Not Frozen in the Ice: Large and Dynamic Rearrangements in the Mitochondrial Genomes of the Antarctic Fish

• Published in: Genome Biology and Evolution
• Main Authors: Papetti, Chiara, Babbucci, Massimiliano, Dettai, Agnes, Basso, Andrea, Lucassen, Magnus, Harms, Lars, Bonillo, Celine, Heindler, Franz, Patarnello, Tomaso, Negrisolo, Enrico
• Other Authors: Universita degli Studi di Padova, Consorzio Nazionale Interuniversitario per le Scienze del Mare Rome, Italie (CoNISma), Institut de Systématique, Evolution, Biodiversité (ISYEB ), Muséum national d'Histoire naturelle (MNHN)-École pratique des hautes études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA), Alfred Wegener Institute for Polar and Marine Research (AWI), Helmholtz Institute for Functional Marine Biodiversity at the University of Oldenburg (HIFMB), Carl Von Ossietzky Universität Oldenburg, Acquisition et Analyse de Données pour l'Histoire naturelle (2AD), Muséum national d'Histoire naturelle (MNHN)-Centre National de la Recherche Scientifique (CNRS), Catholic University of Leuven - Katholieke Universiteit Leuven (KU Leuven)
• Format: Article in Journal/Newspaper
• Language: English
• Published: HAL CCSD 2021
• Subjects: Dissostichus; Trematomus; Notothenioidei; gene order rearrangements; icefish; mitochondrial genome evolution; [SDV]Life Sciences [q-bio]; Antarctic; The Antarctic; Antarc*; Icefish
• Online Access: https://hal.sorbonne-universite.fr/hal-03213305; https://hal.sorbonne-universite.fr/hal-03213305/document; https://hal.sorbonne-universite.fr/hal-03213305/file/evab017.pdf; https://doi.org/10.1093/gbe/evab017

International audience The vertebrate mitochondrial genomes generally present a typical gene order. Exceptions are uncommon and important to study the genetic mechanisms of gene order rearrangements and their consequences on phylogenetic output and mitochondrial function. Antarctic notothenioid fish carry some peculiar rearrangements of the mitochondrial gene order. In this first systematic study of 28 species, we analyzed known and undescribed mitochondrial genome rearrangements for a total of eight different gene orders within the notothenioid fish. Our reconstructions suggest that transpositions, duplications, and inversion of multiple genes are the most likely mechanisms of rearrangement in notothenioid mitochondrial genomes. In Trematominae, we documented an extremely rare inversion of a large genomic segment of 5,300 bp that partially affected the gene compositional bias but not the phylogenetic output. The genomic region delimited by nad5 and trnF, close to the area of the Control Region, was identified as the hot spot of variation in Antarctic fish mitochondrial genomes. Analyzing the sequence of several intergenic spacers and mapping the arrangements on a newly generated phylogeny showed that the entire history of the Antarctic notothenioids is characterized by multiple, relatively rapid, events of disruption of the gene order. We hypothesized that a pre-existing genomic flexibility of the ancestor of the Antarctic notothenioids may have generated a precondition for gene order rearrangement, and the pressure of purifying selection could have worked for a rapid restoration of the mitochondrial functionality and compactness after each event of rearrangement.