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Proc Natl Acad Sci U S A. 2019 Oct 8;116(41):20574-20583. doi: 10.1073/pnas.1907517116. Epub 2019 Sep 23.

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

Author information

1
Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039.
2
Atmosphere & Ocean Research Institute, University of Tokyo, Chiba 277-8564, Japan.
3
Laboratory for Protein Functional & Structural Biology, RIKEN Center for Biosystems Dynamics Research, Yokohama, Kanagawa 230-0045, Japan.
4
Ocean EcoSystems Biology Unit, GEOMAR Helmholtz Centre for Ocean Research, 24105 Kiel, Germany.
5
Department of Botany, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
6
Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University, Okayama 700-8530, Japan.
7
Living Systems Institute, School of Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4SB, United Kingdom.
8
Department of Energy Joint Genome Institute, Walnut Creek, CA 94598.
9
Daniel K. Inouye Center for Microbial Oceanography, University of Hawaii, Manoa, Honolulu, HI 96822.
10
Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA 93106.
11
Atmosphere & Ocean Research Institute, University of Tokyo, Chiba 277-8564, Japan; iwasaki@bs.s.u-tokyo.ac.jp azworden@geomar.de.
12
Department of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo 113-0032, Japan.
13
Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039; iwasaki@bs.s.u-tokyo.ac.jp azworden@geomar.de.

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.

KEYWORDS:

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

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