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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Protein Data Bank
The PSI sequences reported here have been deposited with GenBank under accession numbers EU926752–EU926761(overlapping PCRs) and GQ268816 (long PCR).
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)
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)
Partensky, F., Hess, W. R. & Vaulot, D. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63, 106–127 (1999)
Mann, N. H., Cook, A., Millard, A., Bailey, S. & Clokie, M. Bacterial photosynthesis genes in a virus. Nature 424, 741 (2003)
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)
Lindell, D. et al. Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc. Natl Acad. Sci. USA 101, 11013–11018 (2004)
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)
Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through the eastern tropical Pacific. PLoS Biol. 5, e77 (2007)
Dinsdale, E. A. et al. Functional metagenomic profiling of nine biomes. Nature 452, 629–632 (2008)
Jordan, P. et al. Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411, 909–917 (2001)
Rohwer, F. & Thurber, R. V. Viruses manipulate the marine environment. Nature 459, 207–212 (2009)
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)
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)
Sharon, I. et al. Viral photosynthetic reaction center genes and transcripts in the marine environment. ISME J. 1, 492–501 (2007)
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)
Harismendy, O. et al. Evaluation of next generation sequencing platforms for population targeted sequencing studies. Genome Biol. 10, R32 (2009)
Dinsdale, E. A. et al. Microbial ecology of four coral atolls in the northern line islands. PLoS One 3, e1584 (2008)
Ben-Shem, A., Frolow, F. & Nelson, N. The crystal structure of plant photosystem I. Nature 426, 630–635 (2003)
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)
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)
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)
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)
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)
Nelson, N. & Yocum, C. Structure and function of photosystems I and II. Annu. Rev. Plant Biol. 57, 521–565 (2006)
Merchant, S. & Sawaya, M. R. The light reactions: a guide to recent acquisitions for the picture gallery. Plant Cell 17, 648–663 (2005)
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)
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)
Bailey, S. et al. Alternative photosynthetic electron flow to oxygen in marine Synechococcus . Biochim. Biophys. Acta 1777, 269–276 (2008)
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)
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)
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.
This file contains Supplementary Methods, Supplementary Data, Supplementary Tables S1-S5, Supplementary Figures S1-S2 with Legends and Supplementary References. (PDF 629 kb)
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). https://doi.org/10.1038/nature08284
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