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 SudekThomas A. Richards, Edward F. DeLong, Patrick J. Keeling, Alyson E. Santoro, Mikako Shirouzu, Wataru Iwasaki, Alexandra Z. Worden

Research output: Contribution to journalArticle

3 Citations (Scopus)

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 languageEnglish
Pages (from-to)20574-20583
Number of pages10
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number41
DOIs
Publication statusPublished - Jan 1 2019

Fingerprint

Rhodopsin
Mimiviridae
Oceans and Seas
Phycodnaviridae
Choanoflagellata
Metagenome
Genome
Proton Pumps
Metagenomics
Chitin
Sunlight
Energy Transfer
Eukaryotic Cells
Enzymes
Eukaryota
Genes
Polysaccharides
Ecosystem
Viruses
Bacteria

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 journalArticle

Needham, DM, Yoshizawa, S, Hosaka, T, Poirier, C, Choi, CJ, Hehenberger, E, Irwin, NAT, Wilken, S, Yung, CM, Bachy, C, Kurihara, R, Nakajima, Y, Kojima, K, Kimura-Someya, T, Leonard, G, Malmstrom, RR, Mende, DR, Olson, DK, Sudo, Y, Sudek, S, Richards, TA, DeLong, EF, Keeling, PJ, Santoro, AE, Shirouzu, M, Iwasaki, W & Worden, AZ 2019, 'A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators', Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 41, pp. 20574-20583. https://doi.org/10.1073/pnas.1907517116
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. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 41. pp. 20574-20583.
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AU - Choi, Chang Jae

AU - Hehenberger, Elisabeth

AU - Irwin, Nicholas A.T.

AU - Wilken, Susanne

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AU - Richards, Thomas A.

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