Unorthodox features in two venerid bivalves with doubly uniparental inheritance of mitochondria

Charlotte Capt,Sophie Breton,Davide Guerra,Eric Pante,Brent M Robicheau,Donald T Stewart,Karim Bouvet

doi:10.1038/s41598-020-57975-y

Abstract

In animals, strictly maternal inheritance (SMI) of mitochondria is the rule, but one exception (doubly uniparental inheritance or DUI), marked by the transmission of sex-specific mitogenomes, has been reported in bivalves. Associated with DUI is a frequent modification of the mitochondrial cox2 gene, as well as additional sex-specific mitochondrial genes not involved in oxidative phosphorylation. With the exception of freshwater mussels (for 3 families of the order Unionida), these DUI-associated features have only been shown in few species [within Mytilidae (order Mytilida) and Veneridae (order Venerida)] because of the few complete sex-specific mitogenomes published for these orders. Here, we present the complete sex-specific mtDNAs of two recently-discovered DUI species in two families of the order Venerida, Scrobicularia plana (Semelidae) and Limecola balthica (Tellinidae). These species display the largest differences in genome size between sex-specific mitotypes in DUI species (>10 kb), as well as the highest mtDNA divergences (sometimes reaching >50%). An important in-frame insertion (>3.5 kb) in the male cox2 gene is partly responsible for the differences in genome size. The S. plana cox2 gene is the largest reported so far in the Kingdom Animalia. The mitogenomes may be carrying sex-specific genes, indicating that general mitochondrial features are shared among DUI species.

Highlights

In animals, strictly maternal inheritance (SMI) of mitochondria is the rule, but one exception, marked by the transmission of sex-specific mitogenomes, has been reported in bivalves
An even more extreme departure from the norm in bivalve mitochondrial genomes is their mode of doubly uniparental inheritance (DUI) — both egg and sperm mitochondria are transmitted from generation to generation in several bivalve species, but only male offspring retain paternally-transmitted mitochondria in their gametes[10,11,12]
16,170 bp and 17,492 bp in length, respectively, whereas the complete M mitochondrial DNA (mtDNA) are respectively 26,270 bp and 24,792 bp long (Fig. 1). These values represent the biggest differences in genome size between the F and M mtDNAs in species with DUI (Table 1), which usually do not exceed 2 kb. These differences in length are partly explained by the presence of an insertion in the protein-coding gene (PCG) cox[2] in the M mtDNA of both species (Fcox2 = 855 bp and Mcox2 = 4,815 bp in L. balthica, whereas Fcox2 = 861 bp and Mcox2 = 5,679 bp in S. plana) (Table 2), which is discussed in more details below

Summary

Introduction

Strictly maternal inheritance (SMI) of mitochondria is the rule, but one exception (doubly uniparental inheritance or DUI), marked by the transmission of sex-specific mitogenomes, has been reported in bivalves. Besides indicating that the newly sequenced mitogenomes may be carrying sex-specific genes like in other DUI species, our data reveal that the cox[2] gene in the M mitogenome of S. plana is the largest reported so far in the Kingdom Animalia. It remains to be demonstrated if such unorthodox features play key roles in DUI and sex determination in bivalves

Methods

Results

Conclusion