A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators

David M. Needham, Susumu Yoshizawa, Toshiaki Hosaka, Camille Poirier, Chang Jae Choi, Elisabeth Hehenberger, Nicholas A. T. Irwin, Susanne Wilken, Cheuk-Man Yung, Charles Bachy, Rika Kurihara, Yu Nakajima, Keiichi Kojima, Tomomi Kimura-Someya, Guy Leonard, Rex R. Malmstrom, Daniel R. Mende, Daniel K. Olson, Yuki Sudo, Sebastian Sudek, Thomas A. Richards, Edward F. DeLong, Patrick J. Keeling, Alyson E. Santoro, Mikako Shirouzu, Wataru Iwasaki, and Alexandra Z. Worden
PNAS October 8, 2019 116 (41) 20574-20583; first published September 23, 2019 https://doi.org/10.1073/pnas.1907517116

  1. Edited by W. Ford Doolittle, Dalhousie University, Halifax, Canada, and approved August 8, 2019 (received for review May 27, 2019)

Significance

Although viruses are well-characterized regulators of eukaryotic algae, little is known about those infecting unicellular predators in oceans. We report the largest marine virus genome yet discovered, found in a wild predatory choanoflagellate sorted away from other Pacific microbes and pursued using integration of cultivation-independent and laboratory methods. The giant virus encodes nearly 900 proteins, many unlike known proteins, others related to cellular metabolism and organic matter degradation, and 3 type-1 rhodopsins. The viral rhodopsin that is most abundant in ocean metagenomes, and also present in an algal virus, pumps protons when illuminated, akin to cellular rhodopsins that generate a proton-motive force. Giant viruses likely provision multiple host species with photoheterotrophic capacities, including predatory unicellular relatives of animals.

Abstract

Giant viruses are remarkable for their large genomes, often rivaling those of small bacteria, and for having genes thought exclusive to cellular life. Most isolated to date infect nonmarine protists, leaving their strategies and prevalence in marine environments largely unknown. Using eukaryotic single-cell metagenomics in the Pacific, we discovered a Mimiviridae lineage of giant viruses, which infects choanoflagellates, widespread protistan predators related to metazoans. The ChoanoVirus genomes are the largest yet from pelagic ecosystems, with 442 of 862 predicted proteins lacking known homologs. They are enriched in enzymes for modifying organic compounds, including degradation of chitin, an abundant polysaccharide in oceans, and they encode 3 divergent type-1 rhodopsins (VirR) with distinct evolutionary histories from those that capture sunlight in cellular organisms. One (VirRDTS) is similar to the only other putative rhodopsin from a virus (PgV) with a known host (a marine alga). Unlike the algal virus, ChoanoViruses encode the entire pigment biosynthesis pathway and cleavage enzyme for producing the required chromophore, retinal. We demonstrate that the rhodopsin shared by ChoanoViruses and PgV binds retinal and pumps protons. Moreover, our 1.65-Å resolved VirRDTS crystal structure and mutational analyses exposed differences from previously characterized type-1 rhodopsins, all of which come from cellular organisms. Multiple VirR types are present in metagenomes from across surface oceans, where they are correlated with and nearly as abundant as a canonical marker gene from Mimiviridae. Our findings indicate that light-dependent energy transfer systems are likely common components of giant viruses of photosynthetic and phagotrophic unicellular marine eukaryotes.

Footnotes

  • ↵1D.M.N., S.Y., and T.H. contributed equally to this work.

  • ↵2Present address: Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam 1090 GE, The Netherlands.

  • ↵3Station Biologique de Roscoff, Sorbonne Université, CNRS, 29688 Roscoff, France.

  • ↵4To whom correspondence may be addressed. Email: iwasaki{at}bs.s.u-tokyo.ac.jp or azworden{at}geomar.de.

  • Author contributions: D.M.N., S.Y., E.F.D., M.S., W.I., and A.Z.W. designed research; D.M.N., S.Y., T.H., C.P., S.W., R.K., Y.N., K.K., T.K.-S., R.R.M., D.R.M., D.K.O., Y.S., S.S., T.A.R., E.F.D., P.J.K., A.E.S., W.I., and A.Z.W. performed research; D.M.N., S.Y., T.H., C.P., C.J.C., E.H., N.A.T.I., C.-M.Y., C.B., G.L., T.A.R., E.F.D., P.J.K., A.E.S., M.S., and A.Z.W. analyzed data; and D.M.N., S.Y., W.I., and A.Z.W. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: Data accession numbers and databases in which they have been deposited are provided in Dataset S2 for all sequence data; the protein biochemical characterization/crystallography data have been deposited in the Protein Data Bank, www.wwpdb.org (PDB ID code 6JO0).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1907517116/-/DCSupplemental.

References

  1. ↵
    1. A. E. Zimmerman et al
    ., Closely related viruses of the marine picoeukaryotic alga Ostreococcus lucimarinus exhibit different ecological strategies. Environ. Microbiol. 21, 2148–2170 (2019).
    OpenUrl
  2. ↵
    1. J. S. Weitz,
    2. S. W. Wilhelm
    , Ocean viruses and their effects on microbial communities and biogeochemical cycles. F1000 Biol. Rep. 4, 17 (2012).
    OpenUrlCrossRef
  3. ↵
    1. N. Y. Ankrah et al
    ., Phage infection of an environmentally relevant marine bacterium alters host metabolism and lysate composition. ISME J. 8, 1089–1100 (2014).
    OpenUrlCrossRefPubMed
  4. ↵
    1. D. Lindell,
    2. J. D. Jaffe,
    3. Z. I. Johnson,
    4. G. M. Church,
    5. S. W. Chisholm
    , Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438, 86–89 (2005).
    OpenUrlCrossRefPubMed
  5. ↵
    1. M. Breitbart,
    2. C. Bonnain,
    3. K. Malki,
    4. N. A. Sawaya
    , Phage puppet masters of the marine microbial realm. Nat. Microbiol. 3, 754–766 (2018).
    OpenUrl
  6. ↵
    1. S. Rosenwasser,
    2. C. Ziv,
    3. S. G. V. Creveld,
    4. A. Vardi
    , Virocell metabolism: Metabolic innovations during host-virus interactions in the ocean. Trends Microbiol. 24, 821–832 (2016).
    OpenUrlCrossRef
  7. ↵
    1. A. Monier et al
    ., Phosphate transporters in marine phytoplankton and their viruses: Cross-domain commonalities in viral-host gene exchanges. Environ. Microbiol. 14, 162–176 (2012).
    OpenUrlCrossRefPubMed
  8. ↵
    1. A. Monier et al
    ., Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton. Proc. Natl. Acad. Sci. U.S.A. 114, E7489–E7498 (2017).
    OpenUrlAbstract/FREE Full Text
  9. ↵
    1. D. Raoult et al
    ., The 1.2-megabase genome sequence of Mimivirus. Science 306, 1344–1350 (2004).
    OpenUrlAbstract/FREE Full Text
  10. ↵
    1. C. Abergel,
    2. M. Legendre,
    3. J. M. Claverie
    , The rapidly expanding universe of giant viruses: Mimivirus, Pandoravirus, Pithovirus and Mollivirus. FEMS Microbiol. Rev. 39, 779–796 (2015).
    OpenUrlCrossRefPubMed
  11. ↵
    1. P. Colson,
    2. B. La Scola,
    3. A. Levasseur,
    4. G. Caetano-Anollés,
    5. D. Raoult
    , Mimivirus: Leading the way in the discovery of giant viruses of amoebae. Nat. Rev. Microbiol. 15, 243–254 (2017).
    OpenUrlCrossRef
  12. ↵
    1. F. Schulz et al
    ., Giant viruses with an expanded complement of translation system components. Science 356, 82–85 (2017).
    OpenUrlAbstract/FREE Full Text
  13. ↵
    1. C. M. Deeg,
    2. C. T. Chow,
    3. C. A. Suttle
    , The kinetoplastid-infecting Bodo saltans virus (BsV), a window into the most abundant giant viruses in the sea. eLife 7, e33014 (2018).
    OpenUrlCrossRef
  14. ↵
    1. C. A. Suttle
    , Marine viruses–Major players in the global ecosystem. Nat. Rev. Microbiol. 5, 801–812 (2007).
    OpenUrlCrossRefPubMed
  15. ↵
    1. A. Z. Worden et al
    ., Environmental science. Rethinking the marine carbon cycle: Factoring in the multifarious lifestyles of microbes. Science 347, 1257594 (2015).
    OpenUrlAbstract/FREE Full Text
  16. ↵
    1. C. P. Laber et al
    ., Coccolithovirus facilitation of carbon export in the North Atlantic. Nat. Microbiol. 3, 537–547 (2018).
    OpenUrl
  17. ↵
    1. F. H. Coutinho et al
    ., Marine viruses discovered via metagenomics shed light on viral strategies throughout the oceans. Nat. Commun. 8, 15955 (2017).
    OpenUrlCrossRef
  18. ↵
    1. S. Santini et al
    ., Genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes. Proc. Natl. Acad. Sci. U.S.A. 110, 10800–10805 (2013).
    OpenUrlAbstract/FREE Full Text
  19. ↵
    1. M. Moniruzzaman et al
    ., Genome of brown tide virus (AaV), the little giant of the Megaviridae, elucidates NCLDV genome expansion and host-virus coevolution. Virology 466–467, 60–70 (2014).
    OpenUrl
  20. ↵
    1. C. R. Schvarcz,
    2. G. F. Steward
    , A giant virus infecting green algae encodes key fermentation genes. Virology 518, 423–433 (2018).
    OpenUrl
  21. ↵
    1. M. G. Fischer,
    2. M. J. Allen,
    3. W. H. Wilson,
    4. C. A. Suttle
    , Giant virus with a remarkable complement of genes infects marine zooplankton. Proc. Natl. Acad. Sci. U.S.A. 107, 19508–19513 (2010).
    OpenUrlAbstract/FREE Full Text
  22. ↵
    1. L. Gallot-Lavallée,
    2. G. Blanc,
    3. J. M. Claverie
    , Comparative genomics of Chrysochromulina ericina virus and other microalga-infecting large DNA viruses highlights their intricate evolutionary relationship with the established Mimiviridae family. J. Virol. 91, e00230-17 (2017).
    OpenUrlAbstract/FREE Full Text
  23. ↵
    1. W. H. Wilson et al
    ., Complete genome sequence and lytic phase transcription profile of a Coccolithovirus. Science 309, 1090–1092 (2005).
    OpenUrlAbstract/FREE Full Text
  24. ↵
    1. S. W. Wilhelm et al
    ., A student’s guide to giant viruses infecting small eukaryotes: From acanthamoeba to zooxanthellae. Viruses 9, E46 (2017).
    OpenUrlCrossRef
  25. ↵
    1. P. J. Keeling et al
    ., The marine microbial eukaryote transcriptome sequencing project (MMETSP): Illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 12, e1001889 (2014).
    OpenUrlCrossRefPubMed
  26. ↵
    1. S. Yau et al
    ., Virophage control of antarctic algal host-virus dynamics. Proc. Natl. Acad. Sci. U.S.A. 108, 6163–6168 (2011).
    OpenUrlAbstract/FREE Full Text
  27. ↵
    1. D. J. Richter,
    2. P. Fozouni,
    3. M. B. Eisen,
    4. N. King
    , Gene family innovation, conservation and loss on the animal stem lineage. eLife 7, e34226 (2018).
    OpenUrlCrossRefPubMed
  28. ↵
    1. L. Deng et al
    ., Grazing of heterotrophic flagellates on viruses is driven by feeding behaviour. Environ. Microbiol. Rep. 6, 325–330 (2014).
    OpenUrl
  29. ↵
    1. J. M. Gonzalez,
    2. C. Suttle
    , Grazing by marine nanoflagellates on viruses and virus-sized particles: Ingestion and digestion. Mar. Ecol. Prog. Ser. 94, 1–10 (1993).
    OpenUrlCrossRef
  30. ↵
    1. J. M. Labonté et al
    ., Single-cell genomics-based analysis of virus-host interactions in marine surface bacterioplankton. ISME J. 9, 2386–2399 (2015).
    OpenUrlCrossRefPubMed
  31. ↵
    1. N. Frank,
    2. T. Helge Abuldhauge,
    3. R. Daniel J
    , Bridging the gap between morphological species and molecular barcodes–Exemplified by loricate choanoflagellates. Eur. J. Protistol. 57, 26–37 (2017).
    OpenUrl
  32. ↵
    1. A. J. Limardo et al
    ., Quantitative biogeography of picoprasinophytes establishes ecotype distributions and significant contributions to marine phytoplankton. Environ. Microbiol. 19, 3219–3234 (2017).
    OpenUrlCrossRef
  33. ↵
    1. M. P. Simmons et al
    ., Abundance and biogeography of picoprasinophyte ecotypes and other phytoplankton in the Eastern North Pacific Ocean. Appl. Environ. Microbiol. 82, 1693–1705 (2016).
    OpenUrlAbstract/FREE Full Text
  34. ↵
    1. J. T. Pennington,
    2. F. P. Chavez
    , Seasonal fluctuations of temperature, salinity, nitrate, chlorophyll and primary production at station H3/M1 over 1989-1996 in Monterey Bay, California. Deep Sea Res. Part II Top. Stud. Oceanogr. 47, 947–974 (2000).
    OpenUrlCrossRef
  35. ↵
    1. E. Derelle et al
    ., Diversity of viruses infecting the green microalga Ostreococcus lucimarinus. J. Virol. 89, 5812–5821 (2015).
    OpenUrlAbstract/FREE Full Text
  36. ↵
    1. C. Bachy et al
    ., Transcriptional responses of the marine green alga Micromonas pusilla and an infecting prasinovirus under different phosphate conditions. Environ. Microbiol. 20, 2898–2912 (2018).
    OpenUrl
  37. ↵
    1. Y. Tomaru,
    2. K. Nagasaki
    , Diatom Viruses (Springer, 2011).
  38. ↵
    1. E. R. Tulman et al
    ., The genome of canarypox virus. J. Virol. 78, 353–366 (2004).
    OpenUrlAbstract/FREE Full Text
  39. ↵
    1. P. Forterre
    , The virocell concept and environmental microbiology. ISME J. 7, 233–236 (2013).
    OpenUrlCrossRefPubMed
  40. ↵
    1. N. Yutin,
    2. Y. I. Wolf,
    3. D. Raoult,
    4. E. V. Koonin
    , Eukaryotic large nucleo-cytoplasmic DNA viruses: Clusters of orthologous genes and reconstruction of viral genome evolution. Vriol. J. 6, 223 (2009).
    OpenUrl
  41. ↵
    1. Tara Oceans coordinators
    1. S. Sunagawa et al
    .; Tara Oceans coordinators, Structure and function of the global ocean microbiome. Science 348, 1261359 (2015).
    OpenUrlAbstract/FREE Full Text
  42. ↵
    1. S. Yooseph et al
    ., The Sorcerer II Global Ocean sampling expedition: Expanding the universe of protein families. PLoS Biol. 5, e16 (2007).
    OpenUrlCrossRefPubMed
  43. ↵
    1. J. Abrahão et al
    ., Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere. Nat. Commun. 9, 749 (2018).
    OpenUrlCrossRef
  44. ↵
    1. D. De Corte et al
    ., Metagenomic insights into zooplankton-associated bacterial communities. Environ. Microbiol. 20, 492–505 (2018).
    OpenUrl
  45. ↵
    1. G. Blanc et al
    ., The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22, 2943–2955 (2010).
    OpenUrlAbstract/FREE Full Text
  46. ↵
    1. C. J. Thomas et al
    ., Localization of a baculovirus-induced chitinase in the insect cell endoplasmic reticulum. J. Virol. 72, 10207–10212 (1998).
    OpenUrlAbstract/FREE Full Text
  47. ↵
    1. G. Torruella et al
    ., Phylogenomics reveals convergent evolution of lifestyles in close relatives of animals and fungi. Curr. Biol. 25, 2404–2410 (2015).
    OpenUrlCrossRefPubMed
  48. ↵
    1. F. Azam et al
    ., The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257–263 (1983).
    OpenUrlCrossRef
  49. ↵
    1. O. P. Ernst et al
    ., Microbial and animal rhodopsins: Structures, functions, and molecular mechanisms. Chem. Rev. 114, 126–163 (2014).
    OpenUrlCrossRefPubMed
  50. ↵
    1. L. Gómez-Consarnau et al
    ., Proteorhodopsin phototrophy promotes survival of marine bacteria during starvation. PLoS Biol. 8, e1000358 (2010).
    OpenUrlCrossRefPubMed
  51. ↵
    1. A. Martinez,
    2. A. S. Bradley,
    3. J. R. Waldbauer,
    4. R. E. Summons,
    5. E. F. DeLong
    , Proteorhodopsin photosystem gene expression enables photophosphorylation in a heterologous host. Proc. Natl. Acad. Sci. U.S.A. 104, 5590–5595 (2007).
    OpenUrlAbstract/FREE Full Text
  52. ↵
    1. E. G. Govorunova,
    2. O. A. Sineshchekov,
    3. H. Li,
    4. J. L. Spudich
    , Microbial rhodopsins: Diversity, mechanisms, and optogenetic applications. Annu. Rev. Biochem. 86, 845–872 (2017).
    OpenUrlCrossRefPubMed
  53. ↵
    1. A. Pushkarev et al
    ., A distinct abundant group of microbial rhodopsins discovered using functional metagenomics. Nature 558, 595–599 (2018).
    OpenUrlCrossRef
  54. ↵
    1. O. Béjà,
    2. E. N. Spudich,
    3. J. L. Spudich,
    4. M. Leclerc,
    5. E. F. DeLong
    , Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789 (2001).
    OpenUrlCrossRefPubMed
  55. ↵
    1. L. Gómez-Consarnau et al
    ., Microbial rhodopsins are major contributors to the solar energy captured in the sea. Sci. Adv. 5, eaaw8855 (2019).
    OpenUrlFREE Full Text
  56. ↵
    1. A. Marchetti,
    2. D. Catlett,
    3. B. M. Hopkinson,
    4. K. Ellis,
    5. N. Cassar
    , Marine diatom proteorhodopsins and their potential role in coping with low iron availability. ISME J. 9, 2745–2748 (2015).
    OpenUrlCrossRefPubMed
  57. ↵
    1. N. Yutin,
    2. E. V. Koonin
    , Proteorhodopsin genes in giant viruses. Biol. Direct 7, 34 (2012).
    OpenUrlCrossRefPubMed
  58. ↵
    1. L. B. Lamarche et al
    ., Purification and characterization of RhoPDE, a retinylidene/phosphodiesterase fusion protein and potential optogenetic tool from the choanoflagellate Salpingoeca rosetta. Biochemistry 56, 5812–5822 (2017).
    OpenUrlCrossRefPubMed
  59. ↵
    1. K. Yoshida,
    2. S. P. Tsunoda,
    3. L. S. Brown,
    4. H. Kandori
    , A unique choanoflagellate enzyme rhodopsin exhibits light-dependent cyclic nucleotide phosphodiesterase activity. J. Biol. Chem. 292, 7531–7541 (2017).
    OpenUrlAbstract/FREE Full Text
  60. ↵
    1. D. K. Olson,
    2. S. Yoshizawa,
    3. D. Boeuf,
    4. W. Iwasaki,
    5. E. F. DeLong
    , Proteorhodopsin variability and distribution in the North Pacific Subtropical Gyre. ISME J. 12, 1047–1060 (2018).
    OpenUrl
  61. ↵
    1. A. Philosof,
    2. O. Béjà
    , Bacterial, archaeal and viral-like rhodopsins from the Red Sea. Environ. Microbiol. Rep. 5, 475–482 (2013).
    OpenUrlCrossRefPubMed
  62. ↵
    1. J. L. López et al
    ., Microbial and viral-like rhodopsins present in coastal marine sediments from four polar and subpolar regions. FEMS Microbiol. Ecol. 93, (2017).
  63. ↵
    1. W. R. Briggs,
    2. J. L. Spudich
    1. J. L. Spudich,
    2. K.-H. Jung
    , “Microbial rhodopsins: Phylogenetic and functional diversity” in Handbook of Photosensory Receptors, W. R. Briggs, J. L. Spudich, Eds. (Wiley, 2005), pp. 1–23.
  64. ↵
    1. A. Harris et al
    ., A new group of eubacterial light-driven retinal-binding proton pumps with an unusual cytoplasmic proton donor. Biochim. Biophys. Acta 1847, 1518–1529 (2015).
    OpenUrl
  65. ↵
    1. P. A. Bulzu et al
    ., Casting light on Asgardarchaeota metabolism in a sunlit microoxic niche. Nat. Microbiol. 4, 1129–1137 (2019).
    OpenUrl
  66. ↵
    1. L. Vogeley et al
    ., Anabaena sensory rhodopsin: A photochromic color sensor at 2.0 A. Science 306, 1390–1393 (2004).
    OpenUrlAbstract/FREE Full Text
  67. ↵
    1. J. A. Kyndt,
    2. T. E. Meyer,
    3. M. A. Cusanovich
    , Photoactive yellow protein, bacteriophytochrome, and sensory rhodopsin in purple phototrophic bacteria. Photochem. Photobiol. Sci. 3, 519–530 (2004).
    OpenUrlCrossRefPubMed
  68. ↵
    1. M. Mehler et al
    ., The EF loop in green proteorhodopsin affects conformation and photocycle dynamics. Biophys. J. 105, 385–397 (2013).
    OpenUrlCrossRefPubMed
  69. ↵
    1. Y. Sudo et al
    ., A microbial rhodopsin with a unique retinal composition shows both sensory rhodopsin II and bacteriorhodopsin-like properties. J. Biol. Chem. 286, 5967–5976 (2011).
    OpenUrlAbstract/FREE Full Text
  70. ↵
    1. T. Tsukamoto,
    2. K. Inoue,
    3. H. Kandori,
    4. Y. Sudo
    , Thermal and spectroscopic characterization of a proton pumping rhodopsin from an extreme thermophile. J. Biol. Chem. 288, 21581–21592 (2013).
    OpenUrlAbstract/FREE Full Text
  71. ↵
    1. H. Luecke,
    2. B. Schobert,
    3. H. T. Richter,
    4. J. P. Cartailler,
    5. J. K. Lanyi
    , Structure of bacteriorhodopsin at 1.55 A resolution. J. Mol. Biol. 291, 899–911 (1999).
    OpenUrlCrossRefPubMed
  72. ↵
    1. H. Luecke,
    2. B. Schobert,
    3. J. K. Lanyi,
    4. E. N. Spudich,
    5. J. L. Spudich
    , Crystal structure of sensory rhodopsin II at 2.4 angstroms: Insights into color tuning and transducer interaction. Science 293, 1499–1503 (2001).
    OpenUrlAbstract/FREE Full Text
  73. ↵
    1. J. L. Spudich
    , The multitalented microbial sensory rhodopsins. Trends Microbiol. 14, 480–487 (2006).
    OpenUrlCrossRefPubMed
  74. ↵
    1. G. M. Avelar et al
    ., A rhodopsin-guanylyl cyclase gene fusion functions in visual perception in a fungus. Curr. Biol. 24, 1234–1240 (2014).
    OpenUrlCrossRefPubMed
  75. ↵
    1. D. Laundon,
    2. B. T. Larson,
    3. K. McDonald,
    4. N. King,
    5. P. Burkhardt
    , The architecture of cell differentiation in choanoflagellates and sponge choanocytes. PLoS Biol. 17, e3000226 (2019).
    OpenUrlCrossRef
  76. ↵
    1. G. Sabehi et al
    ., New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLoS Biol. 3, e273 (2005).
    OpenUrlCrossRefPubMed
  77. ↵
    1. J. McCarren,
    2. E. F. DeLong
    , Proteorhodopsin photosystem gene clusters exhibit co-evolutionary trends and shared ancestry among diverse marine microbial phyla. Environ. Microbiol. 9, 846–858 (2007).
    OpenUrlCrossRefPubMed
  78. ↵
    1. J. Pinhassi,
    2. E. F. DeLong,
    3. O. Béjà,
    4. J. M. González,
    5. C. Pedrós-Alió
    , Marine bacterial and archaeal ion-pumping rhodopsins: Genetic diversity, physiology, and ecology. Microbiol. Mol. Biol. Rev. 80, 929–954 (2016).
    OpenUrlAbstract/FREE Full Text
  79. ↵
    1. P. Hingamp et al
    ., Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes. ISME J. 7, 1678–1695 (2013).
    OpenUrlCrossRefPubMed
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A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators
David M. Needham, Susumu Yoshizawa, Toshiaki Hosaka, Camille Poirier, Chang Jae Choi, Elisabeth Hehenberger, Nicholas A. T. Irwin, Susanne Wilken, Cheuk-Man Yung, Charles Bachy, Rika Kurihara, Yu Nakajima, Keiichi Kojima, Tomomi Kimura-Someya, Guy Leonard, Rex R. Malmstrom, Daniel R. Mende, Daniel K. Olson, Yuki Sudo, Sebastian Sudek, Thomas A. Richards, Edward F. DeLong, Patrick J. Keeling, Alyson E. Santoro, Mikako Shirouzu, Wataru Iwasaki, Alexandra Z. Worden
Proceedings of the National Academy of Sciences Oct 2019, 116 (41) 20574-20583; DOI: 10.1073/pnas.1907517116
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