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A myovirus encoding both photosystem I and II proteins enhances cyclic electron flow in infected Prochlorococcus cells

Abstract

Cyanobacteria are important contributors to primary production in the open oceans. Over the past decade, various photosynthesis-related genes have been found in viruses that infect cyanobacteria (cyanophages). Although photosystem II (PSII) genes are common in both cultured cyanophages and environmental samples1,2,3,4, viral photosystem I (vPSI) genes have so far only been detected in environmental samples5,6. Here, we have used a targeted strategy to isolate a cyanophage from the tropical Pacific Ocean that carries a PSI gene cassette with seven distinct PSI genes (psaJF, C, A, B, K, E, D) as well as two PSII genes (psbA, D). This cyanophage, P-TIM68, belongs to the T4-like myoviruses, has a prolate capsid, a long contractile tail and infects Prochlorococcus sp. strain MIT9515. Phage photosynthesis genes from both photosystems are expressed during infection, and the resultant proteins are incorporated into membranes of the infected host. Moreover, photosynthetic capacity in the cell is maintained throughout the infection cycle with enhancement of cyclic electron flow around PSI. Analysis of metagenomic data from the Tara Oceans expedition7 shows that phages carrying PSI gene cassettes are abundant in the tropical Pacific Ocean, composing up to 28% of T4-like cyanomyophages. They are also present in the tropical Indian and Atlantic Oceans. P-TIM68 populations, specifically, compose on average 22% of the PSI-gene-cassette carrying phages. Our results suggest that cyanophages carrying PSI and PSII genes are likely to maintain and even manipulate photosynthesis during infection of their Prochlorococcus hosts in the tropical oceans.

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Acknowledgements

The authors thank N. Keren, N. Adir and J. Golbeck for their insight regarding photosynthesis in cyanobacteria, O. Kleifeld for preliminary proteomics results, I. Pekarsky and M. Rosenberg for help with TEM imaging and Béjà and Lindell laboratory members for continuous discussions. The authors also thank L. Garczarek for providing cyanobacteria abundance data. This work was funded by a European Commission ERC Advanced Grant (no. 321647), the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme FP7/2007-2013/ under REA Grant Agreement No. 317184, an Israel Science Foundation grant (no. 580/10) and the Louis and Lyra Richmond Memorial Chair in Life Sciences to O.B., a European Commission ERC starting grant (no. 203406) to D.L. and the Technion’s Lorry I. Lokey Interdisciplinary Center for Life Sciences and Engineering and the Russell Berrie Nanotechnology Institute. This is contribution number 54 of Tara Oceans. This paper is dedicated to the memory of F.R. (CNRS), who sadly passed away before the paper was finalized.

Author information

S.F., D.L. and O.B. designed the project and the experiments. S.F. isolated the phage and, together with S.L. and O.A., performed laboratory experiments. F.L.R. collected the phage concentrate. T.Z. performed proteomics. J.F.-U., I.S., A.P., C.L.D., F.M.C.-C., P.S., S.G.A. and O.B. performed bioinformatic analyses. S.L., O.L., I.Y., F.S., B.B. and F.R. performed photosynthetic measurements. O.B. and D.L. wrote the manuscript with contributions from all authors to data analysis, figure generation and the final manuscript.

Competing interests

The authors declare no competing financial interests.

Correspondence to Debbie Lindell or Oded Béjà.

Electronic supplementary material

Supplementary Information

Supplementary Results 1 (Supplementary Figures and Tables) and Supplementary Results 2 (VIRFAM analysis).

Supplementary Table 1

Counts of reads that were recruited to the vPSI-7 and P-TIM68 photosynthesis gene cassettes from the different Tara Oceans stations.

Supplementary Table 5

Accession numbers of PsbA, g20 and g23 proteins used to calculate vPSI-7 abundance in Supplementary Table 1.

Supplementary File 1

Tara Oceans dataset used in this study.

Supplementary File 2

CLUSTAL 2.1 multiple sequence alignment.

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Further reading

Fig. 1: P-TIM68 gene organization, phylogeny and morphology.
Fig. 2: Global distribution and relative abundance of P-TIM68 and other vPSI-7 phages.
Fig. 3: Expression of P-TIM68 PSI and PSII genes in infected Prochlorococcus MIT9515 cells.
Fig. 4: Changes in PSII and PSI photosynthetic parameters during infection of Prochlorococcus MIT9515 with phage P-TIM68.