Pervasive mitochondrial tRNA gene loss in the clade B of haplosclerid sponges (Porifera, Demospongiae)

Abstract

AbstractMitochondrial tRNA gene loss and cytosolic tRNA import to mitochondria are two common phenomena in mitochondrial biology, but their importance is often under-appreciated in animals. This is because most bilaterally symmetrical animals (Bilateria) encode a complete set of tRNAs needed for mitochondrial translation. By contrast, studies of mitochondrial genomes in non-bilaterian animals have shown a reduced tRNA gene content in several lineages, necessitating tRNA import. Interestingly, in most of these lineages tRNA gene content appears to be set early in the evolution of the group and conserved thereafter. Here we demonstrate that Clade B of Haplosclerid Sponges (CBHS) represent an exception to this pattern. We determined mt-genome sequences for eight species from this group and analyzed them with six that had been previously available. In addition, we determined mt-genome sequences for two species of haploslerid sponges outside the CBHS and used them with eight previously available sequences as outgroups. We found that tRNA gene content varied widely among CBHS species: from three in an undescribedHaliclonaspecies (Haliclona sp. TLT785) to 25 inXestospongia mutaandX. testudinaria. Furthermore, we found that all CBHS species outside the genusXestospongialackedatp9, while some also lackedatp8. Analysis of nuclear sequences fromNiphates digitalisrevealed that bothatp8andatp9had transferred to the nuclear genome, while the absence of mt-tRNA genes represented their genuine loss. Overall, CBHS can be a useful animal system to study mt-tRNA genes loss, mitochondrial import of cytosolic tRNA, and the impact of both of these processes on mitochondrial evolution.Significance statementIt is generally believed that the gene content is stable in animal mitochondrial (mt) DNA. Indeed, mtDNA in most bilaterally symmetrical animals encompasses a conserved set of 37 genes coding for 13 proteins, two rRNAs and 22 tRNAs. By contrast, mtDNA in non-bilaterian animals shows more variation in mt gene content, in particular in the number of tRNA genes. However, most of this variation occurs between major non-bilaterian lineages. Here we demonstrate that a group of demosponges called Clade B of Haplosclerid Sponges (CBHS) represents a fascinating exception to this pattern, with species experiencing recurrent losses of up to 22 mt-tRNA genes. We argue that this group constitutes a promising system to investigate the effects of tRNA gene loss on evolution of mt-genomes as well as mitochondrial tRNA import machinery.