Novel Mitochondrial Gene Content and Gene Arrangement Indicate Illegitimate Inter-mtDNA Recombination in the Chigger Mite, Leptotrombidium pallidum

Abstract

To better understand the evolution of mitochondrial (mt) genomes in the Acari (mites and ticks), we sequenced the mt genome of the chigger mite, Leptotrombidium pallidum (Arthropoda: Acari: Acariformes). This genome is highly rearranged relative to that of the hypothetical ancestor of the arthropods and the other species of Acari studied. The mt genome of L. pallidum has two genes for large subunit rRNA, a pseudogene for small subunit rRNA, and four nearly identical large noncoding regions. Nineteen of the 22 tRNAs encoded by this genome apparently lack either a T-arm or a D-arm. Further, the mt genome of L. pallidum has two distantly separated sections with identical sequences but opposite orientations of transcription. This arrangement cannot be accounted for by homologous recombination or by previously known mechanisms of mt gene rearrangement. The most plausible explanation for the origin of this arrangement is illegitimate inter-mtDNA recombination, which has not been reported previously in animals. In light of the evidence from previous experiments on recombination in nuclear and mt genomes of animals, we propose a model of illegitimate inter-mtDNA recombination to account for the novel gene content and gene arrangement in the mt genome of L. pallidum.

Doubly Uniparental Inheritance Is Associated With High Polymorphism for Rearranged and Recombinant Control Region Haplotypes in BalticMytilus trossulus

“…Rearrangement mechanisms and evolutionary origin of recombinant haplotypes: A variety of mechanisms have been proposed to explain mtDNA rearrangements (Stanton et al 1994;Lee and Kocher 1995;Boore 2000;Mueller and Boore 2005), including tandem duplication via slipped-strand mispairing followed by random loss or degeneration of redundant DNA (e.g., in lizards, Stanton et al 1994;in ticks, Shao et al 2004;in salamanders, Mueller and Boore 2005), nonhomologous intramolecular recombination (e.g., in nematodes, Lunt and Hyman 1997), homologous intermolecular recombination (e.g., in the flounder, Hoarau et al 2002), and nonhomologous intermolecular recombination (e.g., in mites, Shao et al 2005). The rearrangements observed in this study can be explained in a parsimonious manner by three processes: tandem duplication, deletion, and intermolecular recombination occurring one or more times during the evolution of the haplotypes.…”

Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species

“…With respect to the other mt-encoded genes, the common content consists of 2 rRNA genes (rrnS and rrnL) and 13 protein-coding genes for subunits of the respiratory chain complexes (nad1-nad6; nad4L; cox1-cox3; cob; atp6; atp8). The two rRNA genes are always mitochondrially encoded, and their duplication is very rare, having been observed in only four species (rrnS is duplicated in the bivalve Crassostrea gigas and in distinct haplotypes of the pillbug nematode Thaumamermis cosgrovei (Milbury and Gaffney, 2005;Tang and Hyman, 2007); rrnL is duplicated in the chigger mite Leptotrombidium pallidum (Shao et al, 2005b); both rrnS and rrnL are duplicated in the large mt haplotype of the nematode Strelkovimermis spiculatus). Loss or acquisition of the protein-coding genes are also rather infrequent (Table 2), and the actual loss of genes remains sometimes ambiguous due to uncertainty in gene annotation or to the availability of incomplete mtDNA sequences (see the absence of nad3 and nad6 in the mite Metaseiulus occidentalis, Jeyaprakash and Hoy, 2007, and the absence of atp8 and nad6 in two Hexactinellida sponges, Haen et al, 2007, respectively).…”

Mosaic gene conversion after a tandem duplication of mtDNA sequence in Diomedeidae (albatrosses)

“…Duplicated and concertedly evolved CRs have been reported in snakes (Kumazawa et al, 1996(Kumazawa et al, , 1998, sea cucumbers (Arndt and Smith, 1998), ticks (Black and Roehrdanz, 1998;Campbell and Barker, 1999;Shao et al, 2005a), birds (Eberhard et al, 2001;Abbott et al, 2005;Jouventin et al, 2006;Gibb et al, 2007;Smith et al, 2007;Lawrence et al, 2008;Cho et al, 2009;Gomez-Diaz et al, 2009), fish (Lee et al, 2001;Tatarenkov and Avise, 2007), thrips (Shao et al, 2003), lizards (Kumazawa and Endo, 2004;Amer and Kumazawa, 2005), a sea firefly (Ogoh and Ohmiya, 2004), cephalopods (Yokobori et al, 2004), a frog (Sano et al, 2005), mites (Shao et al, 2005b(Shao et al, , 2006, and turtles (Parham et al, 2006a(Parham et al, , 2006b). Some of the duplications involve structural genes or tRNAs (Kumazawa et al, 1998;Campbell and Barker, 1999;Eberhard et al, 2001;Yokobori et al, 2004;Abbott et al, 2005;Shao et al, 2005b;Parham et al, 2006b;Gibb et al, 2007;Cho et al, 2009). Duplicate and concertedly evolved structural genes, or tRNAs without CR involvement, are rare but have been reported in a chameleon (Townsend and Larson, 2002) and a pentastomid (Lavrov et al, 2004)...…”