title: Mitochondrial DNA of Clathrina clathrus (Calcarea, Calcinea): six linear chromosomes, fragmented rRNAs, tRNA editing, and a novel genetic code.
abstract: Sponges (phylum Porifera) are a large and ancient group of morphologically simple but ecologically important aquatic animals. Although their body plan and lifestyle are relatively uniform, sponges show extensive molecular and genetic diversity. In particular, mitochondrial genomes from three of the four previously studied classes of Porifera (Demospongiae, Hexactinellida, and Homoscleromorpha) have distinct gene contents, genome organizations, and evolutionary rates. Here, we report the mitochondrial genome of Clathrina clathrus (Calcinea, Clathrinidae), a representative of the fourth poriferan class, the Calcarea, which proves to be the most unusual. Clathrina clathrus mitochondrial DNA (mtDNA) consists of six linear chromosomes 7.6-9.4 kb in size and encodes at least 37 genes: 13 protein codings, 2 ribosomal RNAs (rRNAs), and 24 transfer RNAs (tRNAs). Protein genes include atp9, which has now been found in all major sponge lineages, but no atp8. Our analyses further reveal the presence of a novel genetic code that involves unique reassignments of the UAG codons from termination to tyrosine and of the CGN codons from arginine to glycine. Clathrina clathrus mitochondrial rRNAs are encoded in three (srRNA) and ≥6 (lrRNA) fragments distributed out of order and on several chromosomes. The encoded tRNAs contain multiple mismatches in the aminoacyl acceptor stems that are repaired posttranscriptionally by 3'-end RNA editing. Although our analysis does not resolve the phylogenetic position of calcareous sponges, likely due to their high rates of mitochondrial sequence evolution, it confirms mtDNA as a promising marker for population studies in this group. The combination of unusual mitochondrial features in C. clathrus redefines the extremes of mtDNA evolution in animals and further argues against the idea of a "typical animal mtDNA."
authors.affiliation: Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Iowa, USA. dlavrov@iastate.edu
authors.forename: Dennis V
authors.initials: DV
authors.lastname: Lavrov
authors.forename: Walker
authors.initials: W
authors.lastname: Pett
authors.forename: Oliver
authors.initials: O
authors.lastname: Voigt
authors.forename: Gert
authors.initials: G
authors.lastname: Wörheide
authors.forename: Lise
authors.initials: L
authors.lastname: Forget
authors.forename: B Franz
authors.initials: BF
authors.lastname: Lang
authors.forename: Ehsan
authors.initials: E
authors.lastname: Kayal
mesh_terms: D000818:Animals; D001483:Base Sequence; D001499:Bayes Theorem; D002875:Chromosomes / Q000235:genetics; D003062:Codon; D017124:Conserved Sequence; D021901:DNA, Intergenic; D004272:DNA, Mitochondrial / Q000235:genetics*; D014644:Genetic Variation; D054629:Genome, Mitochondrial; D016013:Likelihood Functions; D008957:Models, Genetic; D008969:Molecular Sequence Data; D009690:Nucleic Acid Conformation; D010802:Phylogeny; D011161:Porifera / Q000235:genetics*; D017393:RNA Editing; D012335:RNA, Ribosomal / Q000235:genetics*; D012343:RNA, Transfer / Q000235:genetics*; D017422:Sequence Analysis, DNA; D020079:Terminal Repeat Sequences
chemical_list: D003062:Codon; D021901:DNA, Intergenic; D004272:DNA, Mitochondrial; D012335:RNA, Ribosomal; D012343:RNA, Transfer