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

Abstract

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 analysed 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 5300 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. Analysing 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 hypothesised 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.

Positive and relaxed selective pressures have both strongly influenced the evolution of cryonotothenioid fishes during their radiation in the freezing Southern Ocean

“…This change in selective pressure was detected in several components of the electron transport chain itself (SDHA, QCR1, NDUA8, COX41), amid signatures of relaxed selective pressure on other genes related to mitochondrial function detected under other GO terms (COA7, NDUA8, PRLD1). Similar results were obtained in a previous study for mitochondrially-coded genes for which a prevalence of relaxation of the selective pressure in comparison with the non-Antarctic notothenioids was detected (in particular for COX3, COB, NAD2, NAD4, and NAD6; Papetti et al, 2021). While this may be a result of increased oxygen saturation in cold Antarctic waters, this trend towards relaxation of selective pressure may also be a result of the reduction in resilience to thermal variability in these systems as suggested in prior work (Mark et al, 2012) and may have persistently influenced the inception of the evolution of cryonotothenioids.…”

A Unique Mitochondrial Gene Block Inversion in Antarctic Trematomin Fishes: A Cautionary Tale

“…The phylogenetic relationships of the notothenioids have been studied for more than 2 decades. Recently, the phylogeny of this group has been reanalyzed and updated using a combination of mitochondrial (mt) and nuclear DNA markers, including 15 new complete and 2 partial mt genomes ( Papetti et al 2021 ). The study identified a number of novel rearrangements in the mt genomes, including an extremely rare inversion event in the Trematominae.…”

“…The study identified a number of novel rearrangements in the mt genomes, including an extremely rare inversion event in the Trematominae. Papetti et al (2021) generated a new phylogeny which showed that the mt evolution of the notothenioids has been characterized by multiple, relatively rapid changes in mt gene order.…”

“…In fact, in the 5 Antarctic notothenioid families studied, these 2 genes were not lost but simply translocated from their canonical location between the NADH dehydrogenase subunit 5 ( ND5 ) and cytochrome b ( Cytb ) genes to the CR, and subsequently overlooked ( Zhuang and Cheng 2010 ). Papetti et al (2021) have recently shown that whole mt genomes of Antarctic notothenioids vary greatly with respect to gene order. Their study was the first to report novel gene orders from representative species of all Nototheniidae families, including the trematomins.…”

Toll-Like Receptor Evolution: Does Temperature Matter?

“…The exception was N. rossii where an “in house” de novo multi-tissue transcriptome assembly was used. The figure was drawn considering the relative evolutionary relationship between the six Antarctic fish species and the sub-Antarctic fish ( 35 , 64 ). Gene/transcript accession numbers are available in Supplementary Table 1 .…”