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

Chiara Papetti,Andrea Basso,Franz Maximilian Heindler,Lars Harms,Agnes Dettai,Celine Bonillo,Massimiliano Babbucci,Enrico Negrisolo,Tomaso Patarnello,Magnus Lucassen

doi:10.1093/gbe/evab017

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 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.

Highlights

The Bilaterian mitochondrial genome is usually a double-strand circular DNA molecule spanning 15– 20 kb (Boore 1999)
Our study found that more gene order rearrangements than previously known have occurred during the entire history of the Antarctic notothenioid species by multiple events of transposition, duplication, and inversion of several genes
The mitogenomes of few cryonotothenioids have been available for years, fundamental questions remain unaddressed about 1) the extent of the gene orders (GO) variability within the whole Antarctic clade, 2) the mechanisms and 3) the evolutionary pathways that led to the mitochondrial structural diversity, 4) the different contribute of drift and selection in shaping the GO diversity, and 5) the consequences of gene order rearrangements on phylogenetic output and mitochondrial function in the Notothenioidei. To address these questions about the Antarctic notothenioid mitogenomic evolution, we investigated the origins and steps resulting in the observed gene rearrangements by 1) expanding the sampling to 15 complete and two nearly complete new mitogenomes of notothenioids, 2) determining the structure of the rearranged regions for each GO, 3) analyzing the position and content of all available GR-intergenic spacers (ISPs), 4) assessing the type of selection acting on mitochondrial genes, the compositional bias, and the homogeneity of the substitution pattern, 5) tracing the evolution of each GO on an inferred species phylogeny, and 6) investigating the impact of the GO rearrangements on the phylogenetic output

Summary

Introduction

The Bilaterian mitochondrial genome (hereafter mitogenome) is usually a double-strand circular DNA molecule spanning 15– 20 kb (Boore 1999). Among the 11 mitogenomes (2 partial and 9 complete, see supplementary table S2, Supplementary Material online) available at the time of this study, six different GO were already known for Notothenioidei These preliminary data showed that all early-diverged species carried the VertGO arrangement, whereas extensive gene order rearrangements characterized the Antarctic family (Nototheniidae, Zhuang and Cheng 2010) suggesting that all rearrangements and the radiation in the newly formed polar environment occurred coincidentally. Our results posit new avenues of research to test our preliminary speculations about the adaptive or nonadaptive nature of the extensive rearrangements and the consequences on mitochondrial function

Materials and Methods

Results and Discussion

A Multigene Phylogeny for the Suborder Notothenioidei

Literature Cited