A virophage cross-species infection through mutant selection represses giant virus propagation, promoting host cell survival

Mougari, Said; Chelkha, Nisrine; Sahmi-Bounsiar, Dehia; Pinto, Fabrizio Di; Colson, Philippe; Abrahão, Jônatas Santos; Scola, Bernard La

doi:10.1038/s42003-020-0970-9

Cited by 18 publications

(11 citation statements)

References 56 publications

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“…Therefore, we have not presently confirmed that there is a MIMIVIRE-like system in the cotonvirus genome as in the lineage A mimivirus genome ( 15 ). Additionally, we did not detect sequences highly homologous with those of virophages Sputnik ( 27 ) or Guarani ( 28 ) in the cotonvirus genome.…”

Section: Resultsmentioning

confidence: 57%

Morphological and Taxonomic Properties of the Newly Isolated Cotonvirus japonicus , a New Lineage of the Subfamily Megavirinae

Takahashi

Fukaya

Song

et al. 2021

J Virol

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Since 2003, various viruses from the subfamily Megavirinae in the family Mimiviridae have been isolated worldwide, including icosahedral mimiviruses and tailed tupanviruses. To date, the evolutionary relationship between tailed and non-tailed mimiviruses has not yet been elucidated. Here, we present the genomic and morphological features of a newly isolated giant virus, Cotonvirus japonicus (cotonvirus), belonging to the family Mimiviridae. It contains a linear double-stranded DNA molecule of 1.47 Mb, the largest among the reported viruses in the subfamily Megavirinae , excluding tupanviruses. Among its 1,306 predicted open reading frames, 1,149 (88.0%) were homologous to those of the family Mimiviridae . Several nucleocytoplasmic large DNA virus (NCLDV) core genes, aminoacyl-tRNA synthetase genes, and the host specificity of cotonvirus were highly similar to those of Mimiviridae lineages A, B, and C; however, lineage A was slightly closer to cotonvirus than to the others. Moreover, based on its genome size, the presence of two copies of 18S rRNA-like sequences, and period of infection cycle, cotonvirus is the most similar to the tupanviruses among the icosahedral mimiviruses. Interestingly, the cotonvirus utilizes Golgi apparatus-like vesicles for virion factory (VF) formation. Overall, we showed that cotonvirus is a novel lineage of the subfamily Megavirinae . Our findings support the diversity of icosahedral mimiviruses and provide mechanistic insights into the replication, VF formation, and evolution of the subfamily Mimivirinae . Importance We have isolated a new virus of an independent lineage belonging to the family Mimiviridae , subfamily Megavirinae , from the fresh water of a canal in Japan, named cotonvirus. In a proteomic tree, this new nucleocytoplasmic large DNA virus (NCLDV) is phylogenetically placed at the root of three lineages of the subfamily Megavirinae —lineages A (mimivirus), B (moumouvirus), and C (megavirus). Multiple genomic and phenotypic features of cotonvirus are similar to those of tupanviruses, rather than the A, B, or C lineages, and other genomic features and host specificity of cotonvirus are similar to those of the latter than the former. These results suggest that cotonvirus is a unique virus, with chimeric features of existing viruses of Megavirinae and uses Golgi apparatus-like vesicles of the host cells for virion factory (VF) formation. Thus, cotonvirus can provide novel insights into the evolution of mimiviruses and the underlying mechanisms of VF formation.

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Section: Resultsmentioning

confidence: 57%

Morphological and Taxonomic Properties of the Newly Isolated Cotonvirus japonicus , a New Lineage of the Subfamily Megavirinae

Takahashi

Fukaya

Song

et al. 2021

J Virol

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“…Virophages can play key roles in host defense against their associated giant viruses (Table 1; Berjón-Otero et al, 2019;Blanc et al, 2015;Fischer, 2015;Fischer & Hackl, 2016;Hackl et al, 2021;Koonin & Krupovic, 2016;Mougari et al, 2019Mougari et al, , 2020. While to the best of our knowledge, virophage-mediated defense has not yet been observed in ciliates, it is reasonable to speculate that it occurs.…”

Section: T R a Nsf Er Of V I R A L Dna I N To T H E C I L I At E Ge N...mentioning

confidence: 99%

Epigenetic influences of mobile genetic elements on ciliate genome architecture and evolution

Timmons

Shazib

Katz

2022

J Eukaryotic Microbiology

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“…2020 ). Virophages can parasitize co-infecting giant DNA viruses in a host and may provide adaptive anti-giant virus defence in unicellular eukaryotes ( Fischer and Hackl 2016 ; Duponchel and Fischer 2019 ; Mougari et al. 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Integrated viral elements suggest the dual lifestyle of Tetraselmis spp. Polinton-like viruses

2022

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In this study, we aimed at exploring horizontal gene transfer between viruses and Chlorodendraceae green algae (Chlorophyta) using available genomic and transcriptomic sequences for 20 algal strains. We identified a significant number of genes sharing a higher sequence similarity with viral homologues, thus signaling their possible involvement in HGTs with viruses. Further characterization showed that many of these genes were clustered in DNA regions of several tens to hundreds of kilobases in size, originally belonging to viruses related to known Tetraselmis spp. viruses (TetV and TsV). In contrast, the remaining candidate HGT genes were randomly dispersed in the algal genomes, more frequently transcribed and belonged to large multigene families. The presence of homologs in Viridiplantae suggested that these latter were more likely of algal rather than viral origin. We found a remarkable diversity Polinton-like virus (PLV) elements inserted in Tetraselmis genomes, all of which were most similar to the Tetrasemis striata virus TsV. The genes of PLV elements are transcriptionally inactive with the notable exception of the homologue of the TVSG_00024 gene of TsV whose function is unknown. We suggest that this gene may be involved in a sentinel process to trigger virus reactivation and excision in response to an environmental stimulus. Altogether, these results provide evidence that TsV-related viruses have a dual lifestyle, alternating between a free viral phase (i.e., virion) and a phase integrated into host genomes.

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A virophage cross-species infection through mutant selection represses giant virus propagation, promoting host cell survival

Cited by 18 publications

References 56 publications

Morphological and Taxonomic Properties of the Newly Isolated Cotonvirus japonicus , a New Lineage of the Subfamily Megavirinae

Morphological and Taxonomic Properties of the Newly Isolated Cotonvirus japonicus , a New Lineage of the Subfamily Megavirinae

Epigenetic influences of mobile genetic elements on ciliate genome architecture and evolution

Integrated viral elements suggest the dual lifestyle of Tetraselmis spp. Polinton-like viruses

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