A distinct lineage of Caudovirales that encodes a deeply branching multi-subunit RNA polymerase

Weinheimer, Alaina R.; Aylward, Frank O.

doi:10.1038/s41467-020-18281-3

Cited by 14 publications

(11 citation statements)

References 55 publications

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“…We have previously proposed a similar scenario to explain the ubiquitous distribution of Topo VI in Archaea and the restricted distribution of Topo VIII (both members of the Topo IIB family) in some archaea and bacterial mobile elements (Gadelle et al 2014). In that scenario, the restricted distribution of Topo IIA to a few subgroups of Caudoviricetes seems surprising, but it resembles the restricted distribution of a recently described new version of RNA polymerase in a subgroup of these viruses (Weinheimer and Aylward 2020).…”

Section: Discussionmentioning

confidence: 82%

Viral origin of eukaryotic type IIA DNA topoisomerases

Guglielmini

Gaïa

Cunha³

et al. 2022

Preprint

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Type II DNA topoisomerases of the family A (Topo IIA) are present in all bacteria (DNA gyrase) and eukaryotes. In eukaryotes, they play a major role in transcription, DNA replication, chromosome segregation and modulation of chromosome architecture. The origin of eukaryotic Topo IIA remains mysterious since they are very divergent from their bacterial homologues and have no orthologues in Archaea. Interestingly, eukaryotic Topo IIA have close homologues in viruses of the phylum Nucleocytoviricota, an expansive assemblage of large and giant viruses formerly known as the nucleocytoplasmic large DNA viruses (NCLDV). Topo IIA are also encoded by some bacterioviruses of the class Caudoviricetes (tailed bacteriophages). To elucidate the origin of the eukaryotic Topo IIA, we performed in-depth phylogenetic analyses combining viral and cellular Topo IIA homologs. Topo IIA encoded by bacteria and eukaryotes form two monophyletic groups nested within Topo IIA encoded by Caudoviricetes and Nucleocytoviricota, respectively. Importantly, Nucleocytoviricota remained well separated from eukaryotes after removing both bacteria and Caudoviricetes from the dataset, indicating that the separation of Nucleocytoviricota and eukaryotes is probably not due to long branch attraction artefact. The topology of our tree suggests that the eukaryotic Topo IIA was probably acquired from an ancestral member of the Nucleocytoviricota of the class Megaviricetes, before the emergence of the last eukaryotic common ancestor (LECA). This result further highlights a key role of these viruses in eukaryogenesis and suggests that early proto-eukaryotes used a Topo IIB instead of a Topo IIA for solving their DNA topological problems.

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Section: Discussionmentioning

confidence: 82%

Viral origin of eukaryotic type IIA DNA topoisomerases

Guglielmini

Gaïa

Cunha³

et al. 2022

Preprint

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“…Inspection of the occurrence of these markers can be useful for determining if a sequence derives from NCLDV; for example, of the seven non-NCLDVs that had scores >0, none encoded proteins with matches to MCP, A32, VLTF3, mRNAc, PolB and D5 markers, although divergent hits with low scores were observed for SFII, and RNR homologs. None of these seven non-NCLDVs had hits to the RNA polymerase subunits RNAPL or RNAPS, but identification of these markers without subsequent phylogenetic analysis cannot be considered evidence of NCLDV provenance given the universal presence of these protein families in cellular life as well as some Caudovirales [52].…”

Section: Resultsmentioning

confidence: 99%

ViralRecall—A Flexible Command-Line Tool for the Detection of Giant Virus Signatures in ‘Omic Data

Aylward¹,

Moniruzzaman²

2021

Viruses

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Giant viruses are widespread in the biosphere and play important roles in biogeochemical cycling and host genome evolution. Also known as nucleo-cytoplasmic large DNA viruses (NCLDVs), these eukaryotic viruses harbor the largest and most complex viral genomes known. Studies have shown that NCLDVs are frequently abundant in metagenomic datasets, and that sequences derived from these viruses can also be found endogenized in diverse eukaryotic genomes. The accurate detection of sequences derived from NCLDVs is therefore of great importance, but this task is challenging owing to both the high level of sequence divergence between NCLDV families and the extraordinarily high diversity of genes encoded in their genomes, including some encoding for metabolic or translation-related functions that are typically found only in cellular lineages. Here, we present ViralRecall, a bioinformatic tool for the identification of NCLDV signatures in ‘omic data. This tool leverages a library of giant virus orthologous groups (GVOGs) to identify sequences that bear signatures of NCLDVs. We demonstrate that this tool can effectively identify NCLDV sequences with high sensitivity and specificity. Moreover, we show that it can be useful both for removing contaminating sequences in metagenome-assembled viral genomes as well as the identification of eukaryotic genomic loci that derived from NCLDV. ViralRecall is written in Python 3.5 and is freely available on GitHub: https://github.com/faylward/viralrecall.

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“…Although a wide variety of hypotheses have been proposed to explain the distinct cell membranes of bacteria and archaea and the early evolution of their metabolism, these remain controversial and progress has been constrained by the limited availability of relevant data ( Schoepp-Cothenet et al 2013 ; Sousa et al 2013 ; Sojo et al 2014 ; Russell and Nitschke 2017 ). It is generally assumed that the root in the TOL separates Archaea and Bacteria as inferred based on the use of ancient paralogous gene families for rooting ( Iwabe et al 1989 ; Brown and Doolittle 1995 ; Zhaxybayeva et al 2005 ; Weinheimer and Aylward 2020 ) and genome networks ( Dagan et al 2010 ) ( fig. 1 ).…”

Section: The Primary Domains Of Life and Deep Roots Of The Tolmentioning

confidence: 99%

“…Viruses and other MGEs are generally not considered part of the TOL ( Lopez-Garcia 2012 ), however the nature of their replication and propagation mechanisms have linked them to critical components of cellular genome dynamics and evolution. Recent efforts have tried to connect the deep origins and diversification of viruses to the earliest transitions in the TOL and diversification of cellular life ( Koonin et al 2020 ; Weinheimer and Aylward 2020 ; Irwin et al 2022 ). Parasitic replicators play important roles in host-parasite coevolutionary dynamics and the evolution of host genomes ( Koonin and Krupovic 2018 ) and have been placed at the centre of debates regarding eukaryotic evolution and diversification ( Koonin et al 2015 ; Forterre 2016 ; Guglielmini et al 2019 ; Moniruzzaman, Weinheimer et al 2020 ; Collens and Katz 2021 ; Irwin et al 2022 ).…”

Section: Viruses and The Tree Of Lifementioning

confidence: 99%

Evolving Perspective on the Origin and Diversification of Cellular Life and the Virosphere

Spang

Mahendrarajah

Offre

et al. 2022

Genome Biology and Evolution

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The tree of life (TOL) is a powerful framework to depict the evolutionary history of cellular organisms through time, from our microbial origins to the diversification of multicellular eukaryotes that shape the visible biosphere today. During the past decades, our perception of the TOL has fundamentally changed in part due to profound methodological advances which allowed a more objective approach to studying organismal and viral diversity and led to the discovery of major new branches in the TOL as well as viral lineages. Phylogenetic and comparative genomics analyses of this data have, among others, revolutionized our understanding of the deep roots and diversity of microbial life, the origin of the eukaryotic cell, eukaryotic diversity as well as the origin and diversification of viruses. In this review, we provide an overview of some of the recent discoveries on the evolutionary history of cellular organisms and their viruses and discuss a variety of complementary techniques that we consider crucial for making further progress in our understanding of the TOL and its interconnection with the virosphere.

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A distinct lineage of Caudovirales that encodes a deeply branching multi-subunit RNA polymerase

Cited by 14 publications

References 55 publications

Viral origin of eukaryotic type IIA DNA topoisomerases

Viral origin of eukaryotic type IIA DNA topoisomerases

ViralRecall—A Flexible Command-Line Tool for the Detection of Giant Virus Signatures in ‘Omic Data

Evolving Perspective on the Origin and Diversification of Cellular Life and the Virosphere

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