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Genome analysis of the first Marseilleviridae representative from Australia indicates that most of its genes contribute to virus fitness.
J Virol. 2014 Dec; 88(24):14340-9.JV

Abstract

The family Marseilleviridae consists of Acanthamoeba-infecting large DNA viruses with icosahedral particles ∼ 0.2 μm in diameter and genome sizes in the 346- to 380-kb range. Since the isolation of Marseillevirus from a cooling tower in Paris (France) in 2009, the family Marseilleviridae has expanded rapidly, with representatives from Europe and Africa. Five members have been fully sequenced that are distributed among 3 emerging Marseilleviridae lineages. One comprises Marseillevirus and Cannes 8 virus, another one includes Insectomime virus and Tunisvirus, and the third one corresponds to the more distant Lausannevirus. We now report the genomic characterization of Melbournevirus, the first representative of the Marseilleviridae isolated from a freshwater pond in Melbourne, Australia. Despite the large distance separating this sampling point from France, Melbournevirus is remarkably similar to Cannes 8 virus and Marseillevirus, with most orthologous genes exhibiting more than 98% identical nucleotide sequences. We took advantage of this optimal evolutionary distance to evaluate the selection pressure, expressed as the ratio of nonsynonymous to synonymous mutations for various categories of genes. This ratio was found to be less than 1 for all of them, including those shared solely by the closest Melbournevirus and Cannes 8 virus isolates and absent from Lausannevirus. This suggests that most of the 403 protein-coding genes composing the large Melbournevirus genome are under negative/purifying selection and must thus significantly contribute to virus fitness. This conclusion contrasts with the more common view that many of the genes of the usually more diverse large DNA viruses might be (almost) dispensable.

IMPORTANCE

A pervasive view is that viruses are fast-evolving parasites and carry the smallest possible amount of genomic information required to highjack the host cell machinery and perform their replication. This notion, probably inherited from the study of RNA viruses, is being gradually undermined by the discovery of DNA viruses with increasingly large gene content. These viruses also encode a variety of DNA repair functions, presumably slowing down their evolution by preserving their genomes from random alterations. On the other hand, these viruses also encode a majority of proteins without cellular homologs, including many shared only between the closest members of the same family. One may thus question the actual contribution of these anonymous and/or quasi-orphan genes to virus fitness. Genomic comparisons of Marseilleviridae, including a new Marseillevirus isolated in Australia, demonstrate that most of their genes, irrespective of their functions and conservation across families, are evolving under negative selection.

Authors+Show Affiliations

Structural and Genomic Information Laboratory, UMR 7256 (IMM FR 3479), CNRS Aix-Marseille Université, Luminy campus, Marseille, France.Structural and Genomic Information Laboratory, UMR 7256 (IMM FR 3479), CNRS Aix-Marseille Université, Luminy campus, Marseille, France.Structural and Genomic Information Laboratory, UMR 7256 (IMM FR 3479), CNRS Aix-Marseille Université, Luminy campus, Marseille, France chantal.abergel@igs.cnrs-mrs.fr jean-michel.claverie@univ-amu.fr.Structural and Genomic Information Laboratory, UMR 7256 (IMM FR 3479), CNRS Aix-Marseille Université, Luminy campus, Marseille, France Assistance Publique des Hopitaux de Marseille, La Timone, Marseille, France chantal.abergel@igs.cnrs-mrs.fr jean-michel.claverie@univ-amu.fr.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

25275139

Citation

Doutre, Gabriel, et al. "Genome Analysis of the First Marseilleviridae Representative From Australia Indicates That Most of Its Genes Contribute to Virus Fitness." Journal of Virology, vol. 88, no. 24, 2014, pp. 14340-9.
Doutre G, Philippe N, Abergel C, et al. Genome analysis of the first Marseilleviridae representative from Australia indicates that most of its genes contribute to virus fitness. J Virol. 2014;88(24):14340-9.
Doutre, G., Philippe, N., Abergel, C., & Claverie, J. M. (2014). Genome analysis of the first Marseilleviridae representative from Australia indicates that most of its genes contribute to virus fitness. Journal of Virology, 88(24), 14340-9. https://doi.org/10.1128/JVI.02414-14
Doutre G, et al. Genome Analysis of the First Marseilleviridae Representative From Australia Indicates That Most of Its Genes Contribute to Virus Fitness. J Virol. 2014;88(24):14340-9. PubMed PMID: 25275139.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Genome analysis of the first Marseilleviridae representative from Australia indicates that most of its genes contribute to virus fitness. AU - Doutre,Gabriel, AU - Philippe,Nadège, AU - Abergel,Chantal, AU - Claverie,Jean-Michel, Y1 - 2014/10/01/ PY - 2014/10/3/entrez PY - 2014/10/3/pubmed PY - 2015/1/22/medline SP - 14340 EP - 9 JF - Journal of virology JO - J. Virol. VL - 88 IS - 24 N2 - UNLABELLED: The family Marseilleviridae consists of Acanthamoeba-infecting large DNA viruses with icosahedral particles ∼ 0.2 μm in diameter and genome sizes in the 346- to 380-kb range. Since the isolation of Marseillevirus from a cooling tower in Paris (France) in 2009, the family Marseilleviridae has expanded rapidly, with representatives from Europe and Africa. Five members have been fully sequenced that are distributed among 3 emerging Marseilleviridae lineages. One comprises Marseillevirus and Cannes 8 virus, another one includes Insectomime virus and Tunisvirus, and the third one corresponds to the more distant Lausannevirus. We now report the genomic characterization of Melbournevirus, the first representative of the Marseilleviridae isolated from a freshwater pond in Melbourne, Australia. Despite the large distance separating this sampling point from France, Melbournevirus is remarkably similar to Cannes 8 virus and Marseillevirus, with most orthologous genes exhibiting more than 98% identical nucleotide sequences. We took advantage of this optimal evolutionary distance to evaluate the selection pressure, expressed as the ratio of nonsynonymous to synonymous mutations for various categories of genes. This ratio was found to be less than 1 for all of them, including those shared solely by the closest Melbournevirus and Cannes 8 virus isolates and absent from Lausannevirus. This suggests that most of the 403 protein-coding genes composing the large Melbournevirus genome are under negative/purifying selection and must thus significantly contribute to virus fitness. This conclusion contrasts with the more common view that many of the genes of the usually more diverse large DNA viruses might be (almost) dispensable. IMPORTANCE: A pervasive view is that viruses are fast-evolving parasites and carry the smallest possible amount of genomic information required to highjack the host cell machinery and perform their replication. This notion, probably inherited from the study of RNA viruses, is being gradually undermined by the discovery of DNA viruses with increasingly large gene content. These viruses also encode a variety of DNA repair functions, presumably slowing down their evolution by preserving their genomes from random alterations. On the other hand, these viruses also encode a majority of proteins without cellular homologs, including many shared only between the closest members of the same family. One may thus question the actual contribution of these anonymous and/or quasi-orphan genes to virus fitness. Genomic comparisons of Marseilleviridae, including a new Marseillevirus isolated in Australia, demonstrate that most of their genes, irrespective of their functions and conservation across families, are evolving under negative selection. SN - 1098-5514 UR - https://www.unboundmedicine.com/medline/citation/25275139/Genome_analysis_of_the_first_Marseilleviridae_representative_from_Australia_indicates_that_most_of_its_genes_contribute_to_virus_fitness_ L2 - http://jvi.asm.org/cgi/pmidlookup?view=long&pmid=25275139 DB - PRIME DP - Unbound Medicine ER -