Abstract
Cyanobacteria of the genera Synechococcus and Prochlorococcus are important contributors to photosynthetic productivity in the open ocean. The discovery of genes (psbA, psbD) that encode key photosystem II proteins (D1, D2) in the genomes of phages that infect these cyanobacteria suggests new paradigms for the regulation, function and evolution of photosynthesis in the vast pelagic ecosystem. Reports on the prevalence and expression of phage photosynthesis genes, and evolutionary data showing a potential recombination of phage and host genes, suggest a model in which phage photosynthesis genes help support photosynthetic activity in their hosts during the infection process. Here, using metagenomic data in natural ocean samples, we show that about 60% of the psbA genes in surface water along the global ocean sampling transect are of phage origin, and that the phage genes are undergoing an independent selection for distinct D1 proteins. Furthermore, we show that different viral psbA genes are expressed in the environment.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Adir N, Zer H, Shochat S, Ohad I . (2003). Photoinhibition—a historical perspective. Photosyn Res 76: 343–370.
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.
Angly F, Felts B, Breitbart M, Salamon P, Edwards R, Carlson C et al. (2006). The marine viromes of four oceanic regions. PLoS Biol 4: e368.
Brussow H, Hendrix RW . (2002). Phage genomics: small is beautiful. Cell 108: 13–16.
Casjens SR, Gilcrease EB, Huang WM, Bunny KL, Pedulla ML, Ford ME et al. (2004). The pKO2 linear plasmid prophage of Klebsiella oxytoca. J Bacteriol 186: 1818–1832.
Chen F, Lu J . (2002). Genomic sequence and evolution of marine cyanophage P60: a new insight on lytic and lysogenic phages. Appl Environ Microbiol 68: 2589–2594.
Chow WS, Aro EM . (2005). Photoinactivation and mechanisms of recovery. In: Wydrzynki T, Satoh K (eds). Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase. Springer, The Netherlands. Springer: Dordrecht, The Netherlands, pp 627–648.
Clarke AK, Soitamo A, Gustafsson P, Oquist G . (1993). Rapid interchange between two distinct forms of cyanobacterial photosystem II reaction-center protein D1 in response to photoinhibition. Proc Natl Acad Sci USA 90: 9973–9977.
Clokie MR, Shan J, Bailey S, Jia Y, Krisch HM, West S et al. (2006). Transcription of a ‘photosynthetic’ T4-type phage during infection of a marine cyanobacterium. Environ Microbiol 8: 827–835.
Clokie MRJ, Mann NH . (2006). Marine cyanophages and light. Environ Microbiol 8: 2074–2082.
Debus R . (2001). Amino acid residues that modulate the properties of tyrosine Y(Z) and the manganese cluster in the water oxidizing complex of photosystem II. Biochim Biophys Acta 5: 164–186.
DeLong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard N-U et al. (2006). Community genomics among stratified microbial assemblages in the Ocean's interior. Science 311: 496–503.
Edelman M, Mattoo AK . (2006). The D1 protein: past and future perspectives. In: Demmig-Adams B, Adams WW, Mattoo AK (eds). Photoprotection, Photoinhibition, Gene Regulation, and Environment. Springer: Germany, pp 23–38.
Felsenstein J . (2005). PHYLIP (phylogeny inference package), version 3.6. Department of Genome Sciences, University of Washington, Seattle.
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S . (2004). Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831–1838.
Greenberg BM, Gaba V, Mattoo AK, Edelman M . (1987). Identification of a primary in vivo degradation product of the rapidly-turning-over 32 kd protein of photosystem II. EMBO J 6: 2865–2869.
Jolliffe IT . (1986). Principal Component Analysis. Springer: New York.
Kunik V, Meroz Y, Solan Z, Sandbank B, Weingart U, Ruppin E et al. (2007). Functional representation of enzymes by specific peptides. PLoS Comput Biol (in press).
Li WKW . (1995). Composition of ultraphytoplankton in the central North Atlantic. Mar Ecol Prog Ser 122: 1–8.
Lindell D, Jaffe JD, Johnson ZI, Church GM, Chisholm SW . (2005). Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438: 86–89.
Lindell D, Sullivan MB, Johnson ZI, Tolonen AC, Rohwer F, Chisholm SW . (2004). Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci USA 101: 11013–11018.
Man-Aharonovich D, Kress N, Bar Zeev E, Berman-Frank I, Béjà O . (2007). Molecular ecology of nifH genes and transcripts in Eastern Mediterranean Sea. Environ Microbiol (online early articles doi:10.1111/j.1462-2920.2007.01353.x).
Mann NH, Clokie MRJ, Millard A, Cook A, Wilson WH, Wheatley PG et al. (2005). The genome of S-PM2, a ‘photosynthetic’ T4-type bacteriophage that infects marine Synechococcus strains. J Bacteriol 187: 3188–3200.
Mann NH, Cook A, Millard A, Bailey S, Clokie M . (2003). Bacterial photosynthesis genes in a virus. Nature 424: 741.
Massana R, Murray AE, Preston CM, DeLong ED . (1997). Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara channel. Appl Environ Microbiol 63: 50–56.
Millard A, Clokie MRJ, Shub DA, Mann NH . (2004). Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc Natl Acad Sci USA 101: 11007–11012.
Mrazek J, Karlin S . (2007). Distinctive features of large complex virus genomes and proteomes. Proc Natl Acad Sci USA 104: 5127–5132.
Nixon PJ, Trost JT, Diner BA . (1992). Role of the carboxy terminus of polypeptide D1 in the assembly of a functional water-oxidizing manganese cluster in photosystem II of the cyanobacterium Synechocystis sp. PCC 6803 assembly requires a free carboxyl group at C-terminal position 344. Biochemistry 31: 10859–10871.
Partensky F, Hess WR, Vaulot D . (1999). Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106–127.
Rusch DB, Halpern AL, Heidelberg KB, Sutton G, Williamson SJ, Yooseph S et al. (2007). The Sorcerer II Global Ocean Sampling expedition: I, The northwest Atlantic through the eastern tropical Pacific. PLoS Biol 5: e77.
Schaefer MR, Golden SS . (1989). Light availability influences the ratio of two forms of D1 in cyanobacterial thylakoids. J Biol Chem 264: 7412–7417.
Solan Z, Horn D, Ruppin E, Edelman S . (2005). Unsupervised learning of natural languages. Proc Natl Acad Sci USA 102: 11629–11634.
Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW . (2005). Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3: e144.
Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW . (2006). Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4: e234.
Suorsa M, Regel RE, Paakkarinen V, Battchikova N, Herrmann RG, Aro EM . (2004). Protein assembly of photosystem II and accumulation of subcomplexes in the absence of low molecular mass subunits PsbL and PsbJ. Eur J Biochem 271: 96–107.
Suttle CA . (2005). Viruses in the sea. Nature 437: 356–361.
Tavazoie S, Hughes JD, Campbell MJ, Cho RJ, Church GM . (1999). Systematic determination of genetic network architecture. Nat Genet 22: 281–285.
Venter JC, Remington K, Heidelberg J, Halpern AL, Rusch D, Eisen JA et al. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66–74.
Waterbury JB, Watson SW, Valois FW, Franks DG . (1986). Biological and ecological characterization of the marine unicellular cyanobacterium Synechococcus. Can Bull Fish Aquat Sci 214: 71–120.
Yooseph S, Sutton G, Rusch DB, Halpern AL, Williamson SJ, Remington K et al. (2007). The Sorcerer II Global Ocean Sampling Expedition: expanding the universe of protein families. PLoS Biol 5: e16.
Yutin N, Suzuki MT, Teeling H, Weber M, Venter JC, Rusch D et al. (2007). Assessing diversity and biogeography of aerobic anoxygenic phototrophic bacteria in surface waters of the Atlantic and Pacific Oceans using the Global Ocean sampling expedition metagenomes. Environ Microbiol 9: 1464–1475.
Zeidner G, Bielawski JP, Shmoish M, Scanlan DJ, Sabehi G, Béjà O . (2005). Potential photosynthesis gene recombination between Prochlorococcus & Synechococcus via viral intermediates. Environ Microbiol 7: 1505–1513.
Zeidner G, Preston CM, Delong EF, Massana R, Post AF, Scanlan DJ et al. (2003). Molecular diversity among marine picophytoplankton as revealed by psbA analyses. Environ Microbiol 5: 212–216.
Acknowledgements
We thank E DeLong, M Sullivan, D Lindell, S Chisholm and F Rohwer for the ability to use data before publication, and the captain and crew of the RV Shikmona for their expert assistance at sea. We also thank the governments of Canada, Mexico, Honduras, Costa Rica, Panama, Ecuador and French Polynesia/France for facilitating sampling activities. All sequencing data collected from waters of the above countries remain part of the genetic patrimony of the country from which they were obtained. This work was supported by a grant from the Israel Science Foundation, a grant from the Israeli Ministry of Science and Technology, an EMBO YIP award (OB), a COBI grant from the Israeli Ministry of Science and Technology (MS), grants from the US Department of Energy Office of Science's Biological and Environmental Research Program grant and the Gordon and Betty Moore Foundation (J Craig Venter Institute).
Author information
Authors and Affiliations
Corresponding author
Additional information
Supplementary Information accompanies the paper on The ISME Journal website (http://www.nature.com/ismej)
Supplementary information
Rights and permissions
About this article
Cite this article
Sharon, I., Tzahor, S., Williamson, S. et al. Viral photosynthetic reaction center genes and transcripts in the marine environment. ISME J 1, 492–501 (2007). https://doi.org/10.1038/ismej.2007.67
Received:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2007.67
Keywords
This article is cited by
-
Potential virus-mediated nitrogen cycling in oxygen-depleted oceanic waters
The ISME Journal (2021)
-
Survey of the bacteriophage phoH gene in wetland sediments in northeast China
Scientific Reports (2019)
-
Visualizing Adsorption of Cyanophage P-SSP7 onto Marine Prochlorococcus
Scientific Reports (2017)
-
Narrow distribution of cyanophage psbA genes observed in two paddy waters of Northeast China by an incubation experiment
Virologica Sinica (2016)
-
Diversity of viral photosystem-I psaA genes
The ISME Journal (2015)