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.
| Original language | English |
|---|---|
| Pages (from-to) | 20574-20583 |
| Number of pages | 10 |
| Journal | Proceedings of the National Academy of Sciences of the United States of America |
| Volume | 116 |
| Issue number | 41 |
| DOIs | |
| Publication status | Published - Jan 1 2019 |
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Keywords
- Giant viruses
- Host–virus interactions
- Marine carbon cycle
- Single-cell genomics
- Viral evolution
ASJC Scopus subject areas
- General
Cite this
A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators. / 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.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 41, 01.01.2019, p. 20574-20583.Research output: Contribution to journal › Article
}
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.
PY - 2019/1/1
Y1 - 2019/1/1
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
UR - http://www.scopus.com/inward/record.url?scp=85073052046&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85073052046&partnerID=8YFLogxK
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 -