TY - JOUR
T1 - A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators
AU - Needham, David M.
AU - Yoshizawa, Susumu
AU - Hosaka, Toshiaki
AU - Poirier, Camille
AU - Choi, Chang Jae
AU - Hehenberger, Elisabeth
AU - Irwin, Nicholas A.T.
AU - Wilken, Susanne
AU - Yung, Cheuk Man
AU - Bachy, Charles
AU - Kurihara, Rika
AU - Nakajima, Yu
AU - Kojima, Keiichi
AU - Kimura-Someya, Tomomi
AU - Leonard, Guy
AU - Malmstrom, Rex R.
AU - Mende, Daniel R.
AU - Olson, Daniel K.
AU - Sudo, Yuki
AU - Sudek, Sebastian
AU - Richards, Thomas A.
AU - DeLong, Edward F.
AU - Keeling, Patrick J.
AU - Santoro, Alyson E.
AU - Shirouzu, Mikako
AU - Iwasaki, Wataru
AU - Worden, Alexandra Z.
N1 - Funding Information:
We thank the captain and crew of the R/V Western Flyer, and we thank M. Ares, L. G?mez-Consarnau, and K. Bergauer for discussions. We are grateful for the availability of Monterey Bay Time Series chlorophyll data through the Monterey Bay Aquarium Research Institute (MBARI). We thank a United States Department of Energy Joint Genome Institute Technology Development Program grant for some initial sequencing. Support came from the Canon Foundation (S.Y., T.H., T.K.-S., M.S., and W.I.), Japan Society for the Promotion of Science KAKENHI Grants 16H06279 (to S.Y. and W.I.) and 18H04136 (to S.Y. and W.I.), Gordon & Betty Moore Foundation Grants GBMF3307 (to T.A.R., P.J.K., A.E.S., and A.Z.W.) and GBMF3788 (to A.Z.W.), MBARI (A.Z.W.), and GEOMAR Helmholtz Centre for Ocean Research Kiel (A.Z.W.).
Funding Information:
ACKNOWLEDGMENTS. We thank the captain and crew of the R/V Western Flyer, and we thank M. Ares, L. Gómez-Consarnau, and K. Bergauer for discussions. We are grateful for the availability of Monterey Bay Time Series chlorophyll data through the Monterey Bay Aquarium Research Institute (MBARI). We thank a United States Department of Energy Joint Genome Institute Technology Development Program grant for some initial sequencing. Support came from the Canon Foundation (S.Y., T.H., T.K.-S., M.S., and W.I.), Japan Society for the Promotion of Science KAKENHI Grants 16H06279 (to S.Y. and W.I.) and 18H04136 (to S.Y. and W.I.), Gordon & Betty Moore Foundation Grants GBMF3307 (to T.A.R., P.J.K., A.E.S., and A.Z.W.) and GBMF3788 (to A.Z.W.), MBARI (A.Z.W.), and GEOMAR Helmholtz Centre for Ocean Research Kiel (A.Z.W.).
Publisher Copyright:
© 2019 National Academy of Sciences. All rights reserved.
PY - 2019
Y1 - 2019
N2 - 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.
AB - 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.
KW - Giant viruses
KW - Host–virus interactions
KW - Marine carbon cycle
KW - Single-cell genomics
KW - Viral evolution
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U2 - 10.1073/pnas.1907517116
DO - 10.1073/pnas.1907517116
M3 - Article
C2 - 31548428
AN - SCOPUS:85073052046
VL - 116
SP - 20574
EP - 20583
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
SN - 0027-8424
IS - 41
ER -