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

Nature Microbiology volume 2, pages 1350–1357 (2017)Cite this article

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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.

Oxygenic photosynthetic organisms, including cyanobacteria, use four integral membrane complexes: photosystem II (PSII), b 6  f, photosystem I (PSI) and ATPase, to convert sunlight into chemical energy. Linear electron transfer begins with PSII catalysing the transfer of electrons, derived from water, to the plastoquinone pool. PSI transfers electrons from plastocyanin/cytochrome c 6 to ferredoxin, thereby generating the reducing power needed for CO2 fixation in the form of NADPH. The b 6  f complex then couples electron transfer from the reduced plastoquinone (QH2) to the oxidized plastocyanin/cytochrome c 6 to the pumping of protons in the lumen. Finally, the electrochemical proton gradient drives ATP formation by the ATPase complex.

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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.

References

  1. Mann, N. H., Cook, A., Millard, A., Bailey, S. & Clokie, M. Bacterial photosynthesis genes in a virus. Nature 424, 741 (2003).

    Article  CAS  PubMed  Google Scholar 

  2. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Lindell, D. et al. Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc. Natl Acad. Sci. USA 101, 11013–11018 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Sharon, I. et al. Comparative metagenomics of microbial traits within oceanic viral communities. ISME J. 5, 1178–1190 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Sharon, I. et al. Photosystem-I gene cassettes are present in marine virus genomes. Nature 461, 258–262 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Brum, J. et al. Patterns and ecological drivers of ocean viral communities. Science 348, 1261498 (2015).

    Article  PubMed  Google Scholar 

  8. Puxty, R. J., Millard, A. D., Evans, D. J. & Scanlan, D. J. Shedding new light on viral photosynthesis. Photosynth. Res. 126, 71–97 (2015).

    Article  CAS  PubMed  Google Scholar 

  9. 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).

    Article  CAS  PubMed  Google Scholar 

  10. 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).

    Article  CAS  PubMed  Google Scholar 

  11. Bragg, J. G. & Chisholm, S. W. Modeling the fitness consequences of a cyanophage-encoded photosynthesis gene. PLoS ONE 3, e3550 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Hellweger, F. L. Carrying photosynthesis genes increases ecological fitness of cyanophage in silico. Environ. Microbiol. 11, 1386–1394 (2009).

    Article  CAS  PubMed  Google Scholar 

  13. 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).

    Article  CAS  PubMed  Google Scholar 

  14. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Roitman, S. et al. Closing the gaps on the viral photosystem-I psaDCAB gene organization. Environ. Microbiol. 17, 5100–5108 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Torabi, S. et al. PsbN is required for assembly of the photosystem II reaction center in Nicotiana tabacum. Plant Cell 26, 1183–1199 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. 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).

    Article  CAS  PubMed  Google Scholar 

  19. 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).

    Article  CAS  PubMed  Google Scholar 

  20. Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through the eastern tropical Pacific. PLoS Biol. 5, e77 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  21. 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).

    Article  CAS  PubMed  Google Scholar 

  22. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Wang, K. & Chen, F. Prevalence of highly host-specific cyanophages in the estuarine environment. Environ. Microbiol. 10, 300–312 (2008).

    Article  CAS  PubMed  Google Scholar 

  24. Doron, S. et al. Transcriptome dynamics of a broad host-range cyanophage and its hosts. ISME J. 10, 1437–1455 (2016).

    Article  CAS  PubMed  Google Scholar 

  25. 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).

    Article  CAS  Google Scholar 

  26. 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).

    Article  Google Scholar 

  27. Lindell, D. et al. Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449, 83–86 (2007).

    Article  CAS  PubMed  Google Scholar 

  28. Clokie, M. R. J. & Mann, N. H. Marine cyanophages and light. Environ. Microbiol. 8, 2074–2082 (2006).

    Article  CAS  PubMed  Google Scholar 

  29. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Wyman, M., Gregory, R. P. & Carr, N. G. Novel role for phycoerythrin in a marine cyanobacterium, Synechococcus strain DC2. Science 230, 818–820 (1985).

    Article  CAS  PubMed  Google Scholar 

  32. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Moore, L. R. et al. Culturing the marine cyanobacterium Prochlorococcus. Limnol. Oceanogr. Methods 5, 353–362 (2007).

    Article  CAS  Google Scholar 

  34. 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).

    Google Scholar 

  35. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Hevroni, G., Enav, H., Rohwer, F. & Béjà, O. Diversity of viral photosystem-I psaA genes. ISME J. 9, 1892–1898 (2015).

    Article  PubMed  Google Scholar 

  37. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Zerbino, D. R. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821–829 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  42. 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).

    Article  CAS  PubMed  Google Scholar 

  43. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).

    Article  CAS  PubMed  Google Scholar 

  45. Dereeper, A. et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465–W469 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. 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).

    Article  CAS  PubMed  Google Scholar 

  47. 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).

    Article  CAS  PubMed  Google Scholar 

  48. 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).

    Article  CAS  PubMed  Google Scholar 

  49. 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).

    Article  CAS  Google Scholar 

  50. 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).

    Article  Google Scholar 

  51. Joliot, P. & Joliot, A. Quantification of cyclic and linear flows in plants. Proc. Natl Acad. Sci. USA 102, 4913–4918 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Sunagawa, S. et al. Structure and function of the global ocean microbiome. Science 348, 1261359 (2015).

    Article  PubMed  Google Scholar 

  53. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Anders, S., Pyl, P. T. & Huber, W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015).

    Article  CAS  PubMed  Google Scholar 

  56. 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).

    Article  PubMed  Google Scholar 

  57. 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).

  58. 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).

    Article  CAS  PubMed  Google Scholar 

Download references

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.

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  1. Fabrice Rappaport is deceased.

Authors and Affiliations

  1. Faculty of Biology, Technion-Israel Institute of Technology, Haifa, 32000, Israel

    Svetlana Fridman, José Flores-Uribe, Shirley Larom, Onit Alalouf, Faris Salama, Alon Philosof, Debbie Lindell & Oded Béjà

  2. Department of Molecular Biology and Ecology of Plants, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, 69978, Israel

    Oded Liran & Iftach Yacoby

  3. Institut de Biologie Physico-Chimique, UMR 7141 CNRS and Université Pierre et Marie Curie, 13 rue Pierre et Marie Curie, 75005, Paris, France

    Benjamin Bailleul & Fabrice Rappaport

  4. Smoler Proteomics Center, Technion-Israel Institute of Technology, Haifa, 32000, Israel

    Tamar Ziv

  5. Migal Galilee Research Institute, Kiryat Shmona, 11016, Israel

    Itai Sharon

  6. Tel Hai College, Upper Galilee, 12210, Israel

    Itai Sharon

  7. Department of Marine Biology and Oceanography, Institute of Marine Sciences (ICM), CSIC, 08003, Barcelona, Spain

    Francisco M. Cornejo-Castillo, Pablo Sánchez & Silvia G. Acinas

  8. Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, 92037, USA

    Christopher L. Dupont

  9. Department of Biology, San Diego State University, San Diego, CA, 92182, USA

    Forest L. Rohwer

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  1. Svetlana Fridman
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Contributions

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.

Corresponding authors

Correspondence to Debbie Lindell or Oded Béjà.

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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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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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