mRNA maturation in giant viruses: variation on a theme

Priet, Stéphane; Lartigue, Audrey; Debart, Françoise; Claverie, Jean‐Michel; Abergel, Chantal

doi:10.1093/nar/gkv224

Cited by 19 publications

(22 citation statements)

References 68 publications

(92 reference statements)

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“…structures were detected in the 3' UTR of most putative transcripts (Priet et al, 2015). They are 191 probably recognized and processed by the viral encoded RNase III in a manner similar to APMV (Byrne et 192 al., 2009).…”

Section: Virus Morphology and Replication Kinetics Transmission Elecmentioning

confidence: 99%

The kinetoplastid-infecting Bodo saltans virus (BsV), a window into the most abundant giant viruses in the sea

Deeg

Chow

Suttle

2017

Preprint

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Section: Virus Morphology and Replication Kinetics Transmission Elecmentioning

confidence: 99%

The kinetoplastid-infecting Bodo saltans virus (BsV), a window into the most abundant giant viruses in the sea

Deeg

Chow

Suttle

2017

Preprint

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“…Mimiviruses are unique in their association with two distinct (often co-existing) dependent entities, virophages and transpovirons, somewhat reminiscent of phages and plasmids afflicting bacteria. As for the virophage, the presence of host virus-like regulatory elements (terminator hairpin, late promoter (31–34)) flanking the transpoviron genes suggest that they also use the host virus transcription machinery rather than that of the cell. The transpoviron might also rely on the host virus DNA replication machinery, in absence of transpoviron-encoded DNA polymerase.…”

Section: Discussionmentioning

confidence: 99%

Commensalism in theMimiviridaegiant virus family

Jeudy

Bertaux

Alempic

et al. 2019

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22Acanthamoeba-infecting Mimiviridae belong to three clades: Mimiviruses (A), Moumouviruses (B) 23and Megaviruses (C). The uniquely complex mobilome of these giant viruses includes virophages and 24 linear 7 kb-DNA molecules called "transpovirons". We recently isolated a virophage (Zamilon vitis) 25 and two transpovirons (ma B tv and mv C tv) respectively associated to B-clade and C-clade mimiviruses. 26We used the capacity of the Zamilon virophage to replicate both on B-clade and C-clade host viruses 27 to investigate the three partite interaction network governing the propagation of transpovirons. We 28 found that the virophage could transfer both types of transpovirons to B-clade and C-clade host 29 viruses provided they were devoid of a resident transpoviron (permissive effect). If not, only the 30 resident transpoviron was replicated and propagated within the virophage progeny (dominance 31 effect). Although B-and C-clade viruses devoid of transpoviron could replicate both ma B tv and mv C tv, 32 they did it with a lower efficiency across clades, suggesting an ongoing process of adaptive co-33 evolution. We performed proteomic comparisons of host viruses and virophage particles carrying or 34 cleared of transpovirons in search of proteins involved in this adaptation process. These experiments 35 revealed that transpoviron-encoded proteins are synthetized during the combined 36 mimiviruses/virophage/transpoviron replication process and some of them are specifically 37 incorporated into the virophage and giant virus particles together with the cognate transpoviron 38 DNA. This study also highlights a unique example of intricate commensalism in the viral world, where 39 the transpoviron uses the virophage to propagate from one host virus to another and where the 40 Zamilon virophage and the transpoviron depend on their host giant virus to replicate, this without 41 affecting the giant virus infectious cycle, at least in laboratory conditions. 42 43 3 Author Summary 44 The Mimiviridae are giant viruses with dsDNA genome up to 1.5 Mb. They build huge viral factories in 45 the host cytoplasm in which the nuclear-like virus-encoded functions (transcription and replication) 46 take place. They are themselves the target of infections by 20 kb-dsDNA virophages, replicating in 47 the giant virus factories. They can also be found associated with 7kb-DNA episomes, dubbed 48 transpovirons. We investigated the relationship between these three players by combining 49 competition experiments involving the newly isolated Zamilon vitis virophage as a vehicle for 50 transpovirons of different origins with proteomics analyses of virophage and giant virus particles. Our 51 results suggest that relationship of the virophage, the transpoviron, and their host giant virus, extend 52 the concept of commensalism to the viral world. 53 54 55

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“…We also looked for mRNA methylases that could act as a protective mechanism for the viral transcript. A single one was described in another family of eukaryotic DNA virus: the product of the Megavirus Mg18 gene 22 . Again, no significant homolog of this protein was detected in the pandoraviruses.…”

Section: Discussionmentioning

confidence: 99%

A spectacular anomaly in the 4-mer composition of the giant pandoravirus genomes reveals a stringent new evolutionary selection process

Poirot

Jeudy

Abergel

et al. 2019

Preprint

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A spectacular anomaly in the 4-mer composition of the giant pandoravirus genomes 4 reveals a stringent new evolutionary selection process 5 6 Running title: Unique compositional anomaly in pandoraviruses 7 8 Abstract 19The Pandoraviridae is a rapidly growing family of giant viruses, all of which have been 20 isolated using laboratory strains of Acanthamoeba. The genomes of ten distinct strains 21 have been fully characterized, reaching up to 2.5 Mb in size. These double-stranded DNA 22 genomes encode the largest of all known viral proteomes and are propagated in oblate 23 virions that are among the largest ever-described (1.2 µm long and 0.5 µm wide). The 24 evolutionary origin of these atypical viruses is the object of numerous speculations. 25 Applying the Chaos Game Representation to the pandoravirus genome sequences, we 26 discovered that the tetranucleotide (4-mer) "AGCT" is totally absent from the genomes of 27 2 strains (P. dulcis and P. quercus) and strongly underrepresented in others. Given the 28 amazingly low probability of such an observation in the corresponding randomized 29 sequences, we investigated its biological significance through a comprehensive study of 30 the 4-mer compositions of all viral genomes. Our results indicate that "AGCT" was 31 specifically eliminated during the evolution of the Pandoraviridae and that none of the 32 previously proposed host-virus antagonistic relationships could explain this phenomenon. 33 Unlike the three other families of giant viruses (Mimiviridae, Pithoviridae, Molliviridae) 34 infecting the same Acanthamoeba host, the pandoraviruses exhibit a puzzling genomic 35 anomaly suggesting a highly specific DNA editing in response to a new kind of strong 36 evolutionary pressure. 37 Importance 38 The recent years have seen the discovery of several families of giant DNA viruses all 39 infecting the ubiquitous amoebozoa of the genus Acanthamoeba. With dsDNA genomes 40 reaching 2.5 Mb in length packaged in oblate particles the size of a bacterium, the 41 3 pandoraviruses are the most complex and largest viruses known as of today. In addition to 42 their spectacular dimensions, the pandoraviruses encode the largest proportion of proteins 43 without homolog in other organisms, thought to result from a de novo gene creation 44 process. While using comparative genomics to investigate the evolutionary forces 45 responsible for the emergence of such an unusual giant virus family, we discovered a 46 unique bias in the tetranucleotide composition of the pandoravirus genomes that can only 47 result from an undescribed evolutionary process not encountered in any other 48 microorganism. 49 50 The Pandoraviruses are among the growing number of families of environmental 51 giant DNA viruses infecting protozoans and isolated using the laboratory host 52 Acanthamoeba (Protozoa/Lobosa/Ameobida/ Acanthamoebidae/ Acanthamoeba) 1-4 . As of 53 today, they exhibit the largest fully characterized viral genomes, made of linear dsDNA 54 molecules from 1.9 to 2.5 Mb in size, predicted...

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mRNA maturation in giant viruses: variation on a theme

Cited by 19 publications

References 68 publications

The kinetoplastid-infecting Bodo saltans virus (BsV), a window into the most abundant giant viruses in the sea

The kinetoplastid-infecting Bodo saltans virus (BsV), a window into the most abundant giant viruses in the sea

Commensalism in theMimiviridaegiant virus family

A spectacular anomaly in the 4-mer composition of the giant pandoravirus genomes reveals a stringent new evolutionary selection process

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