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.

Photosynthesis genes in marine viruses yield proteins during host infection

Nature volume 438, pages 86–89 (2005)Cite this article

Abstract

Cyanobacteria, and the viruses (phages) that infect them, are significant contributors to the oceanic ‘gene pool’1,2. This pool is dynamic, and the transfer of genetic material between hosts and their phages3,4,5,6 probably influences the genetic and functional diversity of both. For example, photosynthesis genes of cyanobacterial origin have been found in phages that infect Prochlorococcus5,7 and Synechococcus8,9, the numerically dominant phototrophs in ocean ecosystems. These genes include psbA, which encodes the photosystem II core reaction centre protein D1, and high-light-inducible (hli) genes. Here we show that phage psbA and hli genes are expressed during infection of Prochlorococcus and are co-transcribed with essential phage capsid genes, and that the amount of phage D1 protein increases steadily over the infective period. We also show that the expression of host photosynthesis genes declines over the course of infection and that replication of the phage genome is a function of photosynthesis. We thus propose that the phage genes are functional in photosynthesis and that they may be increasing phage fitness by supplementing the host production of these proteins.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Photosynthesis and phage infection.
Figure 2: Expression of phage and host photosynthesis genes.
Figure 3: Analysis of host and phage peptides.
Figure 4: Co-transcription of phage photosynthesis and capsid genes.

References

  1. Breitbart, M. et al. Genomic analysis of uncultured marine viral communities. Proc. Natl Acad. Sci. USA 99, 14250–14255 (2002)

    Article  ADS  CAS  Google Scholar 

  2. Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004)

    Article  ADS  CAS  Google Scholar 

  3. Canchaya, C., Fournous, G., Chibani-Chennoufi, S., Dillmann, M. L. & Brussow, H. Phage as agents of lateral gene transfer. Curr. Opin. Microbiol. 6, 417–424 (2003)

    Article  CAS  Google Scholar 

  4. Palenik, B. et al. The genome of a motile marine Synechococcus. Nature 424, 1037–1042 (2003)

    Article  ADS  CAS  Google Scholar 

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

    Article  Google Scholar 

  6. 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  Google Scholar 

  7. 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  Google Scholar 

  8. Mann, N. H., Cook, A., Millard, A., Bailey, S. & Clokie, M. Bacterial photosynthesis genes in a virus. Nature 424, 741 (2003)

    Article  ADS  CAS  Google Scholar 

  9. Millard, A., Clokie, M. R. J., 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  Google Scholar 

  10. Adir, N., Zer, H., Shochat, S. & Ohad, I. Photoinhibition—a historical perspective. Photosynth. Res. 76, 343–370 (2003)

    Article  CAS  Google Scholar 

  11. Havaux, M., Guedeney, G., He, Q. & Grossman, A. R. Elimination of high-light-inducible polypeptides related to eukaryotic chlorophyll a/b-binding proteins results in aberrant photoacclimation in Synechocystis PCC6803. Biochim. Biophys. Acta 1557, 21–33 (2003)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Adolph, K. W. & Haskelkorn, R. Photosynthesis and the development of blue–green algal virus N-1. Virology 47, 370–374 (1972)

    Article  CAS  Google Scholar 

  14. MacKenzie, J. J. & Haselkorn, R. Photosynthesis and the development of blue–green algal virus SM-1. Virology 49, 517–521 (1972)

    Article  CAS  Google Scholar 

  15. Sherman, L. A. Infection of Synechococcus cedrorum by the cyanophage AS-1M. Virology 71, 199–206 (1976)

    Article  CAS  Google Scholar 

  16. Suttle, C. A. & Chan, A. M. Marine cyanophages infecting oceanic and coastal strains of Synechococcus—abundance, morphology, cross-infectivity and growth-characteristics. Mar. Ecol. Prog. Ser. 92, 99–109 (1993)

    Article  ADS  Google Scholar 

  17. Ginzburg, D., Padan, E. & Shilo, M. Effect of cyanophage infection on CO2 photoassimilation in Plectonema boryanum. J. Virol. 2, 695–701 (1968)

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Rahoutei, J., Garcia-Luque, I. & Baron, M. Inhibitioin of photosynthesis by viral infection: effect on PSII structure and function. Physiol. Plant. 110, 286–292 (2000)

    Article  CAS  Google Scholar 

  19. Arias, M. C., Lenardon, S. & Taleisnik, E. Carbon metabolism alterations in sunflower plants infected with the sunflower chlorotic mottle virus. J. Phytopath. 151, 267–273 (2003)

    Article  CAS  Google Scholar 

  20. Xu, H., Vavilin, D., Funk, C. & Vermaas, W. Multiple deletions of small Cab-like proteins in the cyanobacterium Synechocystis sp. PCC 6803—consequences for pigment biosynthesis and accumulation. J. Biol. Chem. 279, 27971–27979 (2004)

    Article  CAS  Google Scholar 

  21. Bruyant, F. et al. Diel variations in the photosynthetic parameters of Prochlorococcus strain PCC 9511: combined effects of light and cell cycle. Limnol. Oceanogr. 50, 850–863 (2005)

    Article  ADS  Google Scholar 

  22. 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  Google Scholar 

  23. 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 

  24. Sullivan, M. B., Waterbury, J. B. & Chisholm, S. W. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424, 1047–1051 (2003)

    Article  ADS  CAS  Google Scholar 

  25. Moore, L. R., Post, A. F., Rocap, G. & Chisholm, S. W. Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnol. Oceanogr. 47, 989–996 (2002)

    Article  ADS  CAS  Google Scholar 

  26. Zinser, E. R. et al. Prochlorococcus ecotype abundance in the North Atlantic Ocean revealed by an improved quantitative PCR method. Appl. Environ. Microbiol. (in the press)

  27. Johnson, Z. I. Development and application of the background irradiance gradient–single turnover fluorometer (BIG-STf). Mar. Ecol. Prog. Ser. 283, 73–80 (2004)

    Article  ADS  Google Scholar 

  28. Kolber, Z. S., Prasil, O. & Falkowski, P. G. Measurements of variable chlorophyll fluorescence using fast repetition rate techniques—defining methodology and experimental protocols. Biochim. Biophys. Acta 1367, 88–106 (1998)

    Article  CAS  Google Scholar 

  29. Gerber, S. A., Rush, J., Stemman, O., Kirschner, M. W. & Gygi, S. P. Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc. Natl Acad. Sci. USA 100, 6940–6945 (2003)

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank T. Rector and R. Steen for doing the Affymetrix GeneChip experiments; C. Steglich, M. Sullivan, M. Coleman, and E. Zinser for discussions; and M. Sullivan for comments on the manuscript. This research was supported by grants from the National Science Foundation (to S.W.C.), the Gordon and Betty Moore Foundation's Program in Marine Microbiology (to S.W.C), and the Department of Energy Genomes to Life Program (to S.W.C and G.M.C.).

Author information

Author notes

  1. Jacob D. Jaffe

    Present address: The Broad Institute of Harvard and MIT, Cambridge, Massachusetts, 02141, USA

  2. Zackary I. Johnson

    Present address: Department of Oceanography, University of Hawaii, 1000 Pope Road, Honolulu, Hawaii, 96822, USA

Authors and Affiliations

  1. Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Massachusetts, 02139, Cambridge, USA

    Debbie Lindell, Zackary I. Johnson & Sallie W. Chisholm

  2. Department of Genetics, Harvard Medical School, Massachusetts, 02115, Boston, USA

    Jacob D. Jaffe & George M. Church

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

    Sallie W. Chisholm

Authors
  1. Debbie Lindell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jacob D. Jaffe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zackary I. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. George M. Church
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sallie W. Chisholm
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sallie W. Chisholm.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Table S1

This table provides the nucleotide sequences of the primers used in RT and real-time PCR reactions. (DOC 40 kb)

Supplementary Figure S1

This figure shows transcript levels of the phage and host psbA genes during infection as determined by RT-PCR. These results show that the expression of the phage psbA gene increases with time during infection while host psbA expression declines. These results confirm those from microarray analysis presented in Fig. 2a. (DOC 43 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lindell, D., Jaffe, J., Johnson, Z. et al. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438, 86–89 (2005). https://doi.org/10.1038/nature04111

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature04111

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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