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Research Article

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

David M. Needham, View ORCID ProfileSusumu Yoshizawa, View ORCID ProfileToshiaki Hosaka, Camille Poirier, Chang Jae Choi, View ORCID ProfileElisabeth Hehenberger, Nicholas A. T. Irwin, Susanne Wilken, Cheuk-Man Yung, Charles Bachy, Rika Kurihara, Yu Nakajima, Keiichi Kojima, View ORCID ProfileTomomi Kimura-Someya, Guy Leonard, Rex R. Malmstrom, Daniel R. Mende, Daniel K. Olson, View ORCID ProfileYuki Sudo, Sebastian Sudek, Thomas A. Richards, View ORCID ProfileEdward F. DeLong, Patrick J. Keeling, View ORCID ProfileAlyson E. Santoro, Mikako Shirouzu, View ORCID ProfileWataru Iwasaki, and View ORCID ProfileAlexandra Z. Worden
PNAS October 8, 2019 116 (41) 20574-20583; first published September 23, 2019; https://doi.org/10.1073/pnas.1907517116
David M. Needham
aMonterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
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Susumu Yoshizawa
bAtmosphere & Ocean Research Institute, University of Tokyo, Chiba 277-8564, Japan;
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  • ORCID record for Susumu Yoshizawa
Toshiaki Hosaka
cLaboratory for Protein Functional & Structural Biology, RIKEN Center for Biosystems Dynamics Research, Yokohama, Kanagawa 230-0045, Japan;
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Camille Poirier
aMonterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
dOcean EcoSystems Biology Unit, GEOMAR Helmholtz Centre for Ocean Research, 24105 Kiel, Germany;
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Chang Jae Choi
aMonterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
dOcean EcoSystems Biology Unit, GEOMAR Helmholtz Centre for Ocean Research, 24105 Kiel, Germany;
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Elisabeth Hehenberger
aMonterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
dOcean EcoSystems Biology Unit, GEOMAR Helmholtz Centre for Ocean Research, 24105 Kiel, Germany;
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  • ORCID record for Elisabeth Hehenberger
Nicholas A. T. Irwin
eDepartment of Botany, University of British Columbia, Vancouver, BC V6T 1Z4, Canada;
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Susanne Wilken
aMonterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
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Cheuk-Man Yung
aMonterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
dOcean EcoSystems Biology Unit, GEOMAR Helmholtz Centre for Ocean Research, 24105 Kiel, Germany;
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Charles Bachy
aMonterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
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Rika Kurihara
fGraduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University, Okayama 700-8530, Japan;
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Yu Nakajima
bAtmosphere & Ocean Research Institute, University of Tokyo, Chiba 277-8564, Japan;
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Keiichi Kojima
fGraduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University, Okayama 700-8530, Japan;
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Tomomi Kimura-Someya
cLaboratory for Protein Functional & Structural Biology, RIKEN Center for Biosystems Dynamics Research, Yokohama, Kanagawa 230-0045, Japan;
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  • ORCID record for Tomomi Kimura-Someya
Guy Leonard
gLiving Systems Institute, School of Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4SB, United Kingdom;
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Rex R. Malmstrom
hDepartment of Energy Joint Genome Institute, Walnut Creek, CA 94598;
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Daniel R. Mende
iDaniel K. Inouye Center for Microbial Oceanography, University of Hawaii, Manoa, Honolulu, HI 96822;
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Daniel K. Olson
iDaniel K. Inouye Center for Microbial Oceanography, University of Hawaii, Manoa, Honolulu, HI 96822;
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Yuki Sudo
fGraduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University, Okayama 700-8530, Japan;
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Sebastian Sudek
aMonterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
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Thomas A. Richards
gLiving Systems Institute, School of Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4SB, United Kingdom;
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Edward F. DeLong
iDaniel K. Inouye Center for Microbial Oceanography, University of Hawaii, Manoa, Honolulu, HI 96822;
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Patrick J. Keeling
eDepartment of Botany, University of British Columbia, Vancouver, BC V6T 1Z4, Canada;
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Alyson E. Santoro
jDepartment of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA 93106;
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  • ORCID record for Alyson E. Santoro
Mikako Shirouzu
cLaboratory for Protein Functional & Structural Biology, RIKEN Center for Biosystems Dynamics Research, Yokohama, Kanagawa 230-0045, Japan;
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Wataru Iwasaki
bAtmosphere & Ocean Research Institute, University of Tokyo, Chiba 277-8564, Japan;
kDepartment of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo 113-0032, Japan
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  • ORCID record for Wataru Iwasaki
  • For correspondence: iwasaki@bs.s.u-tokyo.ac.jp azworden@geomar.de
Alexandra Z. Worden
aMonterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
dOcean EcoSystems Biology Unit, GEOMAR Helmholtz Centre for Ocean Research, 24105 Kiel, Germany;
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  • For correspondence: iwasaki@bs.s.u-tokyo.ac.jp azworden@geomar.de
  1. Edited by W. Ford Doolittle, Dalhousie University, Halifax, Canada, and approved August 8, 2019 (received for review May 27, 2019)

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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.

  • giant viruses
  • viral evolution
  • marine carbon cycle
  • single-cell genomics
  • host–virus interactions

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.

  • Copyright © 2019 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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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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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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