Taxon Richness of “Megaviridae” Exceeds those of Bacteria and Archaea in the Ocean

Mihara, Tomoko; Koyano, Hitoshi; Hingamp, Pascal; Grimsley, Nigel; Goto, Susumu; Ogata, Hiroyuki

doi:10.1264/jsme2.me17203

Cited by 94 publications

(80 citation statements)

References 93 publications

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“…The discovery of giant viruses in the early 21 st century has revived the debate on the nature of viruses and their role in evolution 1–13 . The 1µm-long particles of pithoviruses 14 can be seen under a light microscope and the 2.5Mb-long genomes of pandoraviruses, larger than those of many cellular organisms, encode for more than 2,000 proteins, mostly ORFans 15 .…”

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confidence: 99%

Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes

Guglielmini

Woo

Krupovìč

et al. 2018

Preprint

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9Giant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic 10Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially 11 ancient component of the eukaryotic virome. However, their origin(s), evolution and 12 potential roles in the emergence of modern eukaryotes remain a subject of intense 13 debate. Since the characterization of the mimivirus in 2003, many big and giant viruses 14 have been discovered at a steady pace, offering a vast material for evolutionary 15 investigations. In parallel, phylogenetic tools are constantly being improved, offering 16 more rigorous approaches for reconstruction of deep evolutionary history of viruses 17 and their hosts. Here we present robust phylogenetic trees of NCLDVs, based on the 8 18 most conserved proteins responsible for virion morphogenesis and informational 19 processes. Our results uncover the evolutionary relationships between different NCLDV 20 families and support the existence of two superclades of NCLDVs, each encompassing 21 several families. We present evidence strongly suggesting that the NCLDV core genes, 22which are involved in both informational processes and virion formation, were acquired 23 vertically from a common ancestor. Among them, the largest subunits of the DNA-24 dependent RNA polymerase were seemingly transferred from two clades of NCLDVs to 25 7 125The core markers share a similar phylogenetic signal 126Using a maximum-likelihood (ML) framework, the monophyly of all known 127 NCLDV families, except the Phycodnaviridae, was obtained with high support in most of 128 the 8 single-protein phylogenetic trees ( Supplementary Figure 1). As often observed in 129 published NCLDV phylogenies 26 , Ascoviridae were however nested within the 130Iridoviridae in most trees. The grouping of the Mimiviridae with related unclassified 131 viruses with smaller genomes often referred to as the "extended Mimiviridae" 21 or more 132 recently the "Mesomimivirinae" 29 , was obtained in five out of the 8 trees. We will refer 133 to this grouping as the "Megavirales" putative order (see Supplementary Information). 134 135The Poxviridae clade consistently formed a long branch and displayed the most 136 unstable position, branching next to various families (see Supplementary Information). 137

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mentioning

confidence: 99%

Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes

Guglielmini

Woo

Krupovìč

et al. 2018

Preprint

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“…However, this is in stark contrast to genomes of large and giant viruses of the NCLDV, which can be up to several megabases (Abergel et al, 2015;Fischer, 2016) . Importantly, recent studies showed that these viruses are among the most diverse and abundant entities in marine systems (Hingamp et al, 2013;Mihara et al, 2018) and are also found in a wide range of non-marine ecosystems (Graham et al, 2019;Kerepesi and Grolmusz, 2017;Roux et al, 2017;Schulz et al, 2018Schulz et al, , 2017bVavourakis et al, 2016) .…”

Section: Introductionmentioning

confidence: 99%

Advantages and limits of metagenomic assembly and binning of a giant virus

Schulz

Andréani

Francis

et al. 2020

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Giant viruses have large genomes, often within the size range of cellular organisms. This distinguishes them from most other viruses and demands additional effort for the successful recovery of their genomes from environmental sequence data. Here we tested the performance of genome-resolved metagenomics on a recently isolated giant virus, Fadolivirus, by spiking it into an environmental sample from which two other giant viruses were isolated. At high spike-in levels, metagenome assembly and binning led to the successful genomic recovery of Fadolivirus from the sample. A complementary survey of viral hallmark genes indicated the presence of other giant viruses in the sample matrix, but did not detect the two isolated from this sample. Our results indicate that genome-resolved metagenomics is a valid approach for the recovery of near-complete giant virus genomes given that sufficient clonal particles are present. Our data also underline that a vast majority of giant viruses remain currently undetected, even in an era of terabase-scale metagenomics.

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“…The investigation 100 of eukaryotic viruses based on environmental genomics has long been difficult because of 101 their lower concentration in the water column compared with prokaryotic dsDNA viruses 102 (Hingamp et al 2013). Deep sequencing of planktonic community DNA and RNA, as 103 carried out in Tara Oceans, has enabled the identification of marker genes of major viral 104 groups infecting eukaryotes and begun to reveal that these groups represent a sizeable 105 fraction of the marine virosphere (Hingamp et al 2013;Allen et al 2017;Moniruzzaman 106 et al 2017;Carradec et al 2018;Mihara et al 2018). In the present study, we identified 107 several hundred marker-gene sequences of nucleocytoplasmic large DNA viruses 108 (NCLDVs; so-called "giant viruses") in the prokaryotic size fraction.…”

Section: Introductionmentioning

confidence: 99%

Eukaryotic virus composition can predict the efficiency of carbon export in the global ocean

Blanc-Mathieu

Kaneko

Endo

et al. 2019

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32The biological carbon pump (BCP) is the process by which ocean organisms transfer 33 carbon from surface waters to the ocean interior and seafloor sediments for sequestration. 34Viruses are thought to increase the efficiency of the BCP by fostering primary production 35 and facilitating the export of carbon-enriched materials in the deep sea (the viral "shunt 36 and pump"). A prior study using an oligotrophic ocean-dominated dataset from the Tara 37Oceans expedition revealed that bacterial dsDNA viruses are better associated with 38 variation in carbon export than either prokaryotes or eukaryotes, but eukaryotic viruses 39were not examined. Because eukaryotes contribute significantly to ocean biomass and net 40 production (> 40%), their viruses might also play a role in the BCP. Here, we leveraged 41 deep-sequencing molecular data generated in the framework of Tara Oceans to identify 42 and quantify diverse lineages of large dsDNA and smaller RNA viruses of eukaryotes. 43We found that the abundance of these viruses explained 49% of the variation in carbon 44 export (compared with 89% by bacterial dsDNA viruses) and also substantially explained 45 the variation in net primary production (76%) and carbon export efficiency (50%). 46Prasinoviruses infecting Mamiellales as well as Mimivirus relatives putatively infecting 47 haptophytes are among the eukaryotic virus lineages predicted to be the best contributors 48 to BCP efficiency. These findings collectively provide a first-level window into how 49 eukaryotic viruses impact the BCP and suggest that the virus-mediated shunt and pump 50 indeed plays a role. 51 52The oceanic biological carbon pump (BCP) is an organism-driven process by which 53 atmospheric carbon (i.e. CO 2 ) is transferred to the ocean interior and seafloor for 54 sequestration over periods ranging from centuries to those of geological time-scale 55 durations. Between 15% and 20% of net primary production (NPP) is exported out of the 56 euphotic zone, with 1% to 3% (ca. 0.2 gigatons) of fixed carbon reaching the seafloor 57 annually (De La Rocha and Passow 2007;Herndl and Reinthaler 2013; Quéré et al. 2018; 58 Zhang et al. 2018). 59

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Taxon Richness of “Megaviridae” Exceeds those of Bacteria and Archaea in the Ocean

Cited by 94 publications

References 93 publications

Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes

Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes

Advantages and limits of metagenomic assembly and binning of a giant virus

Eukaryotic virus composition can predict the efficiency of carbon export in the global ocean

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