Mitochondrial Analysis of Oribatid Mites Provides Insights into Their Atypical tRNAs Annotation, Genome Rearrangement and Evolution

Abstract

Background: Mitochondrial (mt) genomes of Sarcoptiformes mites typically contain 37 genes. Loss of genes is rare in Sarcoptiformes mite mt genomes, but two of the six previously reported oribatid mites (Acariform Order Sarcoptiformes) are reported to have lost part of their tRNA genes. To determine whether these tRNA genes were indeed lost and whether the loss of tRNAs is universal, we re-annotated all of the available oribatid mites and sequenced the mt genome of Oribatula sakamorii. Methods: The mitogenome of O. sakamorii was sequenced with Illumina Hiseq sequencer. The mt tRNA gene annotated using multi-software combined with manual annotation approach. Phylogenetic analyses of maximum likelihood (ML) and Bayesian inference (BI) were performed with both concatenated nucleotide and amino acid sequences.Results: Mt genomes of O. sakamorii contain 37 genes including 22 tRNA genes. We were able to identify all of the mt tRNA genes that were reported as lost in Steganacarus magnus and Paraleius leontonychus, and revealed some atypical tRNAs annotation errors in oribatid mites. Oribatid mite mt genomes are characterized by low rates of gene rearrangement, with six or seven gene blocks conserved between all of the oribatid mite species and the mt genome of ancestral arthropod. Considering only the relative order of the major genes (PCGs, rRNAs), only one gene or two genes were rearranged relative to the ancestral genome. Both CREx analysis and phylogenetic results supported the origin of the Astigmata within the Oribatida. We also explored the phylogenetic relationships among all of the available oribatid mites and the results also confirm the systematic position of Hermannia in the Crotonioidea superfamily. This is also supported by synapomorphic gene derived boundary.Conclusions: The tRNA "lost" phenomenon is not universal in oribatid mites. Instead of loss, we found that the highly atypical secondary structure of inferred mt tRNA genes makes them unidentifiable by a single type of tRNA search program. Multi-software combined with manual annotation approach can improve the accuracy of tRNA gene annotation. Besides, we determined the correct systematic position of Hermannia and supported the origin of astigmatid mites was from oribatid mites.