The mitochondrial genome of the oribatid mite Paraleius leontonychus: new insights into tRNA evolution and phylogenetic relationships in acariform mites

Abstract

Bilaterian mitochondrial (mt) genomes are circular molecules that typically contain 37 genes. To date, only a single complete mitogenome sequence is available for the species-rich sarcoptiform mite order Oribatida. We sequenced the mitogenome of Paraleius leontonychus, another species of this suborder. It is 14,186 bp long and contains 35 genes, including only 20 tRNAs, lacking tRNA ^Gly and tRNA ^Tyr . Re-annotation of the mitogenome of Steganacarus magnus increased the number of mt tRNAs for this species to 12. As typical for acariform mites, many tRNAs are highly truncated in both oribatid species. The total number of tRNAs and the number of tRNAs with a complete cloverleaf-like structure in P. leontonychus, however, clearly exceeds the numbers previously reported for Sarcoptiformes. This indicates, contrary to what has been previously assumed, that reduction of tRNAs is not a general characteristic for sarcoptiform mites. Compared to other Sarcoptiformes, the two oribatid species have the least rearranged mt genome with respect to the pattern observed in Limulus polyphemus, a basal arachnid species. Phylogenetic analysis of the newly sequenced mt genome and previously published data on other acariform mites confirms paraphyly of the Oribatida and an origin of the Astigmata within the Oribatida.

Figure 1

Mitochondrial genome of P. leontonychus. Genes transcribed on the leading (+)-strand are on the outside of the circles, those on the lagging (−)-strand on the inside of the circles. Color codes for the genes are given in the box; tRNAs are abbreviated by the one-letter code for the corresponding amino acid. All abbreviations are the same as in Table 1.

Figure 2

Predicted secondary structures of the 20 mt tRNAs of P. leontonychus.

Figure 3

Mitochondrial gene arrangements of the two oribatid species, P. leontonychus and S. magnus, compared to L. polyphemus, representing the arthropod ground pattern. For S. magnus, mitogenome orders obtained from different annotations are shown. All abbreviations are the same as in Fig. 1 and Table 1. Arrow pointing to the right represents the (+)-strand and arrow to the left the (−)-strand. Genes are drawn in their original order; intergenic distances are not included and sizes of genes are not true to scale. Orange box represents a gene with a different location relative to L. polyphemus; yellow boxes indicate genes that have different positions and ice blue boxes genes that are different in terms of both position and strand associations. Green boxes highlight the newly predicted tRNAs for S. magnus, grey boxes indicate congruencies between the re-annotation of Klimov and OConnor, and this study.

Figure 4

Phylogenetic relationships among 37 mite taxa inferred from Bayesian Inference analyses of nucleotide sequences of PGCs. Numbers at nodes indicate posterior probabilities ML bootstrap values, respectively. Numbers in parentheses following the species names refer to the total number of tRNAs found in that species. For the acariform taxa, tRNAs with typical clover-leaf secondary structure are shown in different colors (C in orange, D in pink, E in ice-blue, G in rose, K in white, L₁ in dark green, L₂ in light green, M in yellow, N in red, Q in violet and W in light grey).

Figure 5

Neighbor joining (NJ) tree based on distances calculated from a CREx gene rearrangement analysis. Genes are drawn in their original order; intergenic distances are not included and sizes of genes are not to scale. Protein-coding genes are colored in yellow, rRNAs in light grey and control regions in dark grey. All abbreviations are the same as in Fig. 1 and Table 1. Genes are transcribed from left to right excepting the underlined ones, which are located on the (−)-strand. *Gene annotation of the present study was used for this analysis.