Presence of male mitochondria in somatic tissues and their functional importance at the whole animal level in the marine bivalve Arctica islandica

Cyril Dégletagne,Doris Abele,Christoph Held,Heike Gruber,Benjamin Alric,Gernot Glöckner

doi:10.1038/s42003-021-02593-1

Abstract

Metazoans normally possess a single lineage of mitochondria inherited from the mother (♀-type mitochondria) while paternal mitochondria are absent or eliminated in fertilized eggs. In doubly uniparental inheritance (DUI), which is specific to the bivalve clade including the ocean quahog, Arctica islandica, ♂-type mitochondria are retained in male gonads and, in a few species, small proportions of ♂-type mitochondria co-exist with ♀-type in somatic tissues. To the best of our knowledge, we report, for the first time in metazoan, the natural occurrence of male and female individuals with exclusively ♂-type mitochondria in somatic tissues of the bivalve A. islandica. Mitochondrial genomes differ by ~5.5% at DNA sequence level. Exclusive presence of ♂-type mitochondria affects mitochondrial complexes partially encoded by mitochondrial genes and leads to a sharp drop in respiratory capacity. Through a combination of whole mitochondrial genome sequencing and molecular assays (gene presence and expression), we demonstrate that 1) 11% of individuals of an Icelandic population appear homoplasmic for ♂-type mitochondria in somatic tissues, 2) ♂-type mitochondrial genes are transcribed and 3) individuals with ♂-type mitochondria in somatic cells lose 30% of their wild-type respiratory capacity. This mitochondrial pattern in A. islandica is a special case of DUI, highlighted in individuals from both sexes with functional consequences at cellular and conceivably whole animal level.

Highlights

Metazoans normally possess a single lineage of mitochondria inherited from the mother (♀-type mitochondria) while paternal mitochondria are absent or eliminated in fertilized eggs
The phylogenetic analysis of all concatenated protein sequences encoded in the ♂and ♀-type mitochondrial genomes, respectively, show that the two mitochondrial genomes are reciprocally monophyletic and each other’s closest relative, indicating that divergence emerged within the stem lineage leading to A. islandica itself (Fig. 1)
Uniparental inheritance of mitochondrial lineages (DUI) occurs in the bivalve order Unionida, in which the split of the mitochondrial genomes occurred at the base of the higher taxon

Summary

Introduction

Metazoans normally possess a single lineage of mitochondria inherited from the mother (♀-type mitochondria) while paternal mitochondria are absent or eliminated in fertilized eggs. Through a combination of whole mitochondrial genome sequencing and molecular assays (gene presence and expression), we demonstrate that 1) 11% of individuals of an Icelandic population appear homoplasmic for ♂-type mitochondria in somatic tissues, 2) ♂-type mitochondrial genes are transcribed and 3) individuals with ♂-type mitochondria in somatic cells lose 30% of their wild-type respiratory capacity This mitochondrial pattern in A. islandica is a special case of DUI, highlighted in individuals from both sexes with functional consequences at cellular and conceivably whole animal level. Several processes contribute to mtDNA sequence conservation: (1) negative selection against mtDNA variants (mitotypes)[5]; (2) reduction of the number of mtDNA copies per cell during early embryogenesis[9]; and (3) the non-Mendelian inheritance of mitochondria exclusively through the oocyte (♀-type) but not the sperm These mechanisms reduce the risk of mitonuclear genomic incompatibilities and the propagation of cytoplasmic selfish elements[9,10,11]. In DUI species, the reported differentiation between the two mitochondrial lineages ranges from 20% in many marine taxa

Methods

Results

Conclusion