title: Eight new mtDNA sequences of glass sponges reveal an extensive usage of +1 frameshifting in mitochondrial translation.
abstract: Three previously studied mitochondrial genomes of glass sponges (phylum Porifera, class Hexactinellida) contained single nucleotide insertions in protein coding genes inferred as sites of +1 translational frameshifting. To investigate the distribution and evolution of these sites and to help elucidate the mechanism of frameshifting, we determined eight new complete or nearly complete mtDNA sequences from glass sponges and examined individual mitochondrial genes from three others. We found nine new instances of single nucleotide insertions in these sequences and analyzed them both comparatively and phylogenetically. The base insertions appear to have been gained and lost repeatedly in hexactinellid mt protein genes, suggesting no functional significance for the frameshifting sites. A high degree of sequence conservation, the presence of unusual tRNAs, and a distinct pattern of codon usage suggest the "out-of-frame pairing" model of translational frameshifting. Additionally, we provide evidence that relaxed selection pressure on glass sponge mtDNA - possibly a result of their low growth rates and deep-water lifestyle - has allowed frameshift insertions to be tolerated for hundreds of millions of years. Our study provides the first example of a phylogenetically diverse and extensive usage of translational frameshifting in animal mitochondrial coding sequences.
authors.affiliation: Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011, USA. Electronic address: khaen@iastate.edu.
authors.forename: Karri M
authors.initials: KM
authors.lastname: Haen
authors.affiliation: Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA 50011, USA.
authors.forename: Walker
authors.initials: W
authors.lastname: Pett
authors.affiliation: Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA 50011, USA.
authors.forename: Dennis V
authors.initials: DV
authors.lastname: Lavrov
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D004272:DNA, Mitochondrial / Q000235:genetics* / Q000378:metabolism; D019143:Evolution, Molecular; D016368:Frameshift Mutation; D018965:Frameshifting, Ribosomal; D023061:Gene Order; D050259:Genes, Mitochondrial; D054629:Genome, Mitochondrial; D008969:Molecular Sequence Data; D016366:Open Reading Frames; D010802:Phylogeny; D011161:Porifera / Q000145:classification / Q000235:genetics* / Q000378:metabolism; D012343:RNA, Transfer / Q000235:genetics / Q000378:metabolism; D012641:Selection, Genetic; D016415:Sequence Alignment
chemical_list: D004272:DNA, Mitochondrial; D012343:RNA, Transfer
keywords: ATP synthase F0 subunit 6; ATP synthase F0 subunit 8; Codon usage; Hexactinellida; Mitochondrial frameshift; Mitochondrial genome; NADH dehydrogenase subunit 1; NADH dehydrogenase subunit 2; NADH dehydrogenase subunit 3; NADH dehydrogenase subunit 4; NADH dehydrogenase subunit 4l; NADH dehydrogenase subunit 5; NADH dehydrogenase subunit 6; OXPHOS; Oxidative phosphorylation; Programmed translational frameshift; atp6; atp8; cob; cox1; cox2; cox3; cytochrome b; cytochrome c oxidase subunit 1; cytochrome c oxidase subunit 2; cytochrome c oxidase subunit 3; mitochondrial 12s ribosomal RNA; mitochondrial 16s ribosomal RNA; nad1; nad2; nad3; nad4; nad4L; nad5; nad6; oxidative phosphorylation; rnl; rns