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

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 cellularmore » 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 fromMimiviridae. Our findings indicate that light-dependent energy transfer systems are likely common components of giant viruses of photosynthetic and phagotrophic unicellular marine eukaryotes.« less

Authors:
 [1]; ORCiD logo [2]; ORCiD logo [3];  [4];  [4]; ORCiD logo [4];  [5];  [1];  [4];  [1];  [6];  [2];  [6]; ORCiD logo [3];  [7];  [8];  [9];  [9]; ORCiD logo [6];  [1] more »;  [7]; ORCiD logo [9];  [5]; ORCiD logo [10];  [3]; ORCiD logo [11]; ORCiD logo [4] « less
+ Show Author Affiliations
  1. Monterey Bay Aquarium Research Inst., Moss Landing, CA (United States)
  2. Univ. of Tokyo, Chiba (Japan). Atmosphere & Ocean Research Inst.
  3. RIKEN Center for Biosystems Dynamics Research, Yokohama (Japan). Lab. for Protein Functional & Structural Biology
  4. Monterey Bay Aquarium Research Inst., Moss Landing, CA (United States); GEOMAR Helmholtz Centre for Ocean Research, Kiel (Germany)
  5. Univ. of British Columbia, Vancouver, BC (Canada)
  6. Okayama Univ. (Japan)
  7. Univ. of Exeter (United Kingdom). Living Systems Inst.
  8. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  9. Univ. of Hawaii, Honolulu, HI (United States). Daniel K. Inouye Center for Microbial Oceanography
  10. Univ. of California, Santa Barbara, CA (United States)
  11. Univ. of Tokyo, Chiba (Japan). Atmosphere & Ocean Research Inst.; Univ. of Tokyo (Japan). Dept. of Biological Sciences
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Canon Foundation; Japan Society for the Promotion of Science (JSPS); Gordon and Betty Moore Foundation; GEOMAR Helmholtz Centre for Ocean Research Kiel; Monterey Bay Aquarium Research Institute (MBARI)
OSTI Identifier:
1572060
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 116; Journal Issue: 41; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; giant viruses; viral evolution; marine carbon cycle; single-cell genomics; host–virus interactions

Citation Formats

Needham, David M., Yoshizawa, Susumu, Hosaka, Toshiaki, Poirier, Camille, Choi, Chang Jae, Hehenberger, Elisabeth, Irwin, Nicholas A. T., Wilken, Susanne, Yung, Cheuk-Man, Bachy, Charles, Kurihara, Rika, Nakajima, Yu, Kojima, Keiichi, Kimura-Someya, Tomomi, Leonard, Guy, Malmstrom, Rex R., Mende, Daniel R., Olson, Daniel K., Sudo, Yuki, Sudek, Sebastian, Richards, Thomas A., DeLong, Edward F., Keeling, Patrick J., Santoro, Alyson E., Shirouzu, Mikako, Iwasaki, Wataru, and Worden, Alexandra Z. A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators. United States: N. p., 2019. Web. doi:10.1073/pnas.1907517116.
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Needham, David M., Yoshizawa, Susumu, Hosaka, Toshiaki, Poirier, Camille, Choi, Chang Jae, Hehenberger, Elisabeth, Irwin, Nicholas A. T., Wilken, Susanne, Yung, Cheuk-Man, Bachy, Charles, Kurihara, Rika, Nakajima, Yu, Kojima, Keiichi, Kimura-Someya, Tomomi, Leonard, Guy, Malmstrom, Rex R., Mende, Daniel R., Olson, Daniel K., Sudo, Yuki, Sudek, Sebastian, Richards, Thomas A., DeLong, Edward F., Keeling, Patrick J., Santoro, Alyson E., Shirouzu, Mikako, Iwasaki, Wataru, & Worden, Alexandra Z. A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators. United States. https://doi.org/10.1073/pnas.1907517116
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Needham, David M., Yoshizawa, Susumu, Hosaka, Toshiaki, Poirier, Camille, Choi, Chang Jae, Hehenberger, Elisabeth, Irwin, Nicholas A. T., Wilken, Susanne, Yung, Cheuk-Man, Bachy, Charles, Kurihara, Rika, Nakajima, Yu, Kojima, Keiichi, Kimura-Someya, Tomomi, Leonard, Guy, Malmstrom, Rex R., Mende, Daniel R., Olson, Daniel K., Sudo, Yuki, Sudek, Sebastian, Richards, Thomas A., DeLong, Edward F., Keeling, Patrick J., Santoro, Alyson E., Shirouzu, Mikako, Iwasaki, Wataru, and Worden, Alexandra Z. Mon . "A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators". United States. https://doi.org/10.1073/pnas.1907517116. https://www.osti.gov/servlets/purl/1572060.
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@article{osti_1572060,
title = {A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators},
author = {Needham, David M. and Yoshizawa, Susumu and Hosaka, Toshiaki and Poirier, Camille and Choi, Chang Jae and Hehenberger, Elisabeth and Irwin, Nicholas A. T. and Wilken, Susanne and Yung, Cheuk-Man and Bachy, Charles and Kurihara, Rika and Nakajima, Yu and Kojima, Keiichi and Kimura-Someya, Tomomi and Leonard, Guy and Malmstrom, Rex R. and Mende, Daniel R. and Olson, Daniel K. and Sudo, Yuki and Sudek, Sebastian and Richards, Thomas A. and DeLong, Edward F. and Keeling, Patrick J. and Santoro, Alyson E. and Shirouzu, Mikako and Iwasaki, Wataru and Worden, Alexandra Z.},
abstractNote = {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 fromMimiviridae. Our findings indicate that light-dependent energy transfer systems are likely common components of giant viruses of photosynthetic and phagotrophic unicellular marine eukaryotes.},
doi = {10.1073/pnas.1907517116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 41,
volume = 116,
place = {United States},
year = {Mon Sep 23 00:00:00 EDT 2019},
month = {Mon Sep 23 00:00:00 EDT 2019}
}
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https://doi.org/10.1073/pnas.1907517116
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Marine diatom proteorhodopsins and their potential role in coping with low iron availability
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Photosynthesis genes in marine viruses yield proteins during host infection
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Marine viruses discovered via metagenomics shed light on viral strategies throughout the oceans
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Proteorhodopsin variability and distribution in the North Pacific Subtropical Gyre
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Phage puppet masters of the marine microbial realm
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Photoactive yellow protein, bacteriophytochrome, and sensory rhodopsin in purple phototrophic bacteria
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Proteorhodopsin photosystem gene expression enables photophosphorylation in a heterologous host
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Giant virus with a remarkable complement of genes infects marine zooplankton
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The Genome of Canarypox Virus
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We are not so special
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