In-depth study of
            <i>Mollivirus sibericum</i>
            , a new 30,000-y-old giant virus infecting
            <i>Acanthamoeba</i>

Legendre, Matthieu; Lartigue, Audrey; Bertaux, Lionel; Jeudy, Sandra; Bartoli, Julia; Lescot, Magali; Alempic, Jean-Marie; Ramus, Claire; Bruley, Christophe; Labadie, Karine; Shmakova, Lyubov; Rivkina, Elizaveta; Couté, Yohann; Abergel, Chantal; Claverie, Jean‐Michel

doi:10.1073/pnas.1510795112

Cited by 263 publications

(334 citation statements)

References 52 publications

(47 reference statements)

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“…This conclusion is well supported by classical studies which show that the phagocytosis process is triggered in Acanthamoeba by particles of Ͼ500 nm (8). Therefore, most of the giant viruses, such as mimivirus, pandoravirus, pithovirus, and mollivirus, meet this requirement (1)(2)(3)5). Marseillevirus marseillevirus (MsV) particles, on the other hand, are formed by 250-nm icosahedral capsids that do not reach the 500-nm size threshold (6).…”

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confidence: 58%

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The Large Marseillevirus Explores Different Entry Pathways by Forming Giant Infectious Vesicles

Arantes

Rodrigues

Silva

et al. 2016

J Virol

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Triggering the amoebal phagocytosis process is a sine qua non condition for most giant viruses to initiate their replication cycle and consequently to promote their progeny formation. It is well known that the amoebal phagocytosis process requires the recognition of particles of >500 nm, and most amoebal giant viruses meet this requirement, such as mimivirus, pandoravirus, pithovirus, and mollivirus. However, in the context of the discovery of amoebal giant viruses in the last decade, Marseillevirus marseillevirus (MsV) has drawn our attention, because despite its ability to successfully replicate in Acanthamoeba, remarkably it does not fulfill the >500-nm condition, since it presents an ϳ250-nm icosahedrally shaped capsid. We deeply investigated the MsV cycle by using a set of methods, including virological, molecular, and microscopic (immunofluorescence, scanning electron microscopy, and transmission electron microscopy) assays. Our results revealed that MsV is able to form giant vesicles containing dozens to thousands of viral particles wrapped by membranes derived from amoebal endoplasmic reticulum. Remarkably, our results strongly suggested that these giant vesicles are able to stimulate amoebal phagocytosis and to trigger the MsV replication cycle by an acidification-independent process. Also, we observed that MsV entry may occur by the phagocytosis of grouped particles (without surrounding membranes) and by an endosome-stimulated pathway triggered by single particles. Taken together, not only do our data deeply describe the main features of MsV replication cycle, but this is the first time, to our knowledge, that the formation of giant infective vesicles related to a DNA virus has been described. IMPORTANCETriggering the amoebal phagocytosis process is a sine qua non condition required by most giant viruses to initiate their replication cycle. This process requires the recognition of particles of >500 nm, and many giant viruses meet this requirement. However, MsV is unusual, as despite having particles of ϳ250 nm it is able to replicate in Acanthamoeba. Our results revealed that MsV is able to form giant vesicles, containing dozens to thousands of viral particles, wrapped in membranes derived from amoebal endoplasmic reticulum. Remarkably, our results strongly suggest that these giant vesicles are able to stimulate phagocytosis using an acidification-independent process. Our work not only describes the main features of the MsV replication cycle but also describes, for the first time to our knowledge, the formation of huge infective vesicles in a large DNA viruses. T he discovery of the amoebal giant virus Acanthamoeba polyphaga mimivirus (APMV) in 2003 (1) raised new and exciting questions regarding the virosphere and boosted the hunt for new giant viruses. Owing to these efforts, an increasing number of remarkable giant viruses have been described (2-6).Recent data suggest that giant viruses initiate their replication cycles after being phagocytosed by amoebas or other phagocytic cells (1, 7). Th...

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confidence: 58%

“…Owing to these efforts, an increasing number of remarkable giant viruses have been described (2)(3)(4)(5)(6).…”

mentioning

confidence: 99%

The Large Marseillevirus Explores Different Entry Pathways by Forming Giant Infectious Vesicles

Arantes

Rodrigues

Silva

et al. 2016

J Virol

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“…Finally, the presence of contemporary giant viruses, strictly comparable to fossil giant viruses, suggests that, for this viral group, there is no potential threat in the context of the resurrection of prehistoric human-infecting giant viruses, as previously suggested (Legendre et al 2015). …”

Section: Discussionmentioning

confidence: 55%

Comparison of a Modern and FossilPithovirusReveals Its Genetic Conservation and Evolution

et al. 2016

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Most theories on viral evolution are speculative and lack fossil comparison. Here, we isolated a modern Pithovirus-like virus from sewage samples. This giant virus, named Pithovirus massiliensis, was compared with its prehistoric counterpart, Pithovirus sibericum, found in Siberian permafrost. Our analysis revealed near-complete gene repertoire conservation, including horizontal gene transfer and ORFans. Furthermore, all orthologous genes evolved under strong purifying selection with a non-synonymous and synonymous ratio in the same range as the ratio found in the prokaryotic world. The comparison between fossil and modern Pithovirus species provided an estimation of the cadence of the molecular clock, reaching up to 3 × 10−6 mutations/site/year. In addition, the strict conservation of HGTs and ORFans in P. massiliensis revealed the stable genetic mosaicism in giant viruses and excludes the concept of a bag of genes. The genetic stability for 30,000 years of P. massiliensis demonstrates that giant viruses evolve similarly to prokaryotes by classical mechanisms of evolution, including selection and fixation of genes, followed by selective constraints.

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“…A large community of previously unknown viruses is emerging among the former nucleocytoplasmic large DNA viruses (NCLDV). We are witnessing a growing number of new isolates with extraordinary properties in gene content, particle resistance, and/or morphological appearance (3)(4)(5)(6)(7). Genome sequencing and advances in coculture isolation strategies have led to an increase in the discovery of new viruses (8,9).…”

mentioning

confidence: 99%

Pacmanvirus, a New Giant Icosahedral Virus at the Crossroads between Asfarviridae and Faustoviruses

Andréani

Khalil

Sevvana

et al. 2017

J Virol

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African swine fever virus, a double-stranded DNA virus that infects pigs, is the only known member of the Asfarviridae family. Nevertheless, during our isolation and sequencing of the complete genome of faustovirus, followed by the description of kaumoebavirus, carried out over the past 2 years, we observed the emergence of previously unknown related viruses within this group of viruses. Here we describe the isolation of pacmanvirus, a fourth member in this group, which is capable of infecting Acanthamoeba castellanii. Pacmanvirus A23 has a linear compact genome of 395,405 bp, with a 33.62% GϩC content. The pacmanvirus genome harbors 465 genes, with a high coding density. An analysis of reciprocal best hits shows that 31 genes are conserved between African swine fever virus, pacmanvirus, faustovirus, and kaumoebavirus. Moreover, the major capsid protein locus of pacmanvirus appears to be different from those of kaumoebavirus and faustovirus. Overall, comparative and genomic analyses reveal the emergence of a new group or cluster of viruses encompassing African swine fever virus, faustovirus, pacmanvirus, and kaumoebavirus.IMPORTANCE Pacmanvirus is a newly discovered icosahedral double-stranded DNA virus that was isolated from an environmental sample by amoeba coculture. We describe herein its structure and replicative cycle, along with genomic analysis and genomic comparisons with previously known viruses. This virus represents the third virus, after faustovirus and kaumoebavirus, that is most closely related to classical representatives of the Asfarviridae family. These results highlight the emergence of previously unknown double-stranded DNA viruses which delineate and extend the diversity of a group around the asfarvirus members.KEYWORDS giant viruses, pacmanvirus, Asfarviridae, Acanthamoeba castellanii, NCLDV, faustovirus, kaumoebavirus, African swine fever virus T he discovery impacts of "giant viruses," such as Acanthamoeba polyphaga mimivirus (1), pandoraviruses (2), and pithoviruses (3), and their interactions with the world of protists are very common and do not need a long introduction. A large community of previously unknown viruses is emerging among the former nucleocytoplasmic large DNA viruses (NCLDV). We are witnessing a growing number of new isolates with extraordinary properties in gene content, particle resistance, and/or morphological appearance (3-7). Genome sequencing and advances in coculture isolation strategies have led to an increase in the discovery of new viruses (8,9). Some NCLDV are well studied because of their role in infecting algae, in the case of Phycodnaviridae (10), or in swine and wild boar infections, in the case of members of the Asfarviridae (11). The

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In-depth study of Mollivirus sibericum , a new 30,000-y-old giant virus infecting Acanthamoeba

Cited by 263 publications

References 52 publications

The Large Marseillevirus Explores Different Entry Pathways by Forming Giant Infectious Vesicles

The Large Marseillevirus Explores Different Entry Pathways by Forming Giant Infectious Vesicles

Comparison of a Modern and FossilPithovirusReveals Its Genetic Conservation and Evolution

Pacmanvirus, a New Giant Icosahedral Virus at the Crossroads between Asfarviridae and Faustoviruses

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