Pervasive Mitochondrial tRNA Gene Loss in Clade B of Haplosclerid Sponges (Porifera, Demospongiae)

Abstract

Mitochondrial tRNA gene loss and cytosolic tRNA import are two common phenomena in mitochondrial biology, but their importance is often under-appreciated in animals. This is because the mitochondrial DNA (mtDNA) of most bilaterally symmetrical animals (Bilateria) encodes a complete set of tRNAs required for mitochondrial translation. By contrast, the mtDNA of nonbilaterian animals (phyla Cnidaria, Ctenophora, Porifera, and Placozoa) often contains a reduced set of tRNA genes, necessitating tRNA import from the cytosol. Interestingly, in many nonbilaterian lineages, tRNA gene content appears to be set early in evolution and remains conserved thereafter. Here, we report that Clade B of haplosclerid sponges (CBHS) represents an exception to this pattern, displaying considerable variation in tRNA gene content even among relatively closely related species. We determined mt-genome sequences for eight CBHS species and analyzed them in conjunction with six previously available sequences. Additionally, we sequenced mt-genomes for two species of haplosclerid sponges outside the CBHS and used them with eight previously available sequences as outgroups. We found that tRNA gene content varied widely within CBHS, ranging from three in an undescribed Haliclona species (Haliclona sp. TLT785) to 25 in Xestospongia muta and X. testudinaria. Furthermore, we found that all CBHS species outside the genus Xestospongia lacked the atp9 gene, with some also lacking atp8. Analysis of nuclear sequences from Niphates digitalis revealed that both atp8 and atp9 had transferred to the nuclear genome, while the absence of mt-tRNA genes indicated their genuine loss. We argue that CBHS can serve as a valuable system for studying mt-tRNA gene loss, mitochondrial import of cytosolic tRNAs, and the impact of these processes on mitochondrial evolution.