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A persistent giant algal virus, with a unique morphology, encodes an unprecedented number of genes involved in energy metabolism

View ORCID ProfileRomain Blanc-Mathieu, Håkon Dahle, Antje Hofgaard, David Brandt, Hiroki Ban, Jörn Kalinowski, Hiroyuki Ogata, Ruth-Anne Sandaa
doi: https://doi.org/10.1101/2020.07.30.228163
Romain Blanc-Mathieu
1Institute for Chemical Research, Kyoto University, Gokasho, Uji, 611-0011, Japan
2Laboratoire de Physiologie Cellulaire & Végétale, CEA, Univ. Grenoble Alpes, CNRS, INRA, IRIG, Grenoble, France
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  • ORCID record for Romain Blanc-Mathieu
Håkon Dahle
3Department of Biological Sciences and K.G. Jebsen Center for Deep Sea Research, University of Bergen, Bergen, Norway
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Antje Hofgaard
4Department of Biosciences, University of Oslo, Norway
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David Brandt
5Center for Biotechnology, Universität Bielefeld, Bielefeld, 33615, Germany
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Hiroki Ban
1Institute for Chemical Research, Kyoto University, Gokasho, Uji, 611-0011, Japan
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Jörn Kalinowski
5Center for Biotechnology, Universität Bielefeld, Bielefeld, 33615, Germany
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Hiroyuki Ogata
1Institute for Chemical Research, Kyoto University, Gokasho, Uji, 611-0011, Japan
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Ruth-Anne Sandaa
6Department of Biological Sciences, University of Bergen, Bergen, Norway
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  • For correspondence: ruth.sandaa@uib.no
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Abstract

Viruses have long been viewed as entities possessing extremely limited metabolic capacities. Over the last decade, however, this view has been challenged, as metabolic genes have been identified in viruses possessing large genomes and virions—the synthesis of which is energetically demanding. Here, we unveil peculiar phenotypic and genomic features of Prymnesium kappa virus RF01 (PkV RF01), a giant virus of the Mimiviridae family. We found that this virus encodes an unprecedented number of proteins involved in energy metabolism, such as all four succinate dehydrogenase (SDH) subunits (A–D) as well as key enzymes in the β-oxidation pathway. The SDHA gene was transcribed upon infection, indicating that the viral SDH is actively used by the virus— potentially to modulate its host’s energy metabolism. We detected orthologous SDHA and SDHB genes in numerous genome fragments from uncultivated marine Mimiviridae viruses, which suggests that the viral SDH is widespread in oceans. PkV RF01 was less virulent compared with other cultured prymnesioviruses, a phenomenon possibly linked to the metabolic capacity of this virus and suggestive of relatively long co-evolution with its hosts. It also has a unique morphology, compared to other characterized viruses in the Mimiviridae family. Finally, we found that PkV RF01 is the only alga-infecting Mimiviridae virus encoding two aminoacyl-tRNA synthetases and enzymes corresponding to an entire base-excision repair pathway, as seen in heterotroph-infecting Mimiviridae. These Mimiviridae encoded-enzymes were found to be monophyletic and branching at the root of the eukaryotic tree of life. This placement suggests that the last common ancestor of Mimiviridae was endowed with a large, complex genome prior to the divergence of known extant eukaryotes.

Importance Viruses on Earth are tremendously diverse in terms of morphology, functionality, and genomic composition. Over the last decade, the conceptual gap separating viruses and cellular life has tightened because of the detection of metabolic genes in viral genomes that express complex virus phenotypes upon infection. Here, we describe Prymnesium kappa virus RF01, a large alga-infecting virus with a unique morphology, an atypical infection profile, and an unprecedented number of genes involved in energy metabolism (such as the tricarboxylic (TCA) cycle and the β-oxidation pathway). Moreover, we show that the gene corresponding to one of these enzymes (the succinate dehydrogenase subunit A) is transcribed during infection and is widespread among marine viruses. This discovery provides evidence that a virus has the potential to actively regulate energy metabolism with its own gene.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/RomainBlancMathieu/PkV-RF01

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 13, 2021.
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A persistent giant algal virus, with a unique morphology, encodes an unprecedented number of genes involved in energy metabolism
Romain Blanc-Mathieu, Håkon Dahle, Antje Hofgaard, David Brandt, Hiroki Ban, Jörn Kalinowski, Hiroyuki Ogata, Ruth-Anne Sandaa
bioRxiv 2020.07.30.228163; doi: https://doi.org/10.1101/2020.07.30.228163
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A persistent giant algal virus, with a unique morphology, encodes an unprecedented number of genes involved in energy metabolism
Romain Blanc-Mathieu, Håkon Dahle, Antje Hofgaard, David Brandt, Hiroki Ban, Jörn Kalinowski, Hiroyuki Ogata, Ruth-Anne Sandaa
bioRxiv 2020.07.30.228163; doi: https://doi.org/10.1101/2020.07.30.228163

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