Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism

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, molliviruse...

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Autores principales:	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
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	giant viruses nucleocytoplasmic large DNA viruses deep sea sediments metagenomics virus evolution Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/45878f848eff4062a742aa46adc00f26
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spelling	oai:doaj.org-article:45878f848eff4062a742aa46adc00f262021-11-15T15:55:25ZVirus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism10.1128/mBio.02497-182150-7511https://doaj.org/article/45878f848eff4062a742aa46adc00f262019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02497-18https://doaj.org/toc/2150-7511ABSTRACT 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 related to pithoviruses, 5 to marseilleviruses, 1 to iridoviruses, and 2 to klosneuviruses. Some of the identified pithovirus-like and marseillevirus-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, including putative giant members of the family Marseilleviridae, have a broad range of apparent genome sizes, in agreement with the multiple, independent origins of gigantism in different branches of the NCLDV. Phylogenomic analysis reaffirms the monophyly of the pithovirus-iridovirus-marseillevirus branch of the NCLDV. Similarly to other giant viruses, the pithovirus-like viruses from Loki’s Castle encode translation systems components. Phylogenetic analysis of these genes indicates a greater bacterial contribution than had been detected previously. Genome comparison suggests extensive gene exchange between members of the pithovirus-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 are two 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 diversity of the nucleocytoplasmic large DNA viruses of eukaryotes. The results support the concept of independent evolution of giant viruses from smaller ancestors in different virus branches.Disa BäckströmNatalya YutinSteffen L. JørgensenJennah DharamshiFelix HomaKatarzyna Zaremba-NiedwiedzkaAnja SpangYuri I. WolfEugene V. KooninThijs J. G. EttemaAmerican Society for Microbiologyarticlegiant virusesnucleocytoplasmic large DNA virusesdeep sea sedimentsmetagenomicsvirus evolutionMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	giant viruses nucleocytoplasmic large DNA viruses deep sea sediments metagenomics virus evolution Microbiology QR1-502
spellingShingle	giant viruses nucleocytoplasmic large DNA viruses deep sea sediments metagenomics virus evolution Microbiology QR1-502 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 Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism
description	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 related to pithoviruses, 5 to marseilleviruses, 1 to iridoviruses, and 2 to klosneuviruses. Some of the identified pithovirus-like and marseillevirus-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, including putative giant members of the family Marseilleviridae, have a broad range of apparent genome sizes, in agreement with the multiple, independent origins of gigantism in different branches of the NCLDV. Phylogenomic analysis reaffirms the monophyly of the pithovirus-iridovirus-marseillevirus branch of the NCLDV. Similarly to other giant viruses, the pithovirus-like viruses from Loki’s Castle encode translation systems components. Phylogenetic analysis of these genes indicates a greater bacterial contribution than had been detected previously. Genome comparison suggests extensive gene exchange between members of the pithovirus-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 are two 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 diversity of the nucleocytoplasmic large DNA viruses of eukaryotes. The results support the concept of independent evolution of giant viruses from smaller ancestors in different virus branches.
format	article
author	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
author_facet	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
author_sort	Disa Bäckström
title	Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism
title_short	Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism
title_full	Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism
title_fullStr	Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism
title_full_unstemmed	Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism
title_sort	virus genomes from deep sea sediments expand the ocean megavirome and support independent origins of viral gigantism
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/45878f848eff4062a742aa46adc00f26
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Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism

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