The first complete mitochondrial genome of the genus Laelaps with novel gene arrangement reveals extensive rearrangement and phylogenetics in the superfamily Dermanyssoidea.

We collected 56 specimens of Laelaps chini from the endemic Hengduan Mountain rat species (Eothenomys miletus) and obtained the first complete mitochondrial genome of L. chini by next-generation sequencing (NGS). The L. chini mitogenome is 16,507 bp in size and contains 37 genes and a control region of 2380 bp in length. The L. chini mitogenome has a high AT content and a compact arrangement with four overlapping regions ranging from 1 to 2 bp and 16 spacer regions ranging from 1 to 48 bp. We analyzed 13 protein-coding genes of L. chini mitogenome  and found that protein-coding genes in the L. chini mitogenome preferred codons ending in A/U and codon usage pattern was mainly influenced by natural selection. Cox1 has the slowest evolution rate and cox3 has the fastest evolution rate. We combined the mitochondrial genome of eight species of gamasid mites in the superfamily Dermanyssoidea from Genbank and the L. chini mitochondrial genome to analyze its rearrangement patterns and breakpoint numbers. We found that the L. chini mitogenome showed a novel arrangement pattern and nine species of gamasid mites in the superfamily Dermanyssoidea, which have been sequenced complete mitochondrial genomes to date, all showed different degrees of rearrangement. Laelaps chini, Echinolaelaps echidninus and Echinolaelaps fukinenensis were closely related species based on genetic distance and phylogenetic analyses. Notably they are clustered with Varroa destructor of the family Varroidae, suggesting that the family Varroidae is more closely related to the family Laelapidae, but more data are needed to test whether Varroa can be classified under the family Laelapidae. The L. chini mitogenome is the first complete mitochondrial genome for the genus Laelaps, and contributes to further exploration of the mitochondrial gene rearrangements and phylogeny for the superfamily Dermanyssoidea.

Correction: The complete mitochondrial genome of Echinolaelaps fukienensis provide insights into phylogeny and rearrangement in the superfamily Dermanyssoidea.

[This corrects the article DOI: 10.1371/journal.pone.0288991.].

The evolutionary characterization of Gamasida based on mitochondrial genes codon usage pattern.

Mites belonging to the suborder Gamasida are species-rich and habitat-diverse, with a worldwide distribution. To adapt to the environment and obtain better living conditions, all species of the suborder Gamasida have been undergoing constant evolution. The complete mitochondrial genome (mitogenome) is an invaluable molecular marker for studying the origin of species, genetic differentiation between closely related species, and between intraspecific groups. In some species of the suborder Gamasida, mitochondrial tRNA genes are truncated and carried unstable genetic information. This study presents a comparative analysis of codon usage pattern and preference of 13 protein-coding genes of 24 species in 17 genera and 10 families of the suborder Gamasida. Results showed that have an obvious AT preference (0.664-0.829) for codon usage in the suborder Gamasida. Most of the optimal and high-frequency codons also end in A/T. The degree of natural selection varies between the same protein-coding genes of different gamasid mites or among different protein-coding genes within the same gamasid mites. Base and codon usage pattern and preference are very similar between the same species and genus, namely the closer species, the more similar their bases and codons usage patterns and preference are. T bases and C bases were the preference bases for codon usage of 24 species in the suborder Gamasida. Evolution of the suborder Gamasida was dominated by natural selection (64.1%). This study provides the first comprehensive analysis of codon usage in the suborder Gamasida, which will greatly improve our understanding of codon usage patterns and preference, genetics, and evolution of the suborder Gamasida. It will help to evaluate the degree of molecular adaptation in the suborder Gamasida and to further explore evolutionary features of the suborder Gamasida.

The complete mitochondrial genome of Echinolaelaps fukienensis provide insights into phylogeny and rearrangement in the superfamily Dermanyssoidea.

BACKGROUND: Echinolaelaps fukienensis is the dominant mite species parasitic on the body surface of the genus Niviventer. The mitochondrial genome (mitogenome) has its own independent genetic material and genetic system, and is now widely used in population genetics, genealogical biogeography, phylogeny and molecular evolution studies. Species diversity of the superfamily Dermanyssoidea is very rich, but its mitogenomes AT content is high, and it is difficult to amplify the complete mitogenome by routine PCR. To date, we have only obtained the mitogenomes of 6 species, scarcity on sequence data has greatly impeded the studies in the superfamily Dermanyssoidea. METHODS: Echinolaelaps fukienensis were collected in 2019 from the body surface of Niviventer confucianus (Rodentia, Muridae) in Yunnan Province. The E. fukienensis mitogenome was determined and analyzed for the first time using the Illumina Novoseq 6000 platform. Phylogenetic analyses of the superfamily Dermanyssoidea were conducted based on the entire mitogenome sequences. RESULTS: The E. fukienensis mitogenome was 14,402 bp, which is known the smallest genome of the superfamily Dermanyssoidea, encoding a total of 37 genes, including 13 PCGs, 22 tRNAs, 2 rRNAs and 1 control region. Most protein-coding genes use ATN as the start codon and TAN as the stop codon. AT and GC skew of atp8 genes in E. fukienensis were both 0. The average length of 22 tRNA genes of E. fukienensis was 64 bp, and secondary structures of tRNAs showed base mismatches and missing D-arms in many places. Compared with gene arrangement pattern of the hypothetical ancestor of arthropods, the E. fukienensis mitogenome shows a novel arrangement pattern. Phylogenetic tree supported the monophyly of the superfamily Dermanyssoidea. Echinolaelaps fukienensis being the least genetic distant (0.2762) and most closely related to Varroa destructor. CONCLUSIONS: This study analyzed comprehensive the structure and evolution of the E. fukienensis mitogenome for the first time, enriches molecular data of the genus Echinolaelaps, which will contribute to further understand phylogeny and rearrangement patterns of the superfamily Dermanyssoidea.

The first complete mitochondrial genome of the genus Echinolaelaps reveals mitochondrial genome rearrangement type and evolution of Gamasida.

Echinolaelaps echidninus is a gamasid mite that is of medical and veterinary significance as parasites and vectors of disease agents, which can carry pathogens of zoonosis such as Rickettsia tsutsugamushi, Rickettsia Q fever, Rickettsia mooseri, Rickettsia pox pathogens, Corynebacterium pseudotuberculosis and Leptospira. At present, only single mitochondrial genes have been analysed for E. echidninus in the world, and no complete mitochondrial genome has been reported. However, information carried by a single gene is limited. Therefore, the complete mitochondrial genome of E. echidninus was determined for the first time by Illumina Hiseq X-Ten platform in this study. The mitochondrial genome is 15 736 bp in length and contains 13 protein-coding genes, 22 tRNA genes, 2 rRNA genes and a control region of 1561 bp in length. Codon analysis of 13 protein-coding genes revealed that UUU, UUA, AUU, AUA and AAU were the most frequently used, while cox2 had the fastest evolutionary rate and cob the slowest. Comparative analysis of genome structure and breakpoint distances of the mitochondrial genomes of 23 species in 17 genera from 10 families of Gamasida deposited in GenBank revealed a novel gene arrangement type of the E. echidninus mitochondrial genome, and different degrees of rearrangement among different taxa of Gamasida. Phylogenetic analyses of Gamasida were performed using the maximum likelihood and Bayesian inference methods. Echinolaelaps echidninus was clustered with Dermanyssoidea and formed a more supportive sister group with Varroa destructor. This study provides novel insights into rearrangement patterns and evolution of mitochondrial genomes of Gamasida.