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.

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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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