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Virus genomes from deep sea sediments expand the ocean megavirome and support independent origins of viral gigantism

Disa Bäckström, Natalya Yutin, Steffen L. Jørgensen, Jennah Dharamshi, Felix Homa, Katarzyna Zaremba-Niedwiedzka, Anja Spang, Yuri I. Wolf, View ORCID ProfileEugene V. Koonin, Thijs J. G. Ettema
doi: https://doi.org/10.1101/469403
Disa Bäckström
1Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, Box 596, Uppsala SE-75123, Sweden
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Natalya Yutin
2National Center for Biotechnology Information, National Library of Medicine. National Institutes of Health, Bethesda, MD 20894, USA
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Steffen L. Jørgensen
3Department of Biology, Centre for Geobiology, University of Bergen, N-5020 Bergen, Norway
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Jennah Dharamshi
1Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, Box 596, Uppsala SE-75123, Sweden
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Felix Homa
1Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, Box 596, Uppsala SE-75123, Sweden
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Katarzyna Zaremba-Niedwiedzka
1Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, Box 596, Uppsala SE-75123, Sweden
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Anja Spang
1Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, Box 596, Uppsala SE-75123, Sweden
4NIOZ, Royal Netherlands Institute for Sea Research, Department of Marine Microbiology and Biogeochemistry, and Utrecht University, P.O. Box 59, NL-1790 AB Den Burg, The Netherlands
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Yuri I. Wolf
2National Center for Biotechnology Information, National Library of Medicine. National Institutes of Health, Bethesda, MD 20894, USA
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Eugene V. Koonin
2National Center for Biotechnology Information, National Library of Medicine. National Institutes of Health, Bethesda, MD 20894, USA
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  • ORCID record for Eugene V. Koonin
  • For correspondence: koonin@ncbi.nlm.nih.gov thijs.ettema@icm.uu.se
Thijs J. G. Ettema
1Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, Box 596, Uppsala SE-75123, Sweden
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  • For correspondence: koonin@ncbi.nlm.nih.gov thijs.ettema@icm.uu.se
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Abstract

The Nucleocytoplasmic Large DNA Viruses (NCLDV) of eukaryotes (proposed order ”Megavirales”) include the families Poxviridae, Asfarviridae, Iridoviridae, Ascoviridae, Phycodnaviridae, Marseilleviridae, and Mimiviridae, as well as still unclassified Pithoviruses, Pandoraviruses, Molliviruses and Faustoviruses. Several of these virus groups include giant viruses, with genome and particle sizes exceeding those of many bacterial and archaeal cells. We explored the diversity of the NCLDV in deep-sea sediments from the Loki’s Castle hydrothermal vent area. Using metagenomics, we reconstructed 23 high quality genomic bins of novel NCLDV, 15 of which are closest related to Pithoviruses, 5 to Marseilleviruses, 1 to Iridoviruses, and 2 to Klosneuviruses. Some of the identified Pitho-like and Marseille-like genomes belong to deep branches in the phylogenetic tree of core NCLDV genes, substantially expanding the diversity and phylogenetic depth of the respective groups. The discovered viruses have a broad range of apparent genome sizes including putative giant members of the family Marseilleviridae, in agreement with multiple, independent origins of gigantism in different branches of the NCLDV. Phylogenomic analysis reaffirms the monophyly of the Pitho-Irido-Marseille branch of NCLDV. Similarly to other giant viruses, the Pitho-like viruses from Loki’s Castle encode translation systems components. Phylogenetic analysis of these genes indicates a greater bacterial contribution than detected previously. Genome comparison suggests extensive gene exchange between members of the Pitho-like viruses and Mimiviridae. Further exploration of the genomic diversity of “Megavirales” in additional sediment samples is expected to yield new insights into the evolution of giant viruses and the composition of the ocean megavirome.

Importance Genomics and evolution of giant viruses is one of the most vigorously developing areas of virus research. Lately, metagenomics has become the main source of new virus genomes. Here we describe a metagenomic analysis of the genomes of large and giant viruses from deep sea sediments. The assembled new virus genomes substantially expand the known diveristy of the Nucleo-Cytoplasmic Large DNA Viruses of eukaryotes. The results support the concept of independent evolution of giant viruses from smaller ancestors in different virus branches.

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Posted November 14, 2018.
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Virus genomes from deep sea sediments expand the ocean megavirome and support independent origins of viral gigantism
Disa Bäckström, Natalya Yutin, Steffen L. Jørgensen, Jennah Dharamshi, Felix Homa, Katarzyna Zaremba-Niedwiedzka, Anja Spang, Yuri I. Wolf, Eugene V. Koonin, Thijs J. G. Ettema
bioRxiv 469403; doi: https://doi.org/10.1101/469403
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Virus genomes from deep sea sediments expand the ocean megavirome and support independent origins of viral gigantism
Disa Bäckström, Natalya Yutin, Steffen L. Jørgensen, Jennah Dharamshi, Felix Homa, Katarzyna Zaremba-Niedwiedzka, Anja Spang, Yuri I. Wolf, Eugene V. Koonin, Thijs J. G. Ettema
bioRxiv 469403; doi: https://doi.org/10.1101/469403

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