The complete mitochondrial genome of the hermaphroditic freshwater mussel Anodonta cygnea (Bivalvia: Unionidae): in silico analyses of sex-specific ORFs across order Unionoida

E E Chase,S Veinot,S Breton,D T Stewart,B M Robicheau

doi:10.1186/s12864-018-4583-3

E E Chase, S Veinot + Show 3 more

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https://doi.org/10.1186/s12864-018-4583-3

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Abstract

BackgroundDoubly uniparental inheritance (DUI) of mitochondrial DNA in bivalves is a fascinating exception to strictly maternal inheritance as practiced by all other animals. Recent work on DUI suggests that there may be unique regions of the mitochondrial genomes that play a role in sex determination and/or sexual development in freshwater mussels (order Unionoida). In this study, one complete mitochondrial genome of the hermaphroditic swan mussel, Anodonta cygnea, is sequenced and compared to the complete mitochondrial genome of the gonochoric duck mussel, Anodonta anatina. An in silico assessment of novel proteins found within freshwater bivalve species (known as F-, H-, and M-open reading frames or ORFs) is conducted, with special attention to putative transmembrane domains (TMs), signal peptides (SPs), signal cleavage sites (SCS), subcellular localization, and potential control regions. Characteristics of TMs are also examined across freshwater mussel lineages.ResultsIn silico analyses suggests the presence of SPs and SCSs and provides some insight into possible function(s) of these novel ORFs. The assessed confidence in these structures and functions was highly variable, possibly due to the novelty of these proteins. The number and topology of putative TMs appear to be maintained among both F- and H-ORFs, however, this is not the case for M-ORFs. There does not appear to be a typical control region in H-type mitochondrial DNA, especially given the loss of tandem repeats in unassigned regions when compared to F-type mtDNA.ConclusionIn silico analyses provides a useful tool to discover patterns in DUI and to navigate further in situ analyses related to DUI in freshwater mussels. In situ analysis will be necessary to further explore the intracellular localizations and possible role of these open reading frames in the process of sex determination in freshwater mussel.

Highlights

Uniparental inheritance (DUI) of mitochondrial DNA in bivalves is a fascinating exception to strictly maternal inheritance as practiced by all other animals
Previous research has investigated the presence of transmembrane domains (TMs) and signal peptides (SPs) in these sex-specific open reading frames (ORFs); we extend these studies with the inclusion of additional freshwater mussels (FWM) taxa and additional analyses to investigate the specific presence of signal cleavage sites (SCSs) and the topology of putative TMs
General features of the mitochondrial DNA (mtDNA) of the hermaphroditic swan mussel, Anodonta cygnea The mtDNA of Anodonta cygnea contains the 13 proteincoding genes, and the two rRNA and 22 tRNA genes typically found in FWM mtDNAs (Fig. 1) and other animal mtDNAs [53]

Summary

Introduction

Uniparental inheritance (DUI) of mitochondrial DNA in bivalves is a fascinating exception to strictly maternal inheritance as practiced by all other animals. Many gonochoric FWMs (i.e. species with separate male and female sexes), along with a few other bivalve orders (i.e. Mytiloid marine mussels, Nuculanoid nut shells, and Veneroid marine clams), do not exhibit strictly maternal inheritance of mitochondrial DNA (mtDNA) like all other animal species [2] These bivalves transmit mtDNA via an unusual system called doubly uniparental inheritance or DUI (for reviews see [3,4,5]). The respective M-type and F-type mtDNAs are unusual, in contrast to typical animal mtDNA gene content, as each of the sexassociated mitochondrial genomes contains their own novel open reading frames (ORFs; [10]) These genes are referred to as the m-orf and f-orf in the male and female mitochondrial genomes, respectively, and these two regions code for proteins that do not show significant similarity to each other or obvious homology to any other known proteins ([10]; and see [11, 12] who suggested that a duplicated and diverged atp gene evolved into the m-orf gene in freshwater mussels). These molecular structures or signals may be key components of the pathway and/or mechanisms used to export these novel mitochondrial proteins to the nucleus where they could play a role in sex determination

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