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Mitochondrial DNA of the coral sarcophyton glaucum contains a gene for a homologue of bacterial muts: A possible case of gene transfer from the nucleus to the mitochondrion

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Abstract

The nucleotide sequences of two segments of 6,737 ntp and 258 ntp of the 18.4-kb circular mitochondrial (mt) DNA molecule of the soft coral Sarcophyton glaucum (phylum Cnidaria, class Anthozoa, subclass Octocorallia, order Alcyonacea) have been determined. The larger segment contains the 3′ 191 ntp of the gene for subunit 1 of the respiratory chain NADH dehydrogenase (ND1), complete genes for cytochrome b (Cyt b), ND6, ND3, ND4L, and a bacterial MutS homologue (MSH), and the 5’ terminal 1,124 ntp of the gene for the large subunit rRNA (1-rRNA). These genes are arranged in the order given and all are transcribed from the same strand of the molecule. The smaller segment contains the 3′ terminal 134 ntp of the ND4 gene and a complete tRNAf-Met gene, and these genes are transcribed in opposite directions. As in the hexacorallian anthozoan, Metridium senile, the mt-genetic code of S. glaucum is near standard: that is, in contrast to the situation in mt-genetic codes of other invertebrate phyla, AGA and AGG specify arginine, and ATA specifies isoleucine. However, as appears to be universal for metazoan mt-genetic codes, TGA specifies tryptophan rather than termination. Also, as in M. senile the mt-tRNAf-Met gene has primary and secondary structural features resembling those of Escherichia coli initiator tRNA, including standard dihydrouridine and Tv(iC loop sequences, and a mismatched nucleotide pair at the top of the amino-acyl stem. The presence of a mutS gene homologue, which has not been reported to occur in any other known mtDNA, suggests that there is mismatch repair activity in S. glaucum mitochondria. In support of this, phylogenetic analysis of MutS family protein sequences indicates that the S. glaucum mtMSH protein is more closely related to the nuclear DNA-encoded mitochondrial mismatch repair protein (MSH1) of the yeast Saccharomyces cerevisiae than to eukaryotic homologues involved in nuclear function, or to bacterial homologues. Regarding the possible origin of the S. glaucum mtMSH gene, the phylogenetic analysis results, together with comparative base composition considerations, and the absence of an MSH gene in any other known mtDNA best support the hypothesis that S. glaucum mtDNA acquired the mtMSH gene from nuclear DNA early in the evolution of octocorals. The presence of mismatch repair activity in S. glaucum mitochondria might be expected to influence the rate of evolution of this organism’s mtDNA.

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  1. Geneviàve Pont-Kingdon

    Present address: Huntsman Cancer Institute, University of Utah, 84112, Salt Lake City, Utah, USA

  2. Cristi D. Watkins-Sims

    Present address: Department of Human Genetics, University of Utah, 84112, Salt Lake City, Utah, USA

  3. Thomas Cavalier-Smith

    Present address: Department of Botany, University of British Columbia, V6T 1Z4, Vancouver, British Columbia, Canada

Authors and Affiliations

  1. Department of Biology, University of Utah, 84112, Salt Lake City, Utah, USA

    Geneviàve Pont-Kingdon, Norichika A. Okada, Jane L. Macfarlane, C. Timothy Beagley, Cristi D. Watkins-Sims & David R. Wolstenholme

  2. Research School of Biological Sciences, Australian National University, ACT 2601, Canberra, Australia

    Thomas Cavalier-Smith & G. Desmond Clark-Walker

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  1. Geneviàve Pont-Kingdon
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Pont-Kingdon, G., Okada, N.A., Macfarlane, J.L. et al. Mitochondrial DNA of the coral sarcophyton glaucum contains a gene for a homologue of bacterial muts: A possible case of gene transfer from the nucleus to the mitochondrion. J Mol Evol 46, 419–431 (1998). https://doi.org/10.1007/PL00006321

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