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Comparative analysis of the mitochondrial genome of Dermacentor steini from different regions in China

Published online by Cambridge University Press:  09 December 2022

Huijuan Yang ,
Ting Chen  and
Wenge Dong Open the ORCID record for Wenge Dong [Opens in a new window]
Huijuan Yang
Affiliation:
Yunnan Provincial Key Laboratory for Zoonosis Control and Prevention, Institute of Pathogens and Vectors, Dali University, Dali, Yunnan 671000, China
Ting Chen
Affiliation:
Yunnan Provincial Key Laboratory for Zoonosis Control and Prevention, Institute of Pathogens and Vectors, Dali University, Dali, Yunnan 671000, China
Wenge Dong*
Affiliation:
Yunnan Provincial Key Laboratory for Zoonosis Control and Prevention, Institute of Pathogens and Vectors, Dali University, Dali, Yunnan 671000, China
*
Author for correspondence: Wenge Dong, E-mail: dongwenge2740@sina.com
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Abstract

Ticks are a group of blood-sucking ectoparasites that play an important role in human health and livestock production development as vectors of zoonotic diseases. The phylogenetic tree of single genes cannot accurately reflect the true kinship between species. Based on the complete mitochondrial genome analysis one can help to elucidate the phylogenetic relationships among species. In this study, the complete mitochondrial genome of Dermacentor steini (isolate Longyan) was sequenced and compared with the mitochondrial genes of 3 other Chinese isolates (Nanchang, Jinhua and Yingtan). In Dermacentor steini 4 isolates had identical or similar mitochondrial genome lengths and an overall variation of 0.76% between sequences. All nucleotide compositions showed a distinct AT preference. The most common initiation and stop codons were ATG and TAA, respectively. Fewer base mismatches were found in the tRNA gene of D. steini (isolate Longyan), and the vicinity of the control region and tRNA gene was a hot rearrangement region of the genus Dermacentor. Maximum likelihood trees and Bayesian trees indicate that D. steini is most closely related to Dermacentor auratus. The results enrich the mitochondrial genomic data of species in the genus Dermacentor and provide novel insights for further studies on the phylogeographic classification and molecular evolution of ticks.

Keywords

Comparative analysisDermacentor steiniMitochondrial genomePhylogenyTick
Type
Research Article
Information
Parasitology , Volume 150 , Issue 2 , February 2023 , pp. 195 - 205
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Introduction

Ticks are a group of blood-sucking ectoparasites that often parasitize on the body surfaces of mammals, birds, reptiles and amphibians (Burnard and Shao, Reference Burnard and Shao2019). Ticks have become the second largest vector of infectious diseases worldwide after mosquitoes because they can carry a variety of pathogens such as bacteria, fungi, viruses, nematodes and blood protozoans (Mead et al., Reference Mead, Hinckley, Hook and Beard2015). Ticks can also cause severe allergic or toxic reactions, temporary paralysis and secondary infections in humans, livestock and other vertebrates through their bites, seriously endangering human health as well as livestock development (Chen et al., Reference Chen, Yang, Bu, Yang, Yang and Liu2010).

The genus Dermacentor (Ixodida: Ixodidae) is a recently evolved genus with relatively limited species diversity compared to other genera (e.g. Ixodes and Haemaphysalis) in the family Ixodidae (Ernieenor et al., Reference Ernieenor, Apanaskevich, Ernna, Ellyncia, Mariana and Yaakop2021). Forty species of the genus Dermacentor have been reported to be distributed worldwide, and 12 species have been found in China (Guo et al., Reference Guo, Zhang, Fu, Gao, Liu, Qiu, Chang and Wang2016; Nava et al., Reference Nava, Venzal, González-Acuña, Martins and Guglielmone2017). All species of the genus Dermacentor have distinct external morphological characteristics and are classified in the subgenus Indocentor Schulze (Ernieenor et al., Reference Ernieenor, Apanaskevich, Ernna and Mariana2020). Hosts of the genus Dermacentor include horses, cattle, sheep and rodents, and can transmit a variety of pathogens, including Babesia bovis, B. caballi, B. canis, Theileria equi and other protozoa; Brucella, Rickettsia, Rocky Mountain spotted fever, Anaplasma and other bacteria, as well as tick-borne encephalitis virus (Parola et al., Reference Parola, Paddock and Raoult2005; Swei et al., Reference Swei, O'Connor, Couper, Thekkiniath, Conrad, Padgett, Burns, Yoshimizu, Gonzales, Munk, Shirkey, Konde, Mamoun, Lane and Kjemtrup2019; Ličková et al., Reference Ličková, Havlíková, Sláviková, Slovák, Drexler and Klempa2020; Duncan et al., Reference Duncan, Grant, Johnson, Sundstrom, Saleh and Little2021; Eisen and Paddock, Reference Eisen and Paddock2021; Yang et al., Reference Yang, Christie, Köster, Du and Yao2021). In addition, species of the genus Dermacentor are also most frequently associated with human intra-ear infections (Mariana et al., Reference Mariana, Srinovianti, Ho, Halimaton, Hatikah, Shaharudin, Rosmaliza, Wan Ishlah and Sathananthar2008). Among them, Dermacentor steini is considered to be the most abundant member of the subgenus Indocentor and is mainly parasitic on wild boars in Asian countries (Wassef and Hoogstraal, Reference Wassef and Hoogstraal1988; Lim et al., Reference Lim, Khoo, Tan, Zainal, Loong, Khor and AbuBakar2020). D. steini is morphologically most similar to D. auratus and D. atrosignatus and carries pathogens (Rickettsia sp., Anaplasma sp., Lanjan virus and Hepatozoon species) similar to those isolated from D. auratus (Wassef and Hoogstraal, Reference Wassef and Hoogstraal1986, Reference Wassef and Hoogstraal1988). Most importantly, D. steini feeds on human skin or other tissues and is an important reservoir host and vector of zoonotic diseases, which poses a greater threat to public health safety (Vongphayloth et al., Reference Vongphayloth, Brey, Robbins and Sutherland2016; Lim et al., Reference Lim, Khoo, Tan, Zainal, Loong, Khor and AbuBakar2020).

The mitochondrial genome (mitogenome) is a DNA molecule typically 15–20 kb in size, with 37 genes, including 13 protein-coding genes (PCGs), 22 transfer RNA genes (tRNAs), 2 ribosomal RNA genes (rRNAs) and usually longer non-coding regions (control regions) (Wang et al., Reference Wang, Wang, Shi, Wu, Tao, Guo, Ji and Bai2018, Reference Wang, Shi, Guo, Tang, Bai and Wang2020). The mitochondrial genome is widely considered as one of the most reliable and effective genetic markers in molecular phylogenetic studies because of its maternal inheritance, high mutation rate and lack of recombination (Yang et al., Reference Yang, Chen and Dong2022a, Reference Yang, Yang and Dong2022b). Meanwhile, the mitochondrial genome has been proven to be a useful tool for understanding the evolutionary, geographic and pathogenic relationships of tick species (Burger et al., Reference Burger, Shao and Barker2013).

Given the wide distribution of ticks of the genus Dermacentor and their importance as vectors of zoonotic diseases, they have an important role in the development of human and livestock production. Thus, this study reports the mitochondrial genome sequence of D. steini (Longyan isolate) collected in Longyan, Fujian Province, China, and compared with those of 3 other D. steini (Jinhua, Nangchang and Yingtan isolates) from different regions of China.

Materials and methods

Sample collection

Rats were captured using mousetraps in Longyan, Fujian Province, China. Adult ticks were then collected from the body surface of the captured rats (Rattus andamanensis) and preserved in Eppendorf (EP) tubes with 95% ethanol, and the sample number was labelled P299.

Statement: The capture protocol and procedures for small mammals were approved by the Animal Ethics Committee of Dali University. The approval number is MECDU-201806-11.

DNA extraction and mitogenome sequencing

The adult ticks were taken out of the EP tubes containing 95% ethanol and immersed in sterile distilled water for 30 min to remove microorganisms from the surface, and then the ticks were cut with a sterile scalpel blade. Genomic DNA was extracted from ticks with the DNeasy Blood and Tissue Kit (Qiagen, Valencia, California, USA). The extracted DNA was used to construct Illumina PE libraries. The mitochondrial genome was then sequenced on the Illumina Novoseq 6000 platform (Winnerbio, Shanghai, China).

Genome annotation

MitoZ 2.3 (https://doi.org/10.1101/489955) was used to assemble the mitochondrial genome. The MITOS web server was used to predict genes (Bernt et al., Reference Bernt, Donath, Jühling, Externbrink, Florentz, Fritzsch, Pütz, Middendorf and Stadler2013), and 13 PCGs were compared and edited using the BLAST tool in NCBI. The location and length of tRNA genes were further confirmed using tRNAscan-SE (Lowe and Eddy, Reference Lowe and Eddy1997) and ARWEN (Laslett and Canbäck, Reference Laslett and Canbäck2008). Two rRNA genes were identified based on their putative secondary structures and previously sequenced mitochondrial genome sequences. The position of the control region was confirmed based on the boundaries of neighbouring genes. The mitochondrial sequence of D. steini (Longyan isolate) has been deposited in GenBank under the accession number OP383032.

Sequence analysis and phylogenetic reconstruction

Base composition and codon usage were calculated using GeneiousPrime (Kearse et al., Reference Kearse, Moir, Wilson, Stones-Havas, Cheung, Sturrock, Buxton, Cooper, Markowitz, Duran, Thiere, Ashton, Meintjes and Drummond2012) and MEGA X (Kumar et al., Reference Kumar, Stecher and Tamura2016), respectively. Sliding window analysis was performed on the complete mitochondria of different D. steini isolates using DnaSP v5 (Librado and Rozas, Reference Librado and Rozas2009). The sliding window length was set to 100 bp with a step size of 25 bp to estimate the value of nucleotide diversity. Phylogenetic trees were constructed using Bayesian inference (BI) methods and maximum likelihood (ML) methods with Limulus polyphemus and Carcinoscorpius rotundicauda as outgroups. BI and ML analyses were performed in PhyloSuite (Zhang et al., Reference Zhang, Gao, Jakovlić, Zou, Zhang, Li and Wang2020). For the Bayesian analysis, a total of 1 000 000 generations were run, with sampling every 1000 generations. The first 25% of the tree was burned to ensure sample independence and 4 Monte Carlo Markov chains were run. To estimate the support of the BI tree, posterior probabilities (PP) were calculated. For the ML tree, 5000 ultra-fast bootstrap replications were used to calculate branch reliability (bootstrap probability, BP). The constructed phylogenetic tree was viewed and edited with FigTree 1.4.1 (https://github.com/rambaut/figtree/). Species and accession numbers for the construction of the phylogenetic tree are shown in Supplementary Table 1.

Results

Mitochondrial genome characteristics of Dermacentor steini (Longyan isolate)

The mitochondrial genome of D. steini (Longyan isolate) is a circular double-stranded DNA molecule with a length of 14 785 bp. It includes 13 PCGs (cox1-3, cytb, nad1-6, nad4L, atp6 and atp8), 22 tRNA genes, 2 rRNA genes (rrnL and rrnS) and 2 control regions (Table 1), which is consistent with the reported mtgenomes of other species of the genus Dermacentor but not with the mitochondrial genomes of some metazoan, such as in trematodes, cestodes and Chromadorea nema-todes, which have been found to have lost the atp8 gene in their mitochondrial genomes (Yamasaki et al., Reference Yamasaki, Ohmae and Kuramochi2012; Duan et al., Reference Duan, Gao, Hou, Zhang, Liu, Gao, Guo, Yue, Su, Fu and Wang2015; Chang et al., Reference Chang, Liu, Gao, Zheng, Zhang, Duan, Yue, Fu, Su and Wang2016). Of the 37 genes, 23 genes (cox1-3, nad2-3, nad6, atp6, atp8, cytb, trnA, trnC, trnD, trnE, trnG, trnI, trnK, trnM, trnN, trnR, trnS 1, trnS 2, trnT, trnW) are encoded on the J-strand, and the remaining 12 genes (nad1, nad4, nad4L, nad5, trnF, trnH, trnL 1, trnL 2, trnP, trnQ, trnV, trnY) and 2 rRNA genes (16S rRNA and 12S rRNA) are encoded on the N-strand.

Table 1. Dermacentor steini gene content, length, coding strand, initiation and stop codons of mitochondrial genomes of different isolate

L.Y, Longyan; N.C, Nanchang; J.H, Jinhua; Y.T, Yingtan

The mitochondrial genome of D. steini (Longyan isolate) is relatively compact with 12 gene intergenic regions and 16 gene overlap regions (Table 1), with total lengths of 90 and 52 bp, respectively. The intergenic region occurred at 23 gene junctions. The longest intergenic sequence (26 bp) was found between trnQ and trnF, and the shortest intergenic sequence (1 bp) was found between trnA and trnR, trnV and 12S rRNA, nad4L and trnT, and trnP and nad6. Overlap regions occurred at 29 gene junctions. The longest overlap sequence, 8 bp, was found between trnY and cox1. The shortest overlap region, 1 bp, was found between nad3 and trnA, trnS 1 and trnE, trnF and nad5, and trnS 2 and trnL 1. Among them, the 7 bp overlap between the nad4 and nad4L genes has also been widely reported in the mitochondrial genome of insects (Wang and Tang, Reference Wang and Tang2017).

The typical secondary structure of tRNA genes is a cloverleaf structure with 4 arms: amino acid acceptor arm (AA-arm), DHC arm (D-arm), anticodon arm (AC-arm) and TΨC arm (T-arm) (Yuan et al., Reference Yuan, Wei, Wang, Dou and Wang2010). The 22 tRNA genes of D. steini (Longyan isolate) have a total length of 1391 bp. The length of individual tRNA genes ranged from 57 bp (trnC) to 68 bp (trnR), and their secondary structures are shown in Fig. 1. Except for trnC and trnS 1, which lacked the D-arm, the other 20 tRNA genes were able to form a typical cloverleaf structure. Among these tRNA genes, 14 tRNA genes are encoded in the J-strand and the other 8 tRNA genes are encoded in the N-strand. Besides the typical Waston–Crick pairings (A–U, G–C), 12 non-canonical pairings, 9 G–U pairings and 3 U–U mismatches occurred.

Fig. 1. Dermacentor steini (Longyan isolate) tRNA gene putative secondary structure.

Comparative analysis between mitochondrial genomes of D. steini (Longyan, Nanchang, Jinhua and Yingtan isolates)

The mitochondrial genomes of D. steini isolated from Longyan and Nanchang were of the same length, 12 and 18 bp longer than those of Jinhua and Yingtan isolates, respectively. The 37 genes and 2 non-coding regions of the D. steini from Longyan, Nanchang, Jinhua and Yingtan isolate mitochondrial genomes were identical or similar in length, and the overall variation between sequences was 0.76%. From Table 2, the nucleotide composition of the mitochondrial genomes of the 4 isolates (Longyan, Nanchang, Jinhua and Yingtan) showed a distinct AT preference. All PCGs used the typical ATN as the initiation codon and no rare initiation codons (GTG and TTG) were present; of which; ATT and ATG were used up to 5 and 6 times, respectively. With the use of stop codons, most PCGs ended with the complete stop codon TAA. The truncated stop codon T/TA was found in the cox2, cox3 and nad4 genes of 4 isolates (Longyan, Nanchang, Jinhua and Yingtan). Figure 2 shows an analysis of the selection pressure of each protein-coding gene, which revealed that the ratio of non-synonymous mutation to synonymous mutation (Ka/Ks) for each protein-coding gene was less than 1, and the ratio of nad3 and nad4L was 0.

Fig. 2. Selection pressure analysis for different isolates in Dermacentor steini.

Table 2. Dermacentor steini variation in nucleotide and predicted amino acid sequences of the mitochondrial genome of different isolates

The nucleotide and amino acid variations of the 13 PCGs in Longyan, Nanchang, Jinhua and Yingtan isolates are shown in Table 2. The highest variation in nucleotides between homologous genes was found for atp8 (1.89%), and with lowest variation gene was nad3 (0.00%). For amino acid sequences, the lowest variation genes were nad4 and atp6 (0.00%), and the atp8 gene had the highest variation (5.66%). These results suggest that the atp8 gene was the most variable. The 2 rRNAs (rrnL and rrnS) of the Longyan, Nanchang, Jinhua and Yingtan isolates were similar in length to other ticks (Burger et al., Reference Burger, Shao and Barker2014; Williams-Newkirk et al., Reference Williams-Newkirk, Burroughs, Changayil and Dasch2015). rrnL was located between trnL and trnV with a 1.00% nucleotide variation; rrnS was located between trnV and NCR1 with a nucleotide variation of 1.54%.

The nucleotide diversity (Pi) of the 13 PCGs of D. steini (Longyan, Nanchang, Jinhua and Yingtan isolates) was analysed using DnaSP (Fig. 3). It was found that the nucleotide variation of D. steini within and between genes was low, in the range of 0.0000–0.0117. According to the window analysis, the most variable sequences were atp8 (0.0117), nad6 (0.0058), cox1 (0.0050) and nad2 (0.0049), while the most conserved sequences were nad3 (0.000).

Fig. 3. Sliding window analysis of the complete mitochondrial genomes of Dermacentor steini different isolates. The black line indicates the nucleotide diversity values (Pi) in the sliding window analysis with a window size of 100 bp and a step size of 25; the gene boundaries are indicated by the variation rate of each gene.

Rearrangement and phylogenetic analysis of the mitochondrial genome of D. steini (Longyan, Nanchang, Jinhua and Yingtan isolates)

Although the mitochondrial genome evolves at a rapid rate, the order of the 37 genes is very conservative, and the rearrangement characteristics of mitochondrial genes are generally used to resolve controversial phylogenetic questions (Babbucci et al., Reference Babbucci, Basso, Scupola, Patarnello and Negrisolo2014). Compared to the mitochondrial genome the arrangement pattern of arthropod hypothetical ancestors, smaller rearrangements occurred in the mitochondrial genomes of D. steini (Longyan, Nanchang, Jinhua and Yingtan isolates) and other species of the genus Dermacentor (Fig. 4). Rearrangements occurred mainly in 3 regions, namely, nad1-trnL 2, trnI-trnQ-trnF, underwent translocations, as well as trnC underwent translocations and inversions, and all rearrangements occurred in the vicinity of control regions and tRNA genes. Phylogenetic trees were constructed using the maximum likelihood and Bayesian methods based on 13 PCGs with L. polyphemus (NC003057) and C. rotundicauda (JX437074) as outgroups (Fig. 5). The topology of the phylogenetic tree formed by the 2 methods was almost identical, except for slight differences in the support rates of branch nodes: the support rate of the Bayesian tree (BI) was generally higher than that of the maximum likelihood tree (ML), with the majority of nodes having a support rate of 1; while the support rates of the maximum likelihood tree (ML) were all in the range of 80–100, except for 3 nodes with a support rate of less than 80. The phylogenetic tree shows that the family Ixodidae is a monophyletic group, except for the genus Archaeocroton, in which all other genera are clustered separately into a single group. D. steini isolated from Longyan and Nanchang clustered preferentially together and then formed sister branches with high node support (BP > 95, PP > 0.95) to D. steini isolated from Jinhua and Yingtan. The present phylogenetic tree results show that the genus Dermacentor is most closely related to 2 genera (Rhipicentor and Hyalomma) in the family Ixodidae (BP > 95, PP > 0.95).

Fig. 4. Mitochondrial genome rearrangement evolution in the genus Dermacentor. Green indicates translocations, blue indicates translocations and inversions.

Fig. 5. Phylogenetic analysis based on the nucleotide sequences of the 13 PCGs in the mitogenome. The numbers beside the nodes are posterior probabilities (BI) and bootstrap (ML) indicates the species in this study.

Discussion

Most species of the genus Dermacentor are 3-host ticks, with larval and nymph ticks mainly parasitizing small mammals and adult ticks mainly parasitizing cattle, sheep and wild medium and large mammals, and are capable of transmitting a variety of diseases to humans and animals (Hajdušek et al., Reference Hajdušek, Šíma, Ayllón, Jalovecká, Perner, De La Fuente and Kopáček2013; Ernieenor et al., Reference Ernieenor, Apanaskevich, Ernna and Mariana2020). Molecular biology studies are essential for the surveillance, prevention and control of tick-borne diseases.

In this study, the complete mitochondrial genome of D. steini (Longyan isolate) was sequenced and compared with the Nanchang, Jinhua and Yingtan isolates. The mitochondrial genome of D. steini (Longyan, Nanchang, Jinhua and Yingtan isolates) was found to be shorter than that of most species of the genus Dermacentor. The size of the mitochondrial genome varied among species, mainly due to the differences in the number and length of non-coding regions (Mo et al., Reference Mo, Guo, Xiao, Xin, Xia and Zou2019). The nucleotide composition of D. steini (Longyan, Nanchang, Jinhua and Yingtan isolates) showed a distinct AT preference, ranging from 76.8% to 76.9%, which is within the reported range of the Dermacentor genus ticks (Xin et al., Reference Xin, Liu, Zhang, Wang, Tang, Zhang, Zhou, Chai and Liu2018). It has been suggested that the higher AT content than GC content is a common derivative of arthropod mitochondrial genomes (Ikemura, Reference Ikemura1985; Simon et al., Reference Simon, Frati, Beckenbach, Crespi, Liu and Flook1994). All 37 mitochondrial genes of D. steini (Longyan, Nanchang, Jinhua and Yingtan isolates) were non-homogeneously distributed. Of the 23 genes located in the J-strand, the remaining genes were in the N-strand. In general, mitochondrial genes located on the J-strand are more susceptible to hydrolysis and oxidation (Brown et al., Reference Brown, Prager, Wang and Wilson1982). Among the 13 PCGs of D. steini (Longyan, Nanchang, Jinhua and Yingtan isolates), 4 genes (nad1, nad4, nad4L, nad5) were located on the N-strand, indicating that these 4 genes have relative stability.

The initiation codon and stop codon differ between species, and variations in the genetic code can be used as specific markers of the mitochondrial genome (Murrell et al., Reference Murrell, Campbell and Barker2003). For example, ATN is considered to be the most common initiation codon in Insecta, while AGA and AGG are the most common stop codons in vertebrate mitochondrial genomes (Wolstenholme, Reference Wolstenholme1992; Wang et al., Reference Wang, Zhang, Pei, Yu and Liu2019). The most common initiation and stop codons of D. steini (Longyan, Nanchang, Jinhua and Yingtan isolates) are ATG and TAA, respectively, which are also found in the mitochondrial genomes of other ticks (Liu et al., Reference Liu, Liu, Kuermanali, Wang, Chen, Guo, Zhao, Wang, Han, Wang, Wang, Shen, Zhang and Chen2018). Three PCGs (cox2, cox3 and nad4) have incomplete stop codons, and those incomplete stop codons can be modified by post-transcriptional polyadenylation to eventually form complete stop codons (Donath et al., Reference Donath, Jühling, Al-Arab, Bernhart, Reinhardt, Stadler, Middendorf and Bernt2019). The mitochondrial protein-encoding genes have been conserved (Chen et al., Reference Chen, Tian, Shi, Cao and Hao2012). The Ka/Ks of the 13 PCGs of D. steini (Longyan, Nanchang, Jinhua and Yingtan isolates) were all less than 1, indicating that these 13 PCGs were subject to purifying selection and did not undergo rapid evolution. The Ka/Ks of nad3 and nad4L were 0, further indicating that these 2 genes are highly conserved.

As the mitochondrial tRNA genes are approximately the same size, in comparison to nuclear tRNA genes, mitochondrial tRNA genes have a higher evolution rate (Saccone et al., Reference Saccone, De Giorgi, Gissi, Pesole and Reyes1999). The trnS 1 gene lacks the D-arm and fails to form a typical cloverleaf secondary structure, which is considered to be an ancestral characteristic of metazoan (Lowe and Chan, Reference Lowe and Chan2016). The 22 tRNA genes of D. steini (Longyan isolate) also have the trnC gene lacking the D-arm. Dermauw et al. considered the trnC gene lacking D-arm as a common ancestral characteristic of Mesostigmata (Acari: Parasitiformes) species (Dermauw et al., Reference Dermauw, Vanholme, Tirry and Van Leeuwen2010), but it has not been confirmed in the mitochondrial genome of ticks. The D. steini (Longyan isolate) tRNA gene underwent 9 G–U pairings and 3 U–U mismatches during the folding process. Compared with bacterial and cytoplasmic tRNA genes, mitochondrial tRNA genes contain more G–U pairing and mismatching, which is an important factor that makes mitochondrial tRNA genes less stable than cytoplasmic tRNA genes (Helm et al., Reference Helm, Brule, Friede, Giege, Puetz and Florenta2000). The G–U pairing and mismatches that occur on mitochondrial tRNA genes are highly conserved in evolution or involved in the formation of higher structures that can be corrected by RNA editing, and their normal transport function is not affected, which is important for maintaining the stability and specificity of tRNA genes (Kunzmann et al., Reference Kunzmann, Brennicke and Marchfelder1998; Helm et al., Reference Helm, Brule, Friede, Giege, Puetz and Florenta2000). It has been thought that mismatches in tRNA genes may be linked to species evolution (Watanabe et al., Reference Watanabe, Kawai, Yokogawa, Hayashi, Kumazawa, Ueda, Nishikawa, Hirao, Miura and Watanabe1994). Hence, whether the base mismatches occurring in the mitochondrial tRNA gene of D. steini (Longyan isolate) are related to its evolution needs to be further explored.

Geographic location is generally considered to be one of the factors influencing variation in the mitochondrial genome (Burnard and Shao, Reference Burnard and Shao2019). The overall variation among the mitochondrial genome sequences of D. steini (Longyan, Nanchang, Jinhua and Yingtan isolates) was 0.76%, which was less than 1%. It suggests that the variation in the mitochondrial genome of D. steini may be less affected by geographical location; it may also be due to the proximity (<1000 km) between the 4 locations (Longyan, Nanchang, Jinhua and Yingtan), which does not reflect the intra-species variation. The nucleotide and amino acid sequences of homologous genes as well as nucleotide diversity analysis showed that atp8 was the least conserved gene, which is consistent with the results of other tick species (Guo et al., Reference Guo, Zhang, Fu, Gao, Liu, Qiu, Chang and Wang2016). It further suggests that the atp8 gene can be used as an alternative genetic marker for studying D. steini from different host body surfaces and different biogeographies.

The altered gene order of the mitochondrial genome is a well-known specific molecular marker that contains important phylogenetic information (Boore, Reference Boore1999; Boore and Fuerstenberg, Reference Boore and Fuerstenberg2008). The study of mitochondrial genome rearrangement events is one of the hotspots for studying the evolutionary process of species. The mitochondrial genome arrangement is generally considered to be highly conserved at lower taxonomic levels (families and genera) and rearrangements occur much more frequently for short fragments than for long fragments (Dowton et al., Reference Dowton, Cameron, Dowavic, Austin and Whiting2009; Yuan et al. Reference Yuan, Wei, Wang, Dou and Wang2010). The mitochondrial genome rearrangements of species within the genus Dermacentor are relatively simple, not occurring in some very conserved regions (rrnL-trnV-rrnS), but all in 3 regions (nad1-trnL 2, trnI-trnQ-trnF and trnC). These 3 regions are located in the vicinity of the control region and tRNA genes. It has been demonstrated in the mitochondrial genomes of sucking lice, insects and mites that the control region and the vicinity of tRNA genes are the hotspot regions in which rearrangements occur (Wei et al., Reference Wei, Shi, He, Sharkey and Chen2009, Reference Wei, Shi, Sharkey, van Achterberg and Chen2010; Dong et al., Reference Dong, Dong, Guo and Shao2021). It has been suggested that replication of the control region is responsible for the accelerated frequency of mitochondrial gene rearrangements, as in Thrips and Corrodentia (Shao and Barker, Reference Shao and Barker2003; Shao et al., Reference Shao, Barker, Mitani, Aoki and Fukunaga2005; Yan et al., Reference Yan, Tang, Xue, Wang, Liu and Fan2012). It remains to be verified whether the accelerated frequency of mitochondrial genome rearrangements in ticks is related to the replication of control regions. The BI and ML trees indicate that the family Ixodidae is a monophyletic group and the phylogenetic relationships within the family are relatively clear. D. steini isolated from Longyan clustered with 3 other isolates (Nanchang, Jinhua and Yingtan), and then formed a sister branch with D. auratus with high node support. It indicates that among the genus Dermacentor, D. steini is most closely related to D. auratus. It may be related to the similarity of these 2 species in morphology and in the pathogens they carry. Two phylogenetic trees showed that the genus Dermacentor is most closely related to 2 genera (Rhipicentor and Hyalomma), which is consistent with previous studies (Burnard and Shao, Reference Burnard and Shao2019; Uribe et al., Reference Uribe, Nava, Murphy, Tarragona and Castro2020; Kelava et al., Reference Kelava, Mans, Shao, Moustafa, Matsuno, Takano, Kawabata, Sato, Fujita, Ze, Plantard, Hornok, Gao, Barker, Barker and Nakao2021). The analysis of the affinities of the genus Dermacentor facilitates the subsequent understanding of the phylogenetic analysis of species in the genus Dermacentor.

Conclusion

In this study, the complete mitochondrial genome of D. steini (Longyan isolate) parasitized on R. andamanensis was sequenced and compared with Nanchang, Jinhua and Yingtan isolates. The results showed that the mitochondrial genomes of D. steini different isolates were similar in length and the overall variation between sequences was less than 1%; the atp8 gene may serve as an alternative genetic marker for studying D. steini species from different hosts and biogeography; the mitochondrial genome underwent minor rearrangements. Phylogenetic analyses showed that the genus Dermacentor is most closely related to 2 genera (Rhipicentor and Hyalomma) in the family Ixodidae. The results enrich the mitochondrial genomic data of species in the genus Dermacentor and have important implications for the phylogeographic classification and molecular evolution of ticks.

Supplementary material

The supplementary material for this article can be found at https://doi.org/10.1017/S0031182022001639

Data availability

The complete mitochondrial genome sequence of D. steini is available at the National Center for Biotechnology Information (NCBI) at [https://www.ncbi.nlm.nih.gov/] under accession number OP383032.

Acknowledgements

We thank Gangxian He for his assistance in the initial formation of the circular mitochondrial genome map

Author's contributions

Huijuan Yang and Wenge Dong conceived and designed the study. Huijuan Yang and Ting Chen conducted data gathering. Huijuan Yang performed statistical analyses. Huijuan Yang and Ting Chen wrote the manuscript. Wenge Dong revised the manuscript.

Financial support

This work was supported by the National Natural Science Foundation of China [No. 32060143 to Wenge Dong] and Major Science and Technique Programs in Yunnan Province [No. 202102AA310055-X to Xianguo Guo].

Conflict of interest

The authors declare that they have no conflicts of interests.

Ethical standards

Small mammal capture protocols and procedures were approved by the Animal Ethics Committees at Dali University. The approval ID is MECDU-201806-11.

References

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Figure 0

Table 1. Dermacentor steini gene content, length, coding strand, initiation and stop codons of mitochondrial genomes of different isolate

Figure 1

Fig. 1. Dermacentor steini (Longyan isolate) tRNA gene putative secondary structure.

Figure 2

Fig. 2. Selection pressure analysis for different isolates in Dermacentor steini.

Figure 3

Table 2. Dermacentor steini variation in nucleotide and predicted amino acid sequences of the mitochondrial genome of different isolates

Figure 4

Fig. 3. Sliding window analysis of the complete mitochondrial genomes of Dermacentor steini different isolates. The black line indicates the nucleotide diversity values (Pi) in the sliding window analysis with a window size of 100 bp and a step size of 25; the gene boundaries are indicated by the variation rate of each gene.

Figure 5

Fig. 4. Mitochondrial genome rearrangement evolution in the genus Dermacentor. Green indicates translocations, blue indicates translocations and inversions.

Figure 6

Fig. 5. Phylogenetic analysis based on the nucleotide sequences of the 13 PCGs in the mitogenome. The numbers beside the nodes are posterior probabilities (BI) and bootstrap (ML) indicates the species in this study.

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