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

Bäckström, Disa; Yutin, Natalya; Jørgensen, Steffen Leth; Dharamshi, Jennah E.; Homa, Félix; Zaremba-Niedwiedzka, Katarzyna; Spang, Anja; Wolf, Yuri I.; Koonin, Eugene V.; Ettema, Thijs J. G.

doi:10.1101/469403

Cited by 11 publications

(16 citation statements)

References 123 publications

(31 reference statements)

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“…S1 ). Significant BLASTp hits (evalues ranging from 1e−41 to 8e−6) against viruses were also obtained with genes from putative giant viruses whose genomes was assembled from metagenomes obtained from environmental samples 13–15 and from Cafeteria roenbergensis virus, a distant Mimivirus relative 16 . The 322 amino acid long tupanvirus protein exhibits the conserved MBL motif “HxHxDH” in amino acid positions 60-65.…”

Section: Resultsmentioning

confidence: 99%

A metallo-beta-lactamase with both beta-lactamase and ribonuclease activity is linked with traduction in giant viruses

Colson

Pinault

Azza

et al. 2019

Preprint

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25Enzymatic proteins with a metallo-beta-lactamase (MBL) fold have been essentially studied 26 in bacteria for their activity on beta-lactam antibiotics. However, the MBL fold is ancient and 27 highly conserved, and these proteins are capable of cleaving a broad range of substrates. It has 28 recently been shown that MBLs are present in a wide array of cellular organisms, including 29 eukaryotes and archaea. We show here that Tupanvirus deep ocean, a giant virus, also 30 encodes a protein with a MBL fold. Phylogeny showed its clustering with transfer 31 ribonucleases (RNases) and the presence of orthologs in other giant viruses, mainly those 32 harboring the largest sets of translation components. In addition, it suggests an ancient origin 33 for these genes and a transfer between giant viruses and Acanthamoeba spp., a host of many 34 giant viruses. Biologically, after its expression in Escherichia coli, the tupanvirus protein was 35 found to hydrolyse nitrocefin, a chromogenic beta-lactam. We also observed an hydrolysis of 36 penicillin G (10 µg/mL) and detected the metabolite of penicillin G hydrolysis, 37 benzylpenilloic acid. This was inhibited by sulbactam, a beta-lactamase inhibitor. In addition, 38we tested the degradation of single-stranded DNA, double-stranded DNA, and RNAs, and 39 observed a strong activity on RNAs from seven bacteria with G+C varying from 42% to 67%, 40 and from Acanthamoeba castellanii, the tupanvirus host. This was not inhibited by sulbactam 41 or ceftriaxone. RNase activity was estimated to be 0.45±0.15 mU/mg using a fluorescence-42 based assay. Our results still broaden the range of hosts of MBL fold proteins and 43 demonstrate that such protein can have dual beta-lactamase/nuclease activities. We suggest 44 that they should be annotated according to this finding to avoid further confusion. 45 46 3 TEXT 47 48

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Section: Resultsmentioning

confidence: 99%

A metallo-beta-lactamase with both beta-lactamase and ribonuclease activity is linked with traduction in giant viruses

Colson

Pinault

Azza

et al. 2019

Preprint

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“…This indicates clearly that viruses must be older than cellular life . At least with the discovery of mimiviruses (and other giant viruses), it might be plausible that giant viruses have cellular origins …”

Section: Viruses and Their Relativesmentioning

confidence: 99%

“…6,63,64 At least with the discovery of mimiviruses (and other giant viruses), it might be plausible that giant viruses have cellular origins. [65][66][67][68][69][70] We must constantly remember that viruses and subviral infectious genetic parasites are the most abundant biological agents on the planet. 71,72 They outnumber cellular life forms by 10 times, invade all cellular organisms, and serve as key agents in the generation of adaptive and innate immune systems, which are essential for the survival of cellular life forms since they are key for the capacity for self/nonself-differentiation.…”

Section: Viruses and Their Relativesmentioning

confidence: 99%

That is life: communicating RNA networks from viruses and cells in continuous interaction

Villarreal

Witzany²

2019

Annals of the New York Academy of Sciences

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All the conserved detailed results of evolution stored in DNA must be read, transcribed, and translated via an RNA‐mediated process. This is required for the development and growth of each individual cell. Thus, all known living organisms fundamentally depend on these RNA‐mediated processes. In most cases, they are interconnected with other RNAs and their associated protein complexes and function in a strictly coordinated hierarchy of temporal and spatial steps (i.e., an RNA network). Clearly, all cellular life as we know it could not function without these key agents of DNA replication, namely rRNA, tRNA, and mRNA. Thus, any definition of life that lacks RNA functions and their networks misses an essential requirement for RNA agents that inherently regulate and coordinate (communicate to) cells, tissues, organs, and organisms. The precellular evolution of RNAs occurred at the core of the emergence of cellular life and the question remained of how both precellular and cellular levels are interconnected historically and functionally. RNA networks and RNA communication can interconnect these levels. With the reemergence of virology in evolution, it became clear that communicating viruses and subviral infectious genetic parasites are bridging these two levels by invading, integrating, coadapting, exapting, and recombining constituent parts in host genomes for cellular requirements in gene regulation and coordination aims. Therefore, a 21st century understanding of life is of an inherently social process based on communicating RNA networks, in which viruses and cells continuously interact.

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“…Prokaryotic sequences are not color coded. It is worth noting that the Iridovirus sequence comes from a metagenomics assembly (33) and that its taxonomic assignment is uncertain when considering the best blast matchs againt NR of the ORFs encoded in the corresponding genomic contig (Fig. S9A).…”

Section: Motif Enrichment In Intergenic Regionsmentioning

confidence: 99%

“…These so-called "giant viruses" exhibit DNA genomes as large and complex as prokaryotes (21), or even parasitic eukaryotes (29). A growing body of metagenomics surveys shows that they are widespread on the planet in all kinds of environments (31)(32)(33)(34)(35)(36). The first family of giant viruses to be discovered, the Mimiviridae, have megabase-sized AT-rich linear genomes packaged in icosahedral capsids (21)(22)(23).…”

Section: Introductionmentioning

confidence: 99%

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

Cited by 11 publications

References 123 publications

A metallo-beta-lactamase with both beta-lactamase and ribonuclease activity is linked with traduction in giant viruses

A metallo-beta-lactamase with both beta-lactamase and ribonuclease activity is linked with traduction in giant viruses

That is life: communicating RNA networks from viruses and cells in continuous interaction

The DNA Methylation Landscape of Giant Viruses

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