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Photosystem I gene cassettes are present in marine virus genomes


Cyanobacteria of the Synechococcus and Prochlorococcus genera are important contributors to photosynthetic productivity in the open oceans1,2,3. Recently, core photosystem II (PSII) genes were identified in cyanophages and proposed to function in photosynthesis and in increasing viral fitness by supplementing the host production of these proteins4,5,6,7. Here we show evidence for the presence of photosystem I (PSI) genes in the genomes of viruses that infect these marine cyanobacteria, using pre-existing metagenomic data from the global ocean sampling expedition8 as well as from viral biomes9. The seven cyanobacterial core PSI genes identified in this study, psaA, B, C, D, E, K and a unique J and F fusion, form a cluster in cyanophage genomes, suggestive of selection for a distinct function in the virus life cycle. The existence of this PSI cluster was confirmed with overlapping and long polymerase chain reaction on environmental DNA from the Northern Line Islands. Potentially, the seven proteins encoded by the viral genes are sufficient to form an intact monomeric PSI complex. Projection of viral predicted peptides on the cyanobacterial PSI crystal structure10 suggested that the viral–PSI components might provide a unique way of funnelling reducing power from respiratory and other electron transfer chains to the PSI.

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Figure 1: A maximum-likelihood phylogenetic tree of psaA -deduced amino acid sequences obtained from the GOS expedition.
Figure 2: Schematic physical maps of selected viral-suspected GOS clones (top), Prochlorococcus and Synechococcus genomes (middle) and environmental PCR products containing PSI genes (bottom).
Figure 3: Distribution of neighbouring genes involving at least one PSI gene.
Figure 4: Recruitment of GOS clones carrying PSI genes with Northern Line Islands biomes.
Figure 5: Structural consequences of assembling the viral fusion protein PsaJF into PSI.

Accession codes

Primary accessions

Protein Data Bank

Data deposits

The PSI sequences reported here have been deposited with GenBank under accession numbers EU926752–EU926761(overlapping PCRs) and GQ268816 (long PCR).


  1. 1

    Li, W. K. W., Zohary, T., Yacobi, Y. Z. & Wood, A. M. Ultraphytoplankton in the eastern Mediterranean Sea: towards deriving phytoplankton biomass from flow cytometric measurements of abundance, fluorescence and light scatter. Mar. Ecol. Prog. Ser. 102, 79–87 (1993)

    Article  Google Scholar 

  2. 2

    Liu, H., Nolla, H. A. & Campbell, L. Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquat. Microb. Ecol. 12, 39–47 (1997)

    Article  Google Scholar 

  3. 3

    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 

  4. 4

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

    ADS  CAS  Article  Google Scholar 

  5. 5

    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)

    ADS  CAS  Article  Google Scholar 

  6. 6

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

    ADS  CAS  Article  Google Scholar 

  7. 7

    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)

    ADS  CAS  Article  Google Scholar 

  8. 8

    Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through the eastern tropical Pacific. PLoS Biol. 5, e77 (2007)

    Article  Google Scholar 

  9. 9

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

    ADS  CAS  Article  Google Scholar 

  10. 10

    Jordan, P. et al. Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411, 909–917 (2001)

    ADS  CAS  Article  Google Scholar 

  11. 11

    Rohwer, F. & Thurber, R. V. Viruses manipulate the marine environment. Nature 459, 207–212 (2009)

    ADS  CAS  Article  Google Scholar 

  12. 12

    Brown, N. F., Wickham, M. E., Coombes, B. K. & Finlay, B. B. Crossing the line: selection and evolution of virulence traits. PLoS Pathog. 2, e42 (2006)

    Article  Google Scholar 

  13. 13

    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  Google Scholar 

  14. 14

    Sharon, I. et al. Viral photosynthetic reaction center genes and transcripts in the marine environment. ISME J. 1, 492–501 (2007)

    CAS  Article  Google Scholar 

  15. 15

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

    Article  Google Scholar 

  16. 16

    Harismendy, O. et al. Evaluation of next generation sequencing platforms for population targeted sequencing studies. Genome Biol. 10, R32 (2009)

    Article  Google Scholar 

  17. 17

    Dinsdale, E. A. et al. Microbial ecology of four coral atolls in the northern line islands. PLoS One 3, e1584 (2008)

    ADS  Article  Google Scholar 

  18. 18

    Ben-Shem, A., Frolow, F. & Nelson, N. The crystal structure of plant photosystem I. Nature 426, 630–635 (2003)

    ADS  CAS  Article  Google Scholar 

  19. 19

    Naithani, S., Hou, J. M. & Chitnis, P. R. Targeted inactivation of the psaK1, psaK2 and psaM genes encoding subunits of Photosystem I in the cyanobacterium Synechocystis sp. PCC 6803. Photosynth. Res. 63, 225–236 (2000)

    CAS  Article  Google Scholar 

  20. 20

    Xu, Q. et al. Mutational analysis of photosystem I polypeptides in the cyanobacterium Synechocystis sp. PCC 6803. Targeted inactivation of psaI reveals the function of psaI in the structural organization of psaL. J. Biol. Chem. 270, 16243–16250 (1995)

    CAS  Article  Google Scholar 

  21. 21

    Kouril, R., van Oosterwijk, N., Yakushevska, A. E. & Boekema, E. J. Photosystem I: a search for green plant trimers. Photochem. Photobiol. Sci. 4, 1091–1094 (2005)

    CAS  Article  Google Scholar 

  22. 22

    Boekema, E. J. et al. Evidence for a trimeric organization of the photosystem I complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett. 217, 283–286 (1987)

    CAS  Article  Google Scholar 

  23. 23

    Hippler, M., Drepper, F., Farah, J. & Rochaix, J. D. Fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii requires PsaF. Biochemistry 36, 6343–6349 (1997)

    CAS  Article  Google Scholar 

  24. 24

    Nelson, N. & Yocum, C. Structure and function of photosystems I and II. Annu. Rev. Plant Biol. 57, 521–565 (2006)

    CAS  Article  Google Scholar 

  25. 25

    Merchant, S. & Sawaya, M. R. The light reactions: a guide to recent acquisitions for the picture gallery. Plant Cell 17, 648–663 (2005)

    CAS  Article  Google Scholar 

  26. 26

    Kerfeld, C. A. & Krogmann, D. W. Photosynthetic cytochromes c in cyanobacteria, algae and plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 397–425 (1998)

    CAS  Article  Google Scholar 

  27. 27

    Rumeau, D., Peltier, G. & Cournac, L. Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ. 30, 1041–1051 (2007)

    CAS  Article  Google Scholar 

  28. 28

    Bailey, S. et al. Alternative photosynthetic electron flow to oxygen in marine Synechococcus . Biochim. Biophys. Acta 1777, 269–276 (2008)

    CAS  Article  Google Scholar 

  29. 29

    Partensky, F., La Roche, J., Wyman, K. & Falkowski, P. G. The divinyl-chlorophyll a/b-protein complexes of two strains of the oxyphototrophic marine prokaryote Prochlorococcus—characterization and response to changes in growth irradiance. Photosynth. Res. 51, 209–222 (1997)

    CAS  Article  Google Scholar 

  30. 30

    Dammeyer, T., Bagby, S. C., Sullivan, M. B., Chisholm, S. W. & Frankenberg-Dinkel, N. Efficient phage-mediated pigment biosynthesis in oceanic cyanobacteria. Curr. Biol. 18, 442–448 (2008)

    CAS  Article  Google Scholar 

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We would like to thank M. Rosenberg for technical support, D. Rusch, J. Zehr and S. Bench for sharing genomic data, D. Lindell and R. Sorek for encouragement and discussions, and U. Pick for the comments on cyclic photosynthesis. This work was supported in part by grants 1203/06 (O.B.) and 356/06 (N.N.) from the Israel Science Foundation, by the Henry Taub Award for Academic Excellence, and by the Technion V.P.R. Fund-Henri Gutwirth Promotion of Research Fund (O.B.).

Author Contributions A.A. devised the initial idea for the project. I.S. and O.B. conceived the experiments. I.S. wrote the code and analysed the raw data, and together with F.G., R.Y.P., E.V.K., Y.I.W., N.N. and O.B. performed the bioinformatics. F.R. collected DNA and phage concentrates from the Northern Line Islands. A.A., N.A.-I. and M.H. conducted the molecular biology experiments, I.S., F.P., E.V.K., N.N. and O.B. co-wrote the paper.

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Correspondence to Oded Béjà.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Data, Supplementary Tables S1-S5, Supplementary Figures S1-S2 with Legends and Supplementary References. (PDF 629 kb)

Supplementary Data S1

Fasta file with sequences of the different viral GOS scaffolds and reads described in the study. (XLS 46 kb)

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Sharon, I., Alperovitch, A., Rohwer, F. et al. Photosystem I gene cassettes are present in marine virus genomes. Nature 461, 258–262 (2009).

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