Mitochondrial rRNA secondary structures and genome arrangements distinguish chelicerates: Comparisons with a harvestman (Arachnida: Opiliones: Phalangium opilio)

Abstract

Arachnids are a highly diverse group of arthropods, and many of the mitochondrial genomes that have been sequenced from arachnids possess unusual features in their inferred gene structures and genome organization. The first complete sequence of a mitochondrial genome from the arachnid order Opiliones (harvestmen) is presented here. Secondary structures of the two mitochondrial ribosomal subunits of Phalangium opilio are inferred and compared to mitochondrial rRNA structures of a hexapod and a chelicerate. The large subunit rRNA of P. opilio is found to have more helices conserved than in other arthropods, while the small subunit rRNA shows a complexity similar to that of other arthropods. These comparisons suggest that a reduction in rRNA complexity occurred in Pancrustacea after the divergence of Pancrustacea and Chelicerata from a common ancestor. The gene arrangement of the mitochondrial genome of P. opilio is compared with the gene order of taxa from all seven other orders of arachnids for which representative mitochondrial genomes have been sequenced. Taxa from five of these seven orders possess gene arrangements identical to that of Limulus polyphemus, and P. opilio is found to have a similar arrangement. However, in P. opilio, some genes near the putative control region are rearranged, with the suite of genes encoding tRNA Gln, the control region, and tRNA Ile located downstream of the two ribosomal RNA genes, and upstream of where they are typically located in chelicerates. The genome encodes only 21 of the typical 22 mitochondrial tRNA genes and lacks the gene for tRNA Leu(CUN). The protein-coding genes in the mitochondrial genome of P. opilio show a significantly decreased use of codons recognized by tRNA Leu(CUN), likely due to selection to utilize the more specific tRNA Leu(UUR) anticodon. The gene arrangement and lack of a tRNA Leu(CUN) gene in P. opilio is most parsimoniously explained by the occurrence of at least two translocation events, one of which probably destroyed the function of the tRNA Leu(CUN) gene. Phylogenetic relationships among the major orders of arachnids are inferred, using all 13 mt protein-coding genes, and gene rearrangements are mapped onto the phylogeny. The phylogenetic analyses are unable to resolve the placement of P. opilio but are generally consistent with an early divergence of members of the Dromopoda (harvestmen, scorpions, and solifuges) from the Micruran arachnids (spiders, whip spiders, vinegaroons, ricinuleids, and mites). However, unlike some morphologically based phylogenetic analyses, the existence of a clade of Dromopoda is not supported. While data on genome arrangement and gene loss do not provide further information to help resolve relationships among the arachnid orders, they distinguish some groups of arachnids, distinguish chelicerates from other arthropods, and further clarify the ancestral gene order of this diverse group of arthropods.