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Pandoravirus celtis illustrates the microevolution processes at work in the giant Pandoraviridae genomes

View ORCID ProfileMatthieu Legendre, Jean-Marie Alempic, View ORCID ProfileNadège Philippe, View ORCID ProfileAudrey Lartigue, View ORCID ProfileSandra Jeudy, Olivier Poirot, Ngan Thi Ta, Sébastien Nin, View ORCID ProfileYohann Couté, View ORCID ProfileChantal Abergel, View ORCID ProfileJean-Michel Claverie
doi: https://doi.org/10.1101/500207
Matthieu Legendre
1Aix Marseille Univ, CNRS, IGS, Structural and Genomic Information Laboratory (UMR7256), Mediterranean Institute of Microbiology (FR3479), 163 Avenue de Luminy, F-13288 Marseille, France
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Jean-Marie Alempic
1Aix Marseille Univ, CNRS, IGS, Structural and Genomic Information Laboratory (UMR7256), Mediterranean Institute of Microbiology (FR3479), 163 Avenue de Luminy, F-13288 Marseille, France
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Nadège Philippe
1Aix Marseille Univ, CNRS, IGS, Structural and Genomic Information Laboratory (UMR7256), Mediterranean Institute of Microbiology (FR3479), 163 Avenue de Luminy, F-13288 Marseille, France
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Audrey Lartigue
1Aix Marseille Univ, CNRS, IGS, Structural and Genomic Information Laboratory (UMR7256), Mediterranean Institute of Microbiology (FR3479), 163 Avenue de Luminy, F-13288 Marseille, France
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Sandra Jeudy
1Aix Marseille Univ, CNRS, IGS, Structural and Genomic Information Laboratory (UMR7256), Mediterranean Institute of Microbiology (FR3479), 163 Avenue de Luminy, F-13288 Marseille, France
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Olivier Poirot
1Aix Marseille Univ, CNRS, IGS, Structural and Genomic Information Laboratory (UMR7256), Mediterranean Institute of Microbiology (FR3479), 163 Avenue de Luminy, F-13288 Marseille, France
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Ngan Thi Ta
1Aix Marseille Univ, CNRS, IGS, Structural and Genomic Information Laboratory (UMR7256), Mediterranean Institute of Microbiology (FR3479), 163 Avenue de Luminy, F-13288 Marseille, France
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Sébastien Nin
1Aix Marseille Univ, CNRS, IGS, Structural and Genomic Information Laboratory (UMR7256), Mediterranean Institute of Microbiology (FR3479), 163 Avenue de Luminy, F-13288 Marseille, France
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Yohann Couté
2Univ. Grenoble Alpes, CEA, Inserm, BIG-BGE, 38000 Grenoble, France.
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Chantal Abergel
1Aix Marseille Univ, CNRS, IGS, Structural and Genomic Information Laboratory (UMR7256), Mediterranean Institute of Microbiology (FR3479), 163 Avenue de Luminy, F-13288 Marseille, France
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  • For correspondence: jean-michel.claverie@univ-amu.fr chantal.abergel@igs.cnrs-mrs.fr
Jean-Michel Claverie
1Aix Marseille Univ, CNRS, IGS, Structural and Genomic Information Laboratory (UMR7256), Mediterranean Institute of Microbiology (FR3479), 163 Avenue de Luminy, F-13288 Marseille, France
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  • For correspondence: jean-michel.claverie@univ-amu.fr chantal.abergel@igs.cnrs-mrs.fr
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Abstract

With genomes of up to 2.7 Mb propagated in µm-long oblong particles and initially predicted to encode more than 2000 proteins, members of the Pandoraviridae family display the most extreme features of the known viral world. The mere existence of such giant viruses raises fundamental questions about their origin and the processes governing their evolution. A previous analysis of six newly available isolates, independently confirmed by a study including 3 others, established that the Pandoraviridae pan-genome is open, meaning that each new strain exhibits protein-coding genes not previously identified in other family members. With an average increment of about 60 proteins, the gene repertoire shows no sign of reaching a limit and remains largely coding for proteins without recognizable homologs in other viruses or cells (ORFans). To explain these results, we proposed that most new protein-coding genes were created de novo, from pre-existing non-coding regions of the G+C rich pandoravirus genomes. The comparison of the gene content of a new isolate, P. celtis, closely related (96% identical genome) to the previously described P. quercus is now used to test this hypothesis by studying genomic changes in a microevolution range. Our results confirm that the differences between these two similar gene contents mostly consist of protein-coding genes without known homologs (ORFans), with statistical signatures close to that of intergenic regions. These newborn proteins are under slight negative selection, perhaps to maintain stable folds and prevent protein aggregation pending the eventual emergence of fitness-increasing functions. Our study also unraveled several insertion events mediated by a transposase of the hAT family, 3 copies of which are found in P. celtis and are presumably active. Members of the Pandoraviridae are presently the first viruses known to encode this type of transposase.

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Posted February 11, 2019.
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Pandoravirus celtis illustrates the microevolution processes at work in the giant Pandoraviridae genomes
Matthieu Legendre, Jean-Marie Alempic, Nadège Philippe, Audrey Lartigue, Sandra Jeudy, Olivier Poirot, Ngan Thi Ta, Sébastien Nin, Yohann Couté, Chantal Abergel, Jean-Michel Claverie
bioRxiv 500207; doi: https://doi.org/10.1101/500207
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Pandoravirus celtis illustrates the microevolution processes at work in the giant Pandoraviridae genomes
Matthieu Legendre, Jean-Marie Alempic, Nadège Philippe, Audrey Lartigue, Sandra Jeudy, Olivier Poirot, Ngan Thi Ta, Sébastien Nin, Yohann Couté, Chantal Abergel, Jean-Michel Claverie
bioRxiv 500207; doi: https://doi.org/10.1101/500207

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