A Puzzling Anomaly in the 4-Mer Composition of the Giant Pandoravirus Genomes Reveals a Stringent New Evolutionary Selection Process

Poirot, Olivier; Jeudy, Sandra; Abergel, Chantal; Claverie, Jean‐Michel

doi:10.1128/jvi.01206-19

Cited by 8 publications

(6 citation statements)

References 39 publications

(59 reference statements)

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“…The evolutionary mechanism causing the elimination of this motif is still mysterious. One of the rejected hypothesis was that a R-M system targeting AGCT sites could be involved (77). Our methylome data consistently confirm that the AGCT motif is not methylated in the pandoraviruses of neither clade A nor B (Fig.…”

Section: Discussionsupporting

confidence: 66%

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The DNA Methylation Landscape of Giant Viruses

Jeudy

Rigou

Alempic

et al. 2019

Preprint

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DNA methylation is an important epigenetic mark that contributes to various regulations in all domains of life. Prokaryotes use it through Restriction-Modification (R-M) systems as a host-defense mechanism against viruses. The recently discovered giant viruses are widespread dsDNA viruses infecting eukaryotes with gene contents overlapping the cellular world. While they are predicted to encode DNA methyltransferases (MTases), virtually nothing is known about the DNA methylation status of their genomes. Using single-molecule real-time sequencing we studied the complete methylome of a large spectrum of families: the Marseilleviridae, the Pandoraviruses, the Molliviruses, the Mimiviridae along with their associated virophages and transpoviron, the Pithoviruses and the Cedratviruses (of which we report a new strain). Here we show that DNA methylation is widespread in giant viruses although unevenly distributed. We then identified the corresponding viral MTases, all of which are of bacterial origins and subject to intricate gene transfers between bacteria, viruses and their eukaryotic host. If some viral MTases undergo pseudogenization, most are conserved, functional and under purifying selection, suggesting that they increase the viruses' fitness. While the Marseilleviridae, Pithoviruses and Cedratviruses DNA MTases catalyze N 6 -methyl-adenine modifications, some MTases of Molliviruses and Pandoraviruses unexpectedly catalyze the formation of N 4 -methyl-cytosine modifications. In Marseilleviridae, encoded MTases are paired with cognate restriction endonucleases (REases) forming complete R-M systems. Our data suggest that giant viruses MTases could be involved in different kind of virus-virus interactions during coinfections.

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Section: Discussionsupporting

confidence: 66%

“…It was recently discovered that the AGCT tetramer is specifically eliminated from the Pandoraviruses' genomes, in particular the ones belonging to the A-clade (77). The evolutionary mechanism causing the elimination of this motif is still mysterious.…”

Section: Discussionmentioning

confidence: 99%

The DNA Methylation Landscape of Giant Viruses

Jeudy

Rigou

Alempic

et al. 2019

Preprint

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“…It was recently discovered that the AGCT tetramer is specifically eliminated from the pandoraviruses' genomes, in particular the ones belonging to the A-clade 59 . The evolutionary mechanism causing the elimination of this motif is still mysterious.…”

Section: Discussionmentioning

confidence: 99%

“…The evolutionary mechanism causing the elimination of this motif is still mysterious. One of the rejected hypothesis was that a R-M system targeting AGCT sites could be involved 59 . Our methylome data consistently confirm that the AGCT motif is not methylated in the pandoraviruses of neither clade A nor B ( Supplementary Fig.…”

Section: Discussionmentioning

confidence: 99%

The DNA methylation landscape of giant viruses

Jeudy¹,

Rigou²,

Alempic³

et al. 2020

Nat Commun

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DNA methylation is an important epigenetic mark that contributes to various regulations in all domains of life. Giant viruses are widespread dsDNA viruses with gene contents overlapping the cellular world that also encode DNA methyltransferases. Yet, virtually nothing is known about the methylation of their DNA. Here, we use single-molecule real-time sequencing to study the complete methylome of a large spectrum of giant viruses. We show that DNA methylation is widespread, affecting 2/3 of the tested families, although unevenly distributed. We also identify the corresponding viral methyltransferases and show that they are subject to intricate gene transfers between bacteria, viruses and their eukaryotic host. Most methyltransferases are conserved, functional and under purifying selection, suggesting that they increase the viruses' fitness. Some virally encoded methyltransferases are also paired with restriction endonucleases forming Restriction-Modification systems. Our data suggest that giant viruses' methyltransferases are involved in diverse forms of viruspathogens interactions during coinfections.

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“…Pandoraviruses remain the most enigmatic of giant viruses infecting Acanthamoeba spp . with the largest known viral genomes (a linear DNA molecule up to 2.6 Mb) [48, 49], a puzzling bias in their nucleotidic 4-mer composition [50], the largest proportion of protein-coding genes of unknown origins [49, 51], and the apparent capacity to create such genes de novo from non-coding DNA segments at a relatively high frequency [49, 51]. This study is the first to document their presence in ancient soils, in contrast with their scarcity in metagenomic data [52].…”

Section: Resultsmentioning

confidence: 99%

An update on eukaryotic viruses revived from ancient permafrost

Alempic

Lartigue

Гончаров

et al. 2022

Preprint

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One quarter of the Northern hemisphere is underlain by permanently frozen ground, referred to as permafrost. Due to climate warming, irreversibly thawing permafrost is releasing organic matter frozen for up to a million years, most of which decomposes into carbon dioxide and methane, further enhancing the greenhouse effect. Part of this organic matter also consists of revived cellular microbes (prokaryotes, unicellular eukaryotes) as well as viruses that remained dormant since prehistorical times. While the literature abounds on descriptions of the rich and diverse prokaryotic microbiomes found in permafrost, no additional report about live viruses have been published since the two original studies describing pithovirus (in 2014) and mollivirus (in 2015). This wrongly suggests that such occurrences are rare and that zombie viruses are not a public health threat. To restore an appreciation closer to reality, we report the preliminary characterizations of 13 new viruses isolated from 7 different ancient Siberian permafrost samples, 1 from the Lena river and 1 from Kamchatka cryosol. As expected from the host specificity imposed by our protocol, these viruses belong to 5 different clades infecting Acanthamoeba spp. but not previously revived from permafrost: pandoravirus, cedratvirus, megavirus, and pacmanvirus, in addition to a new pithovirus strain.

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A Puzzling Anomaly in the 4-Mer Composition of the Giant Pandoravirus Genomes Reveals a Stringent New Evolutionary Selection Process

Cited by 8 publications

References 39 publications

The DNA Methylation Landscape of Giant Viruses

The DNA Methylation Landscape of Giant Viruses

The DNA methylation landscape of giant viruses

An update on eukaryotic viruses revived from ancient permafrost

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