Pithoviruses Are Invaded by Repeats That Contribute to Their Evolution and Divergence from Cedratviruses

• Published in: Molecular Biology and Evolution
• Main Authors: Rigou, Sofia, Schmitt, Alain, Alempic, Jean-Marie, Lartigue, Audrey, Vendloczki, Peter, Abergel, Chantal, Claverie, Jean-Michel, Legendre, Matthieu
• Other Authors: Hepp, Crystal, Agence Nationale de la Recherche, CNRS Projet de Recherche Conjoint
• Format: Article in Journal/Newspaper
• Language: English
• Published: Oxford University Press (OUP) 2023
• Subjects: permafrost
• Online Access: http://dx.doi.org/10.1093/molbev/msad244; https://academic.oup.com/mbe/advance-article-pdf/doi/10.1093/molbev/msad244/53253432/msad244.pdf; https://academic.oup.com/mbe/article-pdf/40/11/msad244/53676949/msad244.pdf

Abstract Pithoviridae are amoeba-infecting giant viruses possessing the largest viral particles known so far. Since the discovery of Pithovirus sibericum, recovered from a 30,000-yr-old permafrost sample, other pithoviruses, and related cedratviruses, were isolated from various terrestrial and aquatic samples. Here, we report the isolation and genome sequencing of 2 Pithoviridae from soil samples, in addition to 3 other recent isolates. Using the 12 available genome sequences, we conducted a thorough comparative genomic study of the Pithoviridae family to decipher the organization and evolution of their genomes. Our study reveals a nonuniform genome organization in 2 main regions: 1 concentrating core genes and another gene duplications. We also found that Pithoviridae genomes are more conservative than other families of giant viruses, with a low and stable proportion (5% to 7%) of genes originating from horizontal transfers. Genome size variation within the family is mainly due to variations in gene duplication rates (from 14% to 28%) and massive invasion by inverted repeats. While these repeated elements are absent from cedratviruses, repeat-rich regions cover as much as a quarter of the pithoviruses genomes. These regions, identified using a dedicated pipeline, are hotspots of mutations, gene capture events, and genomic rearrangements that contribute to their evolution.