A unique horizontal gene transfer event has provided the octocoral mitochondrial genome with an active mismatch repair gene that has potential for an unusual self-contained function

Abstract

BackgroundThe mitochondrial genome of the Octocorallia has several characteristics atypical for metazoans, including a novel gene suggested to function in DNA repair. This mtMutS gene is favored for octocoral molecular systematics, due to its high information content. Several hypotheses concerning the origins of mtMutS have been proposed, and remain equivocal, although current weight of support is for a horizontal gene transfer from either an epsilonproteobacterium or a large DNA virus. Here we present new and compelling evidence on the evolutionary origin of mtMutS, and provide the very first data on its activity, functional capacity and stability within the octocoral mitochondrial genome.ResultsThe mtMutS gene has the expected conserved amino acids, protein domains and predicted tertiary protein structure. Phylogenetic analysis indicates that mtMutS is not a member of the MSH family and therefore not of eukaryotic origin. MtMutS clusters closely with representatives of the MutS7 lineage; further support for this relationship derives from the sharing of a C-terminal endonuclease domain that confers a self-contained mismatch repair function. Gene expression analyses confirm that mtMutS is actively transcribed in octocorals. Rates of mitochondrial gene evolution in mtMutS-containing octocorals are lower than in their hexacoral sister-group, which lacks the gene, although paradoxically the mtMutS gene itself has higher rates of mutation than other octocoral mitochondrial genes.ConclusionsThe octocoral mtMutS gene is active and codes for a protein with all the necessary components for DNA mismatch repair. A lower rate of mitochondrial evolution, and the presence of a nicking endonuclease domain, both indirectly support a theory of self-sufficient DNA mismatch repair within the octocoral mitochondrion. The ancestral affinity of mtMutS to non-eukaryotic MutS7 provides compelling support for an origin by horizontal gene transfer. The immediate vector of transmission into octocorals can be attributed to either an epsilonproteobacterium in an endosymbiotic association or to a viral infection, although DNA viruses are not currently known to infect both bacteria and eukaryotes, nor mitochondria in particular. In consolidating the first known case of HGT into an animal mitochondrial genome, these findings suggest the need for reconsideration of the means by which metazoan mitochondrial genomes evolve.

Genetic aspects of mitochondrial genome evolution

“…In octocoral mitogenomes an additional msh1 gene is found (McFadden et al, 2006, and references therein). It has recently been identified as a compelling candidate for horizontal gene transfer and appears to have a function in DNA repair (Bilewitch and Degnan, 2011).…”

Horizontal gene transfer in the acquisition of novel traits by metazoans

“…The acquisition by the starlet sea anemone, Nematostella vectensis, of bacterial genes involved in the shikimic acid [14] and glyoxilate pathways [15] has been proposed from bioinformatics studies performed on the Nematostella genome. In addition, an interesting gene encoding a protein with mismatch repair activity has been postulated to be targeted to octocorals mitochondrial DNA [16], however, the gene donor or the relevance of gene function remains unknown.…”

Evolutionary and ecological genomics in deep-sea organisms

“…A confounding factor when analyzing mitochondrial DNA markers is the fact that anthozoans, including octocorals, have slow rates of sequence evolution relative to other metazoans (Shearer et al 2002;Hellberg 2006). Furthermore, octocoral mitochondrion is unique among eukaryotes by having a functional DNA mismatch repair gene -mtMutS -which presumably is responsible for the extremely low sequence variability observed in this group (Bilewitch & Degnan 2011). Traditional molecular markers have thus been remarkably insufficient to resolve relationships at all taxonomic levels within the octocorals (Berntson et al 2001;France et al 2002;Mcfadden et al 2004;Smith et al 2004;Thoma et al 2009;Dueñas et al 2014).…”