Molecular Mechanisms for the Variation of Mitochondrial Gene Content and Gene Arrangement Among Chigger Mites of the Genus Leptotrombidium (Acari: Acariformes)

Abstract

The gene content of a mitochondrial (mt) genome, i.e., 37 genes and a large noncoding region (LNR), is usually conserved in Metazoa. The arrangement of these genes and the LNR is generally conserved at low taxonomic levels but varies substantially at high levels. We report here a variation in mt gene content and gene arrangement among chigger mites of the genus Leptotrombidium. We found previously that the mt genome of Leptotrombidium pallidum has an extra gene for large-subunit rRNA (rrnL), a pseudo-gene for small-subunit rRNA (PrrnS), and three extra LNRs, additional to the 37 genes and an LNR typical of Metazoa. Further, the arrangement of mt genes of L. pallidum differs drastically from that of the hypothetical ancestor of the arthropods. To find to what extent the novel gene content and gene arrangement occurred in Leptotrombidium, we sequenced the entire or partial mt genomes of three other species, L. akamushi, L. deliense, and L. fletcheri. These three species share the arrangement of all genes with L. pallidum, except trnQ (for tRNA-glutamine). Unlike L. pallidum, however, these three species do not have extra rrnL or PrrnS and have only one extra LNR. By comparison between Leptotrombidium species and the ancestor of the arthropods, we propose that (1) the type of mt genome present in L. pallidum evolved from the type present in the other three Leptotrombidium species, and (2) three molecular mechanisms were involved in the evolution of mt gene content and gene arrangement in Leptotrombidium species.

Mitochondrial genome sequence of Unionicola foili (Acari: Unionicolidae): a unique gene order with implications for phylogenetic inference

“…Similar overlaps between these gene pairs have been annotated in other Trombidiformes species with completed genomes (Shao et al 2006(Shao et al , 2005 and GenBank accession AB300500. For genes on opposite strands, tRNA-Thr and tRNA-Tyr overlap by one base, tRNA-Gln and tRNA-Ile overlap by one base, and tRNA-Arg and tRNA-Val overlap by three bases.…”

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

“…In particular, L. pallidum differs from two congeneric species for the presence of a rrnS pseudogene, two identical and oppositely oriented rrnL genes, and four nearly identical extra non-coding regions. However, the arrangement of the shared mt genes is almost identical within the genus, except for the translocation of trnQ (Shao et al, 2005b(Shao et al, , 2006a. These peculiarities, combined with a gene arrangement drastically different from the ancestral arthropod gene order, have led to the hypothesis that the mtDNA AR of L. pallidum arose by a mechanism of 'duplication-random gene loss' followed by inter-genome non-homologous recombination (Shao et al, 2006a).…”

“…However, the arrangement of the shared mt genes is almost identical within the genus, except for the translocation of trnQ (Shao et al, 2005b(Shao et al, , 2006a. These peculiarities, combined with a gene arrangement drastically different from the ancestral arthropod gene order, have led to the hypothesis that the mtDNA AR of L. pallidum arose by a mechanism of 'duplication-random gene loss' followed by inter-genome non-homologous recombination (Shao et al, 2006a). Interestingly, clues of mtDNA recombination have been found even in other congeneric comparisons of Acari.…”

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

“…Sequence duplications in the mt genome frequently involve the control region (CR), which is associated with the initiation of transcription and mtDNA replication. 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).…”