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Background  The 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.    Results  The  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.    Conclusions  The 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.

bmc evolutionary biology

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