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

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.

An Unusual Evolutionary Strategy: The Origins, Genetic Repertoire, and Implications of Doubly Uniparental Inheritance of Mitochondrial DNA in Bivalves

“…This insertion is absent in the Fcox2 gene of both species. In S. plana, this in-frame insertion, if translated, means that the Mcox2 gene would be 5,679bp-long and, to our knowledge, would therefore encode for the longest COX2 protein in the animal kingdom (i.e., 1,893 amino acids) (Capt et al 2020).…”

“…Their complete mtDNAs have been published, revealing an intriguing difference of ~10 kb between the F and M mt genomes in both species (Capt et al 2020). A large part of this difference is due to the exceptionally large size of the Mcox2 gene, which possesses a >4.5kb and >3.5kb insertion in S. plana and L. balthica, respectively.…”

“…Quite differently, the Mcox2 gene in L. balthica is split in two by the insertion, which divides the gene into Mcox2a, encoding the two transmembrane helices and the "heme-patch" region followed by a complete stop codon (TAA), and Mcox2b, encoding an enlarged intermembrane space and the Cua centers (Capt et al 2020). This situation is confirmed by transcriptomic data (Pante et al unpublished), which indicate that both regions are transcribed That said, a similar case has been described in another bivalve species, i.e.…”

“…The strict sex-specific mtDNA segregation in DUI germline cause different selective pressures to act on the two mtDNA F & M variants, leading them to evolve distinctly for female and male functions. Sexually antagonist selection is also supported by the extreme divergence between the F-and the M-mtDNA, ranging from 8-50% of nucleotide divergence, depending on the gene and species involved (Breton et al 2007;Passamonti and Ghiselli 2009;Zouros 2013;Capt et al 2020). Given the exclusive presence of the M-type mtDNA in DUI sperm, and that mutations in the mtDNA are likely to affect the functioning of mitochondrial respiration, a rational indication is that the evolution of DUI male mitochondria could embrace bioenergetic adaptations for male-associated functions, fostering sperm performance and reproductive success (Burt and Trivers 2006;Breton et al 2007;Breton et al 2009b).…”

The complete mitogenome of the inarticulate brachiopod Glottidia pyramidata reveals insights into gene order variation, deviant ATP8 and mtORFans in the Brachiopoda

“…As for DUI bivalves (e.g. Breton et al 2010 , 2011a , 2011b , 2014 ; Milani et al 2013 ; Lubośny et al 2018 ; Guerra et al 2019 ; Capt et al 2020 ), brachiopods present important variation in mtDNA size (17 to >28 kb) and gene arrangement, with longer and deviant protein-coding sequences compared to their homologues in other animals (e.g. longer cox2 gene and deviant ATP8 protein sequences) as well as supernumerary open reading frames (ORFs) or mtORFans (ORFs without recognizable homologies to other known genes) (Helfenbein et al 2001 ; Endo et al 2005 ; Luo et al 2015 ; Karagozlu et al 2017a ).…”