Variability of mitochondrial ORFans hints at possible differences in the system of doubly uniparental inheritance of mitochondria among families of freshwater mussels (Bivalvia: Unionida)

Davide Guerra,Arthur E Bogan,Elsa Froufe,Paz Ondina,Donald T Stewart,Manuel Lopes-Lima,Michael W Klunzinger,Rafaela Amaro,Vincent Prié,Claudia Callil,Sophie Breton,Han Ming Gan

doi:10.1186/s12862-019-1554-5

Abstract

BackgroundSupernumerary ORFan genes (i.e., open reading frames without obvious homology to other genes) are present in the mitochondrial genomes of gonochoric freshwater mussels (Bivalvia: Unionida) showing doubly uniparental inheritance (DUI) of mitochondria. DUI is a system in which distinct female-transmitted and male-transmitted mitotypes coexist in a single species. In families Unionidae and Margaritiferidae, the transition from dioecy to hermaphroditism and the loss of DUI appear to be linked, and this event seems to affect the integrity of the ORFan genes. These observations led to the hypothesis that the ORFans have a role in DUI and/or sex determination. Complete mitochondrial genome sequences are however scarce for most families of freshwater mussels, therefore hindering a clear localization of DUI in the various lineages and a comprehensive understanding of the influence of the ORFans on DUI and sexual systems. Therefore, we sequenced and characterized eleven new mitogenomes from poorly sampled freshwater mussel families to gather information on the evolution and variability of the ORFan genes and their protein products.ResultsWe obtained ten complete plus one almost complete mitogenome sequence from ten representative species (gonochoric and hermaphroditic) of families Margaritiferidae, Hyriidae, Mulleriidae, and Iridinidae. ORFan genes are present only in DUI species from Margaritiferidae and Hyriidae, while non-DUI species from Hyriidae, Iridinidae, and Mulleriidae lack them completely, independently of their sexual system. Comparisons among the proteins translated from the newly characterized ORFans and already known ones provide evidence of conserved structures, as well as family-specific features.ConclusionsThe ORFan proteins show a comparable organization of secondary structures among different families of freshwater mussels, which supports a conserved physiological role, but also have distinctive family-specific features. Given this latter observation and the fact that the ORFans can be either highly mutated or completely absent in species that secondarily lost DUI depending on their respective family, we hypothesize that some aspects of the connection among ORFans, sexual systems, and DUI may differ in the various lineages of unionids.

Highlights

Supernumerary ORFan genes are present in the mitochondrial genomes of gonochoric freshwater mussels (Bivalvia: Unionida) showing doubly uniparental inheritance (DUI) of mitochondria
As is typical for DUI freshwater mussels, the cox2 gene carried by W. carteri M mt genome is longer compared to its F counterpart and to those of non-DUI species [6] (Table 3)
Apart from the occasional species-specific difference in length of some noncoding regions, in Hyriidae and Iridinidae (1049 bp between nad5 and trnF in C. rubens, compared to the 23-76 bp of the other species Mitochondrial DNA (mtDNA)), the most notable features lie in the presence/absence of ORFans, on which we will focus

Summary

Introduction

Supernumerary ORFan genes (i.e., open reading frames without obvious homology to other genes) are present in the mitochondrial genomes of gonochoric freshwater mussels (Bivalvia: Unionida) showing doubly uniparental inheritance (DUI) of mitochondria. In families Unionidae and Margaritiferidae, the transition from dioecy to hermaphroditism and the loss of DUI appear to be linked, and this event seems to affect the integrity of the ORFan genes. These observations led to the hypothesis that the ORFans have a role in DUI and/or sex determination. DUI seems to be strictly associated with the gonochoristic sexual system of a particular species, as it was discovered that four species of unionids and one species of margaritiferid each appear to have lost independently their M mtDNA during the transition from dioecy to hermaphroditism [3] Notice that, it is not known if the loss of the M type is perfectly contemporaneous with the switch to hermaphroditism. In absence of further functional studies, this leads us to hypothesize that the primary function of these genes, if they retain functionality, might be related to oxidative phosphorylation

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