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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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).
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. Comparative metagenomics of microbial traits within oceanic viral communities. ISME J. 5, 1178–1190 (2011).
Sharon, I. et al. Photosystem-I gene cassettes are present in marine virus genomes. Nature 461, 258–262 (2009).
Brum, J. et al. Patterns and ecological drivers of ocean viral communities. Science 348, 1261498 (2015).
Puxty, R. J., Millard, A. D., Evans, D. J. & Scanlan, D. J. Shedding new light on viral photosynthesis. Photosynth. Res. 126, 71–97 (2015).
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).
Clokie, M. R. J. et al. Transcription of a ‘photosynthetic’ T4-type phage during infection of a marine cyanobacterium. Environ. Microbiol. 8, 827–835 (2006).
Bragg, J. G. & Chisholm, S. W. Modeling the fitness consequences of a cyanophage-encoded photosynthesis gene. PLoS ONE 3, e3550 (2008).
Hellweger, F. L. Carrying photosynthesis genes increases ecological fitness of cyanophage in silico. Environ. Microbiol. 11, 1386–1394 (2009).
Millard, A. D., Zwirglmaier, K., Downey, M. J., Mann, N. H. & Scanlan, D. J. Comparative genomics of marine cyanomyoviruses reveals the widespread occurrence of Synechococcus host genes localized to a hyperplastic region: implications for mechanisms of cyanophage evolution. Environ. Microbiol. 11, 2370–2387 (2009).
Sullivan, M. B. et al. Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ. Microbiol. 12, 3035–3056 (2010).
Roitman, S. et al. Closing the gaps on the viral photosystem-I psaDCAB gene organization. Environ. Microbiol. 17, 5100–5108 (2015).
Torabi, S. et al. PsbN is required for assembly of the photosystem II reaction center in Nicotiana tabacum. Plant Cell 26, 1183–1199 (2014).
Thompson, L. R. et al. Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc. Natl Acad. Sci. USA 108, E757–E764 (2011).
Ignacio-Espinoza, J. C. & Sullivan, M. B. Phylogenomics of T4 cyanophages: lateral gene transfer in the ‘core’ and origins of host genes. Environ. Microbiol. 14, 2113–2126 (2012).
Puxty, R. J., Millard, A. D., Evans, D. J. & Scanlan, D. J. Viruses inhibit CO2 fixation in the most abundant phototrophs on Earth. Curr. Biol. 26, 1585–1589 (2016).
Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through the eastern tropical Pacific. PLoS Biol. 5, e77 (2007).
Dupont, C. L. et al. Genomes and gene expression across light and productivity gradients in eastern subtropical Pacific microbial communities. ISME J. 9, 1076–1092 (2015).
Comeau, A. M., Arbiol, C. & Krisch, H. M. Gene network visualization and quantitative synteny analysis of more than 300 marine T4-like phage scaffolds from the GOS metagenome. Mol. Biol. Evol. 27, 1935–1944 (2010).
Wang, K. & Chen, F. Prevalence of highly host-specific cyanophages in the estuarine environment. Environ. Microbiol. 10, 300–312 (2008).
Doron, S. et al. Transcriptome dynamics of a broad host-range cyanophage and its hosts. ISME J. 10, 1437–1455 (2016).
Wilson, W. H., Carr, N. G. & Mann, N. H. The effect of phosphate status on the kinetics of cyanophage infection of the oceanic cyanobacterium Synechococcus sp. WH7803. J. Phycol. 32, 506–516 (1996).
Kirzner, S., Barak, E. & Lindell, D. Variability in progeny production and virulence of cyanophages determined at the single-cell level. Environ. Microbiol. Rep 8, 605–613 (2016).
Lindell, D. et al. Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449, 83–86 (2007).
Clokie, M. R. J. & Mann, N. H. Marine cyanophages and light. Environ. Microbiol. 8, 2074–2082 (2006).
Farrant, G. K. et al. Delineating ecologically significant taxonomic units from global patterns of marine picocyanobacteria. Proc. Natl Acad. Sci. USA 113, E3365–E3374 (2016).
Fraser, J. M. et al. Photophysiological and photosynthetic complex changes during iron starvation in Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942. PLoS ONE 8, e59861 (2013).
Wyman, M., Gregory, R. P. & Carr, N. G. Novel role for phycoerythrin in a marine cyanobacterium, Synechococcus strain DC2. Science 230, 818–820 (1985).
Lindell, D., Padan, E. & Post, A. F. Regulation of ntcA expression and nitrite uptake in the marine Synechococcus sp. strain WH 7803. J. Bacteriol. 180, 1878–1886 (1998).
Moore, L. R. et al. Culturing the marine cyanobacterium Prochlorococcus. Limnol. Oceanogr. Methods 5, 353–362 (2007).
Haas, A. F. et al. Unraveling the unseen players in the ocean—a field guide to water chemistry and marine microbiology. J. Vis. Exp. 5, e52131 (2014).
Béjà, O., Fridman, S. & Glaser, F. Viral clones from the GOS expedition with an unusual photosystem-I gene cassette organization. ISME J. 6, 1617–1620 (2012).
Hevroni, G., Enav, H., Rohwer, F. & Béjà, O. Diversity of viral photosystem-I psaA genes. ISME J. 9, 1892–1898 (2015).
Sabehi, G. et al. A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans. Proc. Natl Acad. Sci. USA 109, 2037–2042 (2012).
Zerbino, D. R. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821–829 (2008).
Casjens, S. R. & Gilcrease, E. B. Determining DNA packaging strategy by analysis of the termini of the chromosomes in tailed-bacteriophage virions. Methods Mol. Biol. 502, 91–111 (2009).
Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010).
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
Zinser, E. R. et al. Prochlorococcus ecotype abundances in the North Atlantic Ocean as revealed by an improved quantitative PCR method. Appl. Environ. Microbiol. 72, 723–732 (2006).
Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).
Dereeper, A. et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465–W469 (2008).
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).
Whelan, S. & Goldman, N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18, 691–699 (2001).
Rappaport, F., Béal, D., Joliot, A. & Joliot, P. On the advantages of using green light to study fluorescence yield changes in leaves. Biochim. Biophys. Acta 1767, 56–65 (2007).
Genty, B., Briantais, J. M. & Baker, N. R. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 990, 87–92 (1989).
Béal, D., Rappaport, F. & Joliot, P. A new high-sensitivity 10-ns time-resolution spectrophotometric technique adapted to in vivo analysis of the photosynthetic apparatus. Rev. Sci. Instrum. 70, 202–207 (1999).
Joliot, P. & Joliot, A. Quantification of cyclic and linear flows in plants. Proc. Natl Acad. Sci. USA 102, 4913–4918 (2005).
Sunagawa, S. et al. Structure and function of the global ocean microbiome. Science 348, 1261359 (2015).
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
Anders, S., Pyl, P. T. & Huber, W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015).
O’Leary, N. A. et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 44, D733–D745 (2016).
Sharon, I., Pati, A., Markowitz, V. M. & Pinter, R. Y. in Research in Computational Molecular Biology Vol. 5541 (ed. Batzoglou, S.) 496–511 (Springer, Berlin, Heidelberg, 2009).
Peng, Y., Leung, H. C., Yiu, S. M. & Chin, F. Y. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420–1428 (2012).
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.
The authors declare no competing financial interests.
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Electronic supplementary material
Supplementary Results 1 (Supplementary Figures and Tables) and Supplementary Results 2 (VIRFAM analysis).
Counts of reads that were recruited to the vPSI-7 and P-TIM68 photosynthesis gene cassettes from the different Tara Oceans stations.
Accession numbers of PsbA, g20 and g23 proteins used to calculate vPSI-7 abundance in Supplementary Table 1.
Tara Oceans dataset used in this study.
CLUSTAL 2.1 multiple sequence alignment.
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Fridman, S., Flores-Uribe, J., Larom, S. et al. A myovirus encoding both photosystem I and II proteins enhances cyclic electron flow in infected Prochlorococcus cells. Nat Microbiol 2, 1350–1357 (2017). https://doi.org/10.1038/s41564-017-0002-9
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