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Article

The Complete Mitogenome of the Wood-Feeding Cockroach Cryptocercus meridianus (Blattodea: Cryptocercidae) and Its Phylogenetic Relationship among Cockroach Families

by
Weijun Li
,
Zongqing Wang
and
Yanli Che
*
College of Plant Protection, Southwest University, Beibei, Chongqing 400716, China
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2017, 18(11), 2397; https://doi.org/10.3390/ijms18112397
Submission received: 23 September 2017 / Revised: 6 November 2017 / Accepted: 7 November 2017 / Published: 12 November 2017
(This article belongs to the Section Biochemistry)
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Abstract

:
In this study, the complete mitochondrial genome of Cryptocercus meridianus was sequenced. The circular mitochondrial genome is 15,322 bp in size and contains 13 protein-coding genes, two ribosomal RNA genes (12S rRNA and 16S rRNA), 22 transfer RNA genes, and one D-loop region. We compare the mitogenome of C. meridianus with that of C. relictus and C. kyebangensis. The base composition of the whole genome was 45.20%, 9.74%, 16.06%, and 29.00% for A, G, C, and T, respectively; it shows a high AT content (74.2%), similar to the mitogenomes of C. relictus and C. kyebangensis. The protein-coding genes are initiated with typical mitochondrial start codons except for cox1 with TTG. The gene order of the C. meridianus mitogenome differs from the typical insect pattern for the translocation of tRNA-SerAGN, while the mitogenomes of the other two Cryptocercus species, C. relictus and C. kyebangensis, are consistent with the typical insect pattern. There are two very long non-coding intergenic regions lying on both sides of the rearranged gene tRNA-SerAGN. The phylogenetic relationships were constructed based on the nucleotide sequence of 13 protein-coding genes and two ribosomal RNA genes. The mitogenome of C. meridianus is the first representative of the order Blattodea that demonstrates rearrangement, and it will contribute to the further study of the phylogeny and evolution of the genus Cryptocercus and related taxa.

Graphical Abstract

1. Introduction

Cryptocercus is a genus of woodroaches which occur in the high mountainous forests of temperate regions, specifically in the Nearctic, Palaearctic, and Oriental Regions, and feed on rotten wood in logs [1,2,3]. Their distributional pattern has been strongly affected by palaeogeographic events that influenced their source tree hosts, such as the appearance of land bridges and the uplift of mountains [4]. Additionally, Cryptocercus is regarded as a link between termites and Blattodea. Recent studies of phylogenetic relationships among Dictyoptera or Blattodea show that Cryptocercus is the sister group of termites [1,5,6,7,8]. Therefore this genus is an important model for elucidating the early stages of social evolution in termite eusociality [9].
Insect mitochondrial genomes, which tend to evolve faster than nuclear genes, are very useful for studies of evolutionary genomics and are widely used to discern the phylogenetic relationships at various taxonomic levels and the investigation of population structures [10,11]. Jeon & Park (2015) investigated the mitogenome of Cryptocercus kyebangensis and compared it with Cryptocercus relictus [12]. They found that C. kyebangensis has a close relationship with C. relictus and these two Cryptocercus species share the same mitochondrial gene order.
Cryptocercus meridianus is distributed in Lijiang, Yunnan Province, which is located in the Hengduan Mountains [13]. Che et al. (2016) indicated that C. meridianus forms a sister taxon relationship with the group of C. relictus from Northeast China and C. kyebangensis from Korea, but had a distant phylogenetic relationship with species in the Hengduan Mountains [1]. Given this situation, we sequenced the complete mitochondrial genome of C. meridianus and compared it with previously published mitogenomes of C. relictus (GenBank: JX144941) and C. kyebangensis (GenBank: KP872847). We compared the gene orders in these three members of the Cryptocercus genus and found a gene rearrangement in the mitogenome of C. meridianus. For phylogenetic analyses, we constructed phylogenetic trees based on 13 protein-coding genes and two rRNAs. In order to discern more accurate phylogenetic relationships and reduce systematic errors from compositional and mutational biases in insect mitochondrial genomes, we used a site-heterogeneous mixture model for Bayesian Inference. In addition, we removed the third codons of the 13 protein-coding genes as they are fast-evolving sites. Despite many studies that have attempted to clarify the phylogenetic analyses within Blattodea based on mitogenomes, the phylogenetic relationships are still unresolved. This is mainly because the mitogenomes of members of the order Blattodea are poorly published. Therefore, more mitogenomes of species in the order Blattodea are needed to be added in ongoing research to establish the phylogenetic relationships.

2. Results and Discussion

2.1. Mitogenome Organization and Nucleotide Composition

The complete mitochondrial genome of C. meridianus is found to be 15,322 bp in size, which is smaller than that of C. relictus (15,373 bp) and C. kyebangensis (15,720 bp), with an asymmetric nucleotide composition (45.20% A, 16.06% C, 9.74% G, and 29.00% T) and an AT bias (74.2%) (Table 1). The circular map of the C. meridianus mitogenome is shown in Figure 1, drawn by the software GenomeVx [14]. AT content of the C. meridianus mitogenome (74.2%) is slightly higher than that of C. relictus (73.5%) and slightly lower than in C. kyebangensis (74.4%). Similar to other insects, it is a circular double-stranded molecule, which contains a typical set of 13 protein-coding genes (PCGs), 22 transfer RNA genes (tRNAs), two ribosomal RNA genes (rRNAs) and a large non-coding region (A + T rich region or D-loop region) [15,16]. For the whole mitochondrial genome of C. meridianus, four PCGs (nad5, nad4, nad4L and nad1), eight tRNAs (tRNA-Gln, -Cys, -Tyr, -Phe, -His, -Pro, -LeuCUN, and -Val) and two rRNAs (12S and 16S) are encoded on the light strand, while all the other genes are on the heavy strand [17]. In comparison with C. relictus and C. kyebangensis, the location of tRNA-SerAGN is quite different in the mitochondrial genome of C. meridianus, where it is located between nad3 and tRNA-Ala, while in the other two species the tRNA-SerAGN gene is located between tRNA-Asn and tRNA-Glu. The annotation of the whole mitogenome is shown in Table 2. In addition, there are three unusual non-coding sequences inserted along with the mitochondrial gene rearrangement.
AT and GC skews of the mitochondrial gene regions are approximately the same among the three Cryptocercus species, but the D-loop regions seem to be an exception. In the D-loop region, the AT skew value of C. meridianus (0.37) is much higher than that of C. relictus (0.15) and C. kyebangensis (0.27), and the GC skew value of C. meridianus (−0.52) is much weaker than that of C. relictus (−0.09) and C. kyebangensis (−0.33) (Table 3).f

2.2. PCGs (Protein-Coding Genes)

The total size of the 13 mitochondrial protein-coding genes (PCGs) of C. meridianus is 11,190 bp, which can be translated into 3720 amino acid residues, with the exception of stop codons (30 bp). Compared to C. kyebangensis and C. relictus, the total number of the C. meridianus mitochondrial amino acid residues is two more than C. kyebangensis and C. relictus. Further analysis shows differences in the number of mitochondrial amino acid residues that were found in nad3 and nad1; the C. meridianus mitogenome encodes one amino acid residue more than C. kyebangensis and C. relictus in nad3 and one amino acid residue less than them in nad1.
There are four kinds of start codons (ATG, ATA, ATT, and TTG) included in the mitogenome of C. meridianus. The nad5 gene is initiated with the GTG codon in the mitochondrial genome of C. kyebangensis while it is ATG in C. meridianus and C. relictus. Generally, there are three kinds of stop codons (TAA, TA*, T**) for translation termination. The C. meridianus mitogenome is no exception; for the incomplete stop codons, the missed nucleotides may result from post-transcriptional polyadenylation [18]. As the TAA stop codon is completed by the addition of 3′ A residues to the mRNA, the PCG nad3 harbors the incomplete stop codon TA* in the mitochondrial genome of C. relictus while TAA occurs in the other two Cryptocercus species. The other PCGs except nad3 use the same stop codons among the mitochondrial genomes of three Cryptocercus species.
Relative synonymous codon usage (RSCU) was analyzed in the mitochondrial genomes of the three Cryptocercus species (Figure 2). In the mitochondrial protein-coding genes of the three Cryptocercus species, SerUCN (S2) was most commonly used in all three Cryptocercus species. Furthermore, analysis of the RSCU values for the 13 protein-coding genes indicated an A + T bias [19]. As for protein-coding genes, the A + T bias can be responsible for the frequent use of NNA and NNU (N repesents A, T, C, G) codons. The A + T content of C. kyebangensis was slightly higher than in the other two, and the usage of NNA and NNU codons of C. kyebangensis was also higher than in the other two Cryptocercus species.
The average Ka/Ks ratios were calculated for each PCG of the three Cryptocercus mitogenomes (Figure 3). It shows that atp8 has the highest evolutionary rate, followed by nad6. cox1 had the lowest.

2.3. The tRNA Genes and rRNA Genes

The 22 tRNA genes range from 62 to 70 bp in size, and the total length of the 22 C. meridianus mitogenome tRNA genes was 1450 bp, which is the same as in C. relictus and only one-base different from C. kyebangensis. The AT content of the total C. meridianus mitogenome transfer RNA genes is 74.9%, which is higher than in C. relictus (74.4%) and C. kyebangensis (74.6%) (Table 2). Most tRNA sequences can fold into the typical cloverleaf secondary structure [20]. The translocation of tRNA-SerAGN is shown in Figure 4. Furthermore, tRNA-Ser and tRNA-Leu are in double copies, while all the others only have one single copy.
The two rRNA genes of C. meridianus’ mitogenome are 777 bp (12S) and 1283 bp (16S) in size, respectively.

2.4. The D-Loop Region

The D-loop region is located between tRNA-Ile and the 12S gene, which includes the origin sites for transcription and replication [21] and is the control region of the mitochondrial genome. It is found to be 240 bp in size. This region is often the main source of variation in genome length [22], as the non-coding sequences in the D-loop are more prone to mutation [23]. There exists a divergence among the D-loop region sizes in the three Cryptocercus species. The D-loop region size of C. meridianus is much smaller than that of C. relictus (672 bp) and C. kyebangensis (1009 bp), so it can be inferred that the mutation rate of the D-loop region in the mitochondrial genome of Cryptocercus meridianus is lower than in the other two Cryptocercus species, as the mutational region of the former is much shorter than the latter two. In the three Cryptocercus species, the AT content of the D-loop region is higher than that of other genes (Table 2): 77.5% in C. meridianus D-loop region, which is lower than that of C. relictus (80.3%) and C. kyebangensis (80.2%). In addition, we also found a 31 bp relatively conserved sequence in the D-loop regions of all three Cryptocercus species (Figure S1).

2.5. Intergenic Spacer and Overlapping Regions

The total length of C. meridianus mitogenome intergenic spacer regions is 414 bp [24], which is much larger than that of C. relictus (32 bp) and C. kyebangensis (31 bp). There are three long intergenic spacer regions, which are also called non-coding regions. One is located between tRNA-SerAGN and tRNA-Ala (174 bp); another is located between nad3 and tRNA-SerAGN (147 bp); and the third is located between tRNA-Asn and tRNA-Glu (62 bp). These three long spacer regions contribute to the unusually large whole intergenic spacer region of the C. meridianus mitochondrial genome. In addition, the AT content of these three intergenic spacer regions is higher than in other mitogenome genes. There are seven intergenic overlapping regions ranging from 1 to 8 bp in length, fewer than in C. relictus and C. kyebangensis, with the latter two having eight intergenic overlapping regions ranging from 1 to 8 bp. The longest overlapping region is consistently located between tRNA-Trp and tRNA-Cys in the three species.

2.6. Rearrangement

Generally, animal mitochondrial genomes have relatively conserved gene arrangements and stable gene content. Although their mitochondrial sequences evolve rapidly over long periods of evolution, their gene arrangements often remain unchanged [25]. With more and more sequences of mitochondrial DNA molecules of insect species being determined [26], the issue of rearrangement of insect mitochondrial genomes has become a focus of more research.
So far, mitochondrial gene rearrangement has been reported as occurring in many insect species, but Blattodea seems to be an exception. C. meridianus is the first species where mitochondrial gene rearrangement has been found in the Blattodea, due to a translocation of tRNA-SerAGN. The mitochondrial gene arrangement of the model organism, Drosophila, was considered to be the insect pattern formula; while C. relictus and C. kyebangensis follow this rule, C. meridianus does not. The location of tRNA-SerAGN is between the nad3 and tRNA-Ala genes in the mitochondrial genome of C. meridianus, but in the other two Cryptocercus species mitogenome tRNA-SerAGN genes are located between the tRNA-Asn and tRNA-Glu genes. The secondary structure of tRNA-SerAGN gene of C. meridianus is shown in Figure 5, and the secondary structure of 22 tRNA genes can be seen in Figure S2. Compared with other tRNA genes of C. meridianus, the Anticodon arm of tRNA-SerAGN is shorter, the Variable loop is longer and it lacks DHU arm. These features contribute to the unstable structure of tRNA-SerAGN.

2.7. Phylogenetic Analyses

For the concatenated datasets (PCGR, PCG12R), phylogenetic analyses yielded essentially identical topologies with relatively high support values except for the inner relationship of the group Blaberidae across the topologies for standard Maximum likelihood (ML) and Bayesian inference (BI) analysis using site-homogenous models and Bayesian (PhyloBayes) analyses under site-heterogeneous models. Three recognized major lineages of Blattodea from all inferences were: Corydioidea, Blattoidea, and Blaberoidea, with high support values. AliGROOVE found slight heterogeneity in sequence divergence for a subset of 32 taxa (Figure S3).
In this study, the topologies of phylogenetic trees are always stable regardless of ingroup change. All datasets show a monophyletic clade containing Cryptocercidae and Isoptera with Blattidae as the sister group of their formed branch (Figure 6). Blaberidae is the sister group of Ectobiidae. Cryptocercus relictus is a sister group of Cryptocercus kyebangensis. Cryptocercus meridianus is well supported as the sister group of (Cryptocercus relictus + Cryptocercus kyebangensis). This work was based on several mitogenomes published to date and presents a stable phylogeny of Cryptocercidae and other related lineages. More complete mitogenomes are needed to better reconstruct phylogeny within Blattodea in the future.
The mitogenome of Cryptocercus meridianus shows many common features observed in other Cryptocercus species, such as AT bias, truncated stop codons, and codon usage. They have the same genome structure which contains 22 tRNA, 13 protein-coding genes (PCGs) and 2 rRNA. The length variation of D-loop regions is the main cause for the diversity of whole genome size; moreover, as for C. meridianus, some extra non-coding regions located in nad3~nad5 also contribute to the genome size variation.
Generally speaking, mitochondrial gene arrangement is stable within major animal lineages [25], however this is not the case for Cryptocercus. C. meridianus is the first representative of the order Blattodea that demonstrates mitochondrial gene rearrangement, but as this species is poorly sampled, there may be more cases of mitochondrial gene rearrangement in this group. Most probably, the translocation of tRNA-SerAGN led to this rearrangement, potentially enabled by the presence of two unconventionally long intergenic spacers on both sides of the tRNA-SerAGN gene; this phenomenon is similar to that found in Hymenoptera [27]. In hymenopteran mitochondrial genomes, overlapping genes rarely are involved in rearrangement, and those rearranged genes usually have intergenic regions on both sides. This kind of rearrangement would be gene shuffling, which means that a rearranged gene moves closely on the same strand while never crossing PCGs nearby. Several mechanisms involving the mitochondrial gene have been put forward [28,29,30,31,32,33]. One of the soundest mechanisms suited to explain this phenomenon is described by the duplication-random loss theory; that is, the slipped-strand mispairing took place first [34] and then gene deletions led to the resulting phenomenon.
Figure 6 shows the results of the six phylogenetic analyses. These results are consistent with the work of Cheng et al. [20] on the sister groups of (Blaberidae + Ectobiidae), but the internal topologies of Blaberidae are heterogeneous among the six analyses. In this section, only the node of sister group (Panchlota nivea + Blaptica dubia) are stable in these six analyses, but with relatively low support values; the other two nodes are absent in some analyses. In addition, there exists some differences in the clade of Corydiidae: our work indicates the relationship as (Corydiidae + (Blattidae + (Cryptocercidae + Isoptera))), while Cheng et al. [20] report the relationship as (Corydiidae + (Cryptocercidae + Isoptera) + (Blattidae + (Ectobiidae + Blaberidae))). These conflicts may be explained by the choice of taxa used to construct phylogenetic trees, as this result may be due to the lack of key taxon. Currently, published mitogenomes of Blattodea are very scarce, so more mitogenomes of members of the Blattodea should be sequenced to better elucidate these phylogenetic relationships.

3. Materials and Methods

3.1. Sampling and DNA Extraction

Specimens of Cryptocercus meridianus were collected from Lijiang (27.08° N; 100.14° E), Yunnan Province in the Yulong Mountain region of Southwest China. Our study activities were not banned by any organization or individual and did not involve protected or endangered species. Voucher specimens of C. meridianus were deposited in the Institute of Entomology, Southwest University (SWU), Chongqing. Specimens of Cryptocercus meridianus were preserved in 100% ethanol and stored at −80 °C. Total genomic DNA was extracted from fresh muscle of one leg using the TIANamp Genomic DNA Kit (DP304, TIANGEN, Beijing, China) according to the manufacturer’s protocol.

3.2. PCR Amplification, Sequencing and Sequence Assembly

The primers used in this study were referred from [35], which are universal for Cryptocercus species. All primers used in this study are provided in Table S1. All reactions were carried out in volumes of 25 µL, containing 14.25 µL of ultrapure water, 2.5 µL of 10× buffer (Mg2+ Free), 2 µL of MgCl2 (25 mM), 2 µL of dNTP mixture, 1 µL of each primer, 0.25 µL of Taq polymerase, and 2 µL of DNA template. The concentration of Taq stock solutions is 5 units/µL, the primers and dNTPs are 0.5 and 200 µM respectively. The following steps were performed on a programmable thermal cycler. The amplification protocol settings used are: 94 °C for 5 min; followed by 35 cycle 94 °C for 45 s, 48 °C for 45 s, and 72 °C for 45 s; and final extension at 72 °C for 10 min. PCR products were examined by electrophoresis on a 1% agarose gel to confirm PCR availability, and then sequenced via primer walking by BGI Tech (Beijing, China). In addition, the complete mitochondrial genome of C. meridianus was also sent for high-throughput sequencing with the Illumina Hiseq 2500 platform by Personal Biotechnology Company, Shanghai, China. Overlapping nucleotide sequences were assembled using SeqMan (DNAStar) and mitoMaker software (http://sourceforge.net/projects/mitomaker/).

3.3. Sequence Analysis

The complete mitogenome of Cryptocercus meridianus was annotated on the Mitos Web Server (http://mitos.bioinf.uni-leipzig.de/index.py). Then 22 transfer RNA genes were identified by tRNA scan-SE Search Server V.1.21 [36] and ARWEN (online version) [37]. The protein-coding and rRNA genes were inferred based on alignment with other two Cryptocercus mitogenomes and BLAST 2.6.0 searches against the GenBank database (https://blast.ncbi.nlm.nih.gov/Blast.cgi). The base composition and relative synonymous codon usage (RSCU) were calculated using MEGA 5 [38]. The average values of Ka/Ks across the three Cryptocercus species’ pairwise comparisons were calculated by DNASP v.5.0 with Genetic code = mtDNA Drosophila [39]. The overlapping regions and intergenic spacers between genes were counted manually as in [40]. AT/GC skew analyses were carried out respectively with the formulas AT skew = [A − T]/[A + T] and GC skew = [G − C]/[G + C] [41].

3.4. Phylogenetic Analysis

To infer the phylogenetic relationships within Dictyoptera, the newly generated mitogenomes and previously reported mitogenome sequences from families of cockroaches and other orders were used to reconstruct phylogenetic trees (Table 4). The phylogenetic tree was rooted using Parafronurus youi (Insecta: Ephemeroptera) [42], which is shown to have the farmost genetic relationship with other lineages. Each protein-coding gene was aligned individually based on codon-based multiple alignments by using the MAFFT algorithm implemented in TranslatorX with the L-INS-i strategy [43]. Two rRNA genes were individually aligned using the MAFFT 7.0 online server with the G-INS-I strategy [44]. We generated two datasets of each running, (1) PCGR matrix, including all three codon positions of protein-coding genes and two rRNA genes; and (2) PCG12R matrix, excluding the third codon position of protein-coding genes and two rRNA genes. The two datasets were divided by codon positions within each gene, resulting in 41 partitions (first codon positions, second codon positions, third codon positions of 13 protein-coding genes and two rRNAs genes) and 28 partitions (first codon positions, second codon positions of 13 protein-coding genes and two rRNAs genes) respectively. Phylogenetic analyses were performed using maximum likelihood (ML) and Bayesian inference (BI) methods. ML analyses were implemented using RAxML 7.3.0 [45], and BI analyses were implemented using MrBayes 3.2 [46]. For ML analyses, as the software does not allow different substitution models for different partitions, node reliability was estimated using the GTRGAMMA model with 1000 bootstrap replicates. For BI analyses, we determined the best-fit model for each partition with PartitionFinder v1.1.1 [47] (more details in Table S2). Two independent sets of Markov chains were run simultaneously [48], each with one cold and three heated chains for 10,000,000 generations; trees were sampled every 1000th generation and the first 25% of the generations were discarded as burn-in, the remaining samples were used to construct the consensus tree and Bayesian posterior probabilities (BPP). Convergence was inferred when a standard deviation of split frequencies <0.01 was presented. In our RAxML and MrBayes settings, the clustered partitions are totally based on the PartitionFinder result, and the best partitioning scheme can be seen in Table S2.
The heterogeneity of sequence divergence within different datasets was analyzed using AliGROOVE with the default sliding window size [66], and indels of nucleotide datasets were treated as ambiguity and the BLOSUM62 matrix was used as a default amino acid substitution matrix. The obtained scoring distance between sequences in a dataset is then compared with similarity. Values can vary between −1 if comparisons have full random similarity to +1 for comparisons that have totally non-random similarity. This provides an indirect measure of heterogeneity of a given sequence or clade with respect to the full data set [67].
To reconstruct more reasonable and responsible phylogenetic trees and suppress the systematic errors from base compositional and sequence mutational biases in all mitogenomes used in this study, we used PhyloBayes MPI to analyze the phylogenetic relationships based on the site-heterogeneous mixture models (CAT and CAT + GTR) [68]. Similar to the previous analyses, we analyzed two datasets using PhyloBayes each time we added or reduced insect taxa. In each individual analysis, two independent chains starting from a random tree were run for 20,000 cycles, and trees were sampled at each cycle (for more details, see PhyloBayes manual), the result shows that maxdiff = 0.216667 and meandiff = 0.0109477.

4. Conclusions

The mitogenome of C. meridianus is the first representative of the order Blattodea that exhibits rearrangement. Since mitochondrial gene rearrangements appear to be unique, the rearrangement of the C. meridianus mitochondrial gene would be helpful for our further understanding of the phylogeny and evolution of the genus Cryptocercus and related species. The result of phylogenetic study shows a little difference from previous studies based on mitochondrial genomes of species in Blattodea, so more data should be added in order to rebuild the phylogenetic relationships among the Blattodea.

Supplementary Materials

Supplementary materials can be found at www.mdpi.com/1422-0067/18/11/2397/s1.

Acknowledgments

We give our thanks to Qikun Bai and Shulin He for their fieldwork collecting samples. We also thank John Richard Schrock (Department of Biological Sciences, Emporia State University) for revising the manuscript. This research was funded by the National Natural Sciences Foundation of China (No. 31672329) and the Natural Science Foundation Project of Chongqing (No. cstc2016jcyjA0487).

Author Contributions

Weijun Li performed the experiments; Weijun Li, Zongqing Wang, and Yanli Che assembled sequences and analyzed the data; Weijun Li wrote the manuscript. All authors have read and approved the final manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

atp6ATPase subunit 6
atp8ATPase subunit 8
cox1-3cytochrome c oxidase subunit I-III
cytbcytochrome b
nad1-6, 4LNADH dehydrogenase subunit 1-6, 4L
PCGsprotein-coding genes
tRNAtransfer RNA genes
rRNAribosomal RNA genes
12/16Ssmall and large subunit of ribosomal RNA genes
MLmaximum likelihood analyses
BIbayesian inference analyses
RSCUrelative synonymous codon usage
IGSintergenic spacer region
BPPbayesian posterior probabilities

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Ijms 18 02397 g001 550
Figure 1. Genetic map of the complete mitochondrial genome of C. meridianus. The genes are abbreviated as follows: nad1, 2, 3, 4, 4L, 5, 6 refer to nicotinamide adenine dinucleotide subunit; cox1, 2, 3 refer to cytochrome oxidase subunit; 16S refers to large subunit of ribosomal RNA gene, 12S refers to small subunit of ribosomal RNA gene; atp6, 8 refer to ATP synthase F0 subunit; cytb refers to cytochrome B. tRNAs are red colored, protein coding genes (PCGs) are green colored, rRNAs are purple colored. Genes on the light strand are encoded in clockwise orientation; genes on the heavy strand are encoded in anti-clockwise orientation.
Figure 1. Genetic map of the complete mitochondrial genome of C. meridianus. The genes are abbreviated as follows: nad1, 2, 3, 4, 4L, 5, 6 refer to nicotinamide adenine dinucleotide subunit; cox1, 2, 3 refer to cytochrome oxidase subunit; 16S refers to large subunit of ribosomal RNA gene, 12S refers to small subunit of ribosomal RNA gene; atp6, 8 refer to ATP synthase F0 subunit; cytb refers to cytochrome B. tRNAs are red colored, protein coding genes (PCGs) are green colored, rRNAs are purple colored. Genes on the light strand are encoded in clockwise orientation; genes on the heavy strand are encoded in anti-clockwise orientation.
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Figure 2. Relative synonymous codon usage (RSCU) for protein coding genes of the three Cryptocercus mitochondrial genomes. Codon families are provided on the x-axis.
Figure 2. Relative synonymous codon usage (RSCU) for protein coding genes of the three Cryptocercus mitochondrial genomes. Codon families are provided on the x-axis.
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Ijms 18 02397 g003 550
Figure 3. Average Ka/Ks ratios of 13 protein-coding genes. Ka/Ks is the ratio of non-synonymous substitutions rate (Ka) to synonymous substitutions rate (Ks).
Figure 3. Average Ka/Ks ratios of 13 protein-coding genes. Ka/Ks is the ratio of non-synonymous substitutions rate (Ka) to synonymous substitutions rate (Ks).
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Ijms 18 02397 g004 550
Figure 4. Partial mitochondrial gene arrangements of the three Cryptocercus species along with insect typical pattern. The translocation of tRNA-Ser1 caused the mitochondrial gene rearrangement of C. meridianus, tRNA-Ser1 refers to tRNA-SerAGN. Genes are not drawn to scale but are arranged practically. Three blank areas refer to unusually long intergenic spacer regions which only occur in the mitogenome of C. meridianus. Genes underlined are encoded on the light strand.
Figure 4. Partial mitochondrial gene arrangements of the three Cryptocercus species along with insect typical pattern. The translocation of tRNA-Ser1 caused the mitochondrial gene rearrangement of C. meridianus, tRNA-Ser1 refers to tRNA-SerAGN. Genes are not drawn to scale but are arranged practically. Three blank areas refer to unusually long intergenic spacer regions which only occur in the mitogenome of C. meridianus. Genes underlined are encoded on the light strand.
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Figure 5. Inferred secondary structure of several tRNA genes for C. meridianus.
Figure 5. Inferred secondary structure of several tRNA genes for C. meridianus.
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Ijms 18 02397 g006 550
Figure 6. Phylogenetic relationships of major lineages within Blattodea and termites inferred from the concatenated protein-coding genes and ribosomal RNA genes, with the third codon position included (PCGR) and excluded (PCG12R). Branch labels are support for the six analyses in the following order: Bayesian posterior probabilities (BPP) of the Bayesian trees inferred from the dataset PCGR and PCG12R using site-homogeneous models; Bootstrap supports of the maximum-likelihood trees inferred from the dataset PCGR and PCG12R; and Bayesian posterior probabilities (BPP) of the Bayesian trees inferred from the dataset PCGR and PCG12R using site-heterogeneous mixture models. (*) indicates 100% support value for all six analyses. (-) indicates that the node is absent for the corresponding analysis. (▲) indicates BPP below 0.95.
Figure 6. Phylogenetic relationships of major lineages within Blattodea and termites inferred from the concatenated protein-coding genes and ribosomal RNA genes, with the third codon position included (PCGR) and excluded (PCG12R). Branch labels are support for the six analyses in the following order: Bayesian posterior probabilities (BPP) of the Bayesian trees inferred from the dataset PCGR and PCG12R using site-homogeneous models; Bootstrap supports of the maximum-likelihood trees inferred from the dataset PCGR and PCG12R; and Bayesian posterior probabilities (BPP) of the Bayesian trees inferred from the dataset PCGR and PCG12R using site-heterogeneous mixture models. (*) indicates 100% support value for all six analyses. (-) indicates that the node is absent for the corresponding analysis. (▲) indicates BPP below 0.95.
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Table
Table 1. Size, AT content (%) for C. meridianus, C. relictus, and C. kyebangensis mitogenomes.
Table 1. Size, AT content (%) for C. meridianus, C. relictus, and C. kyebangensis mitogenomes.
GeneC. meridianusC. relictusC. kyebangensis
Size (bp)A + T (%)Size (bp)A + T (%)Size (bp)A + T (%)
PCGs11,18673.311,18372.511,18473.4
tRNAs145074.9145074.4145174.6
rRNAs206076.2206375.8206776.5
D-loop24077.567280.3100980.2
Genome15,32274.215,37373.515,72074.4
Table
Table 2. Annotation of the complete mitogenome of Cryptocercus meridianus.
Table 2. Annotation of the complete mitogenome of Cryptocercus meridianus.
Gene NameStrandLocationSize (bp)IGSAnticodonStart/Stop Codon
tRNA-IleH1–6565 GAT
tRNA-GlnL64–13269−2TTG
tRNA-MetH140–205667CAT
nad2H206–123310280 ATG/TA*
tRNA-TrpH1234–1299660TCA
tRNA-CysL1292–135564−8GCA
tRNA-TyrL1356–1424690GTA
cox1H1429–296415364 TTG/TAA
tRNA-LeuUURH2967–3032662TAA
cox2H3033–37176850 ATA/T**
tRNA-LysH3718–3787700CTT
tRNA-AspH3788–3849620GTC
atp8H3850–40081590 ATT/TAA
atp6H4002–4682681−7 ATG/TAA
cox3H4682–5470789−1 ATG/TAA
tRNA-GlyH5475–5538644TCC
nad3H5536–5892357−3 ATA/TAA
tRNA-SerAGNH6040–610869147GCT
tRNA-AlaH6283–634765174TGC
tRNA-ArgH6348–6410630TCG
tRNA-AsnH6414–6478653GTT
tRNA-GluH6541–66046462TTC
tRNA-PheL6605–6671670GAA
nad5L6672–840017290 ATG/T**
tRNA-HisL8401–8464640GTG
nad4L8467–980713412 ATG/TAA
nad4LL9801–10,088288−7 ATG/TAA
tRNA-ThrH10,093–10,157654TGT
tRNA-ProL10,158–10,221640TGG
nad6H10,224–10,7214982 ATT/TAA
cytbH10,724–11,85511322 ATG/T**
tRNA-SerUCNH11,856–11,923680TGA
nad1L11,920–12,886967−4 ATG/T**
tRNA-LeuCUNL12,888–12,954671TAG
16SL12,955–14,23712830
tRNA-ValL14,238–14,305680TAC
12SL14,306–15,0827770
D-loop 15,083–15,3222400
H/L indicates that the gene is encoded on the heavy/light strand, while D-loop region is non-coding. T** or TA* represents incomplete stop codons. Intergenic spacer region (IGS) denotes the length of the intergenic spacer region, for which positive numbers/negative numbers indicate intergenic/overlapping regions between adjacent genes.
Table
Table 3. AT skew and GC skew of C. meridianus, C. relictus and C. kyebangensis mitogenomes.
Table 3. AT skew and GC skew of C. meridianus, C. relictus and C. kyebangensis mitogenomes.
GeneC. meridianusC. relictusC. kyebangensis
AT SkewGC SkewAT SkewGC SkewAT SkewGC Skew
PCGs0.22−0.230.24−0.230.23−0.23
tRNAs0.12−0.160.15−0.160.14−0.15
rRNAs0.29−0.360.30−0.340.31−0.34
D-loop0.37−0.520.15−0.090.27−0.33
Genome0.22−0.250.23−0.230.24−0.24
Table
Table 4. GenBank accession numbers of taxa used to reconstruct phylogenetic trees.
Table 4. GenBank accession numbers of taxa used to reconstruct phylogenetic trees.
OrderSpeciesAccession NumberReference
EphemeropteraParafronurus youiEU349015[42]
OdonataBrachythemis contaminataNC_026305[49]
MantophasmatodeaSclerophasma paresisenseNC_007701[50]
OrthopteraDeracantha onosEU137664[51]
Physemacris variolosaNC_014491[52]
Atractomorpha sinensisNC_011824[53]
PlecopteraKamimuria wangiKC894944[54]
PhasmatodeaBacillus rossiusGU001956[55]
Heteropteryx dilatataAB477468[56]
MantodeaTamolanica tamolanaNC_007702[35]
Leptomantella albellaNC_024028[57]
IsopteraMastotermes darwiniensisNC_018120[35]
Microhodotermes viatorNC_018122[35]
Neotermes insularisNC_018124[35]
Zootermopsis nevadensisNC_024658[58]
Zootermopsis angusticollisNC_018123[35]
Macrotermes natalensisNC_025522[59]
Coptotermes formosanusAB626147[60]
Porotermes adamsoniNC_018121[35]
BlattodeaCryptocercus meridianusMG518617this study
Cryptocercus relictusNC_018132[35]
Cryptocercus kyebangensisKP872847[12]
Blattella germanicaNC_012901[61]
Eupolyphaga sinensisNC_014274[62]
Blattella bisignataNC_018549[63]
Periplaneta americanaNC_016956[61]
Periplaneta fuliginosaAB126004[64]
Opisthoplatia orientalisKT893460[65]
Panchlota niveaKU684412[20]
Shelfordella lateralisKU684413[20]
GromphadorhinaKU684411[20]
portentosa
Blaptica dubiaKU684410[20]

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Li, W.; Wang, Z.; Che, Y. The Complete Mitogenome of the Wood-Feeding Cockroach Cryptocercus meridianus (Blattodea: Cryptocercidae) and Its Phylogenetic Relationship among Cockroach Families. Int. J. Mol. Sci. 2017, 18, 2397. https://doi.org/10.3390/ijms18112397

AMA Style

Li W, Wang Z, Che Y. The Complete Mitogenome of the Wood-Feeding Cockroach Cryptocercus meridianus (Blattodea: Cryptocercidae) and Its Phylogenetic Relationship among Cockroach Families. International Journal of Molecular Sciences. 2017; 18(11):2397. https://doi.org/10.3390/ijms18112397

Chicago/Turabian Style

Li, Weijun, Zongqing Wang, and Yanli Che. 2017. "The Complete Mitogenome of the Wood-Feeding Cockroach Cryptocercus meridianus (Blattodea: Cryptocercidae) and Its Phylogenetic Relationship among Cockroach Families" International Journal of Molecular Sciences 18, no. 11: 2397. https://doi.org/10.3390/ijms18112397

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