light inducible protein (hli), transaldolase (talC) and ribonucleotide reductase (nrd)—are transcribed together with phage DNA replication genes and seem to make up a functional unit involved in energy and deoxynucleotide production for phage replication in resource-poor oceans. Also unique to this system was the upregulation of numerous genes in the host during infection. These may be host stress response genes and/or genes induced by the phage. Many of these host genes are located in genome islands and have homologues in cyanophage genomes. We hypothesize that phage have evolved to use upregulated host genes, leading to their stable incorporation into phage genomes and their subsequent transfer back to hosts in genome islands. Thus activation of host genes during infection may be directing the co-evolution of gene content in both host and phage genomes.

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Figure 1: Infection dynamics of Prochlorococcus MED4 by podovirus P-SSP7.
Figure 2: Temporal expression dynamics of P-SSP7 phage genes during infection of Prochlorococcus MED4.
Figure 3: Transcriptional profiles of Prochlorococcus MED4 genes with time after infection by P-SSP7.

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References

  1. Canchaya, C., Proux, C., Fournous, G., Bruttin, A. & Brussow, H. Prophage genomics. Microbiol. Mol. Biol. Rev. 67, 238–276 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Filee, J., Forterre, P. & Laurent, J. The role played by viruses in the evolution of their hosts: a view based on informational protein phylogenies. Res. Microbiol. 154, 237–243 (2003)

    Article  CAS  PubMed  Google Scholar 

  3. Hendrix, R. W., Lawrence, J. G., Hatfull, G. F. & Casjens, S. The origins and ongoing evolution of viruses. Trends Microbiol. 8, 504–508 (2000)

    Article  CAS  PubMed  Google Scholar 

  4. Hsiao, W. W. L. et al. Evidence of a large novel gene pool associated with prokaryotic genome islands. PLoS Genet. 1, e62 (2006)

    Article  Google Scholar 

  5. Lindell, D. et al. Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc. Natl Acad. Sci. USA 101, 11013–11018 (2004)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  ADS  CAS  PubMed  Google Scholar 

  7. Partensky, F., Hess, W. R. & Vaulot, D. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63, 106–127 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Breitbart, M., Miyake, J. H. & Rohwer, F. Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol. Lett. 236, 249–256 (2004)

    Article  CAS  PubMed  Google Scholar 

  9. Mann, N. H. et al. The genome of S-PM2, a “photosynthetic” T4-type bacteriophage that infects marine Synechococcus. J. Bacteriol. 187, 3188–3200 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Millard, A., Clokie, M. R., Shub, D. A. & Mann, N. H. Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc. Natl Acad. Sci. USA 101, 11007–11012 (2004)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  11. Sullivan, M. B., Coleman, M., Weigele, P., Rohwer, F. & Chisholm, S. W. Three Prochlorococcus cyanophage genomes: Signature features and ecological interpretations. PLoS Biol. 3, e144 (2005)

    Article  PubMed  PubMed Central  Google Scholar 

  12. Lindell, D., Jaffe, J. D., Johnson, Z. I., Church, G. M. & Chisholm, S. W. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438, 86–89 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  13. Clokie, M. R. J., Shan, J., Bailey, S., Jia, Y. & Krisch, H. M. Transcription of a 'photosynthetic' T4-type phage during infection of a marine cyanobacterium. Environ. Microbiol. 8, 827–835 (2006)

    Article  CAS  PubMed  Google Scholar 

  14. Zeidner, G. et al. Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ. Microbiol. 7, 1505–1513 (2005)

    Article  CAS  PubMed  Google Scholar 

  15. Sullivan, M. B. et al. Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol. 4, e234 (2006)

    Article  PubMed  PubMed Central  Google Scholar 

  16. Molineux, I. in The Bacteriophages (ed. Calendar, R.) 277–301 (Oxford University Press, New York, 2005)

    Google Scholar 

  17. Chen, Z. & Schneider, T. D. Information theory based T7-like promoter models: classification of bacteriophages and differential evolution of promoters and their polymerases. Nucleic Acids Res. 33, 6172–6187 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Miller, E. S. et al. Bacteriophage T4 genome. Microbiol. Mol. Biol. Rev. 67, 86–156 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lenski, R. E. & Levin, B. R. Constraints on the coevolution of bacteria and virulent phage: A model, some experiments, and predictions for natural communities. Am. Nat. 124, 585–602 (1985)

    Article  Google Scholar 

  20. Tabor, S., Huber, H. E. & Richardson, C. C. Escherichia coli thioredoxin confers processivity on the DNA polymerase activity of the gene 5 protein of bacteriophage T7. J. Biol. Chem. 262, 16212–16223 (1987)

    CAS  PubMed  Google Scholar 

  21. Tilly, K., Murialdo, H. & Georgopoulos, C. P. Identification of a second Escherichia coli groE gene whose product is necessary for bacteriophage morphogenesis. Proc. Natl Acad. Sci. USA 78, 1629–1633 (1981)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ueno, H. & Yonesaki, T. Phage-induced change in the stability of mRNAs. Virology 329, 134–141 (2004)

    Article  CAS  PubMed  Google Scholar 

  23. Tolonen, A. C. et al. Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability. Mol. Systems Biol. 2, 53 (2006)

    Article  Google Scholar 

  24. Irizarry, R. A. et al. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15 (2003)

    Article  PubMed  PubMed Central  Google Scholar 

  25. Jaffe, J. D. et al. The complete genome and proteome of Mycoplasma mobile. Genome Res. 14, 1447–1461 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank C. Steglich, S. Bhattacharya, H. Keller, L. Thompson, P. Weigele, S. Choe, D. Endy, S. Kosuri, M. Shmoish and J. Aach for discussions, and J. Waldbauer and M. Osburne for comments on the manuscript, and the MIT Center for Environmental Health Sciences. This work was funded by the DOE Genomes to Life System Biology Center Grant (G.M.C. and S.W.C.), the Gordon and Betty Moore Foundation’s Marine Microbiology Program (S.W.C.), and the National Science Foundation (S.W.C).

The microarray data have been deposited in the GEO database under the accession number GSE8382.

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Author notes

  1. Debbie Lindell & Jacob D. Jaffe

    Present address: Present addresses: Department of Biology, Technion—Israel Institute of Technology, Haifa 32000, Israel (D.L.); The Broad Institute of Harvard and MIT, Cambridge, Massachusetts 02141, USA (J.D.J).,

Authors and Affiliations

  1. Department of Civil and Environmental Engineering,

    Debbie Lindell, Maureen L. Coleman, Gregory Kettler, Matthew B. Sullivan & Sallie W. Chisholm

  2. Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA,

    Sallie W. Chisholm

  3. Department of Genetics,

    Jacob D. Jaffe & George M. Church

  4. Department of Genetics Harvard Medical School, BioPolymers Facility, Boston, Massachusetts 02115, USA,

    Trent Rector & Robert Steen

  5. Institute for Theoretical Biology, Humboldt University, Berlin 10115, Germany

    Matthias E. Futschik & Ilka M. Axmann

  6. Institute of Biology, University of Freiburg, Freiburg 79104, Germany

    Wolfgang R. Hess

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Correspondence to Sallie W. Chisholm.

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Supplementary information

Supplementary Information

This file contains Supplementary Methods with details of the experimental methodology and additional references; Supplementary Tables 1-8 and Supplementary Figures 1-10 with Legends showing proteomic and promoter results, list of upregulated host genes, phage gene expression cluster analysis and significance, hli gene expression table, RT-PCR verification of microarray results and normalization methods, comparison of phage quantification methods to quantitative PCR results and lists of primers used in this study (PDF 1691 kb)

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Lindell, D., Jaffe, J., Coleman, M. et al. Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449, 83–86 (2007). https://doi.org/10.1038/nature06130

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