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Photosystem I gene cassettes are present in marine virus genomes

Nature volume 461, pages 258–262 (2009)Cite this article

Abstract

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).

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Acknowledgements

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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Author notes

  1. Itai Sharon and Ariella Alperovitch: These authors contributed equally to this work.

Authors and Affiliations

  1. Faculty of Biology,,

    Itai Sharon, Ariella Alperovitch, Nof Atamna-Ismaeel & Oded Béjà

  2. Faculty of Computer Science,,

    Itai Sharon & Ron Y. Pinter

  3. Bioinformatics Knowledge Unit, Lorry I. Lokey Interdisciplinary Center for Life Sciences and Engineering, Technion-Israel Institute of Technology, Haifa 32000, Israel ,

    Fabian Glaser

  4. Department of Biology,,

    Forest Rohwer & Matthew Haynes

  5. Center for Microbial Sciences, San Diego State University, San Diego, California 92182, USA ,

    Forest Rohwer

  6. CNRS and UPMC-Université Paris 6 (UMR 7144), Station Biologique, 29682 Roscoff, France ,

    Frédéric Partensky

  7. National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland 20894, USA ,

    Eugene V. Koonin & Yuri I. Wolf

  8. Department of Biochemistry, George S. Wise Faculty of Life Sciences, Daniella Rich Institute for Structural Biology, Tel Aviv University, Tel Aviv 69978, Israel

    Nathan Nelson

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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). https://doi.org/10.1038/nature08284

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