Research Article
The complete mitochondrial genome of Meloe proscarabaeus (Coleoptera, Meloidae): genome descriptions and phylogenetic inferences
Song Chen‡,
Changhua Liu‡,
Yuanmin Hao‡,
Yueyue Liu§,
Xu Liu‡,
Chao Du|
‡ Institute of Plant Protection, Sichuan Academy of Agricultural Sciences, Chengdu, China
§ Institute of Quality Standard and Testing Technology Research, Sichuan Academy of Agricultural Sciences, Chengdu, China
| Baotou Teachers College, Baotou, China
Corresponding author:
Xu Liu
(
liuxu6186@126.com
)
Corresponding author:
Chao Du
(
ductub@163.com
)
Academic editor: Warren Steiner
© 2022 Song Chen, Changhua Liu, Yuanmin Hao, Yueyue Liu, Xu Liu, Chao Du. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Chen S, Liu C, Hao Y, Liu Y, Liu X, Du C (2022) The complete mitochondrial genome of Meloe proscarabaeus (Coleoptera, Meloidae): genome descriptions and phylogenetic inferences. ZooKeys 1109: 103-114. https://doi.org/10.3897/zookeys.1109.81544
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Abstract
Oil beetles are meloids, which are characterised for their cleptoparasitic habits in bee nests and oily fluid of cantharidin that causes blistering and swelling of the skin. The complete mitochondrial genome of Meloe proscarabaeus is determined using the next-generation sequencing technology and its genomic characteristics are described. The 15,653-bp long genome is a circular molecule consisting of 13 protein-coding genes (PCG), 22 transport RNA, two ribosomal RNA, and a control region. The A + T bias of the mitochondrial genome is manifested in the complete sequence and the codon usage of protein-coding genes. The genetic distance within and between genera is calculated to confirm the taxonomic status of M. proscarabaeus. The phylogenetic relationships among 15 available meloid taxa are inferred by the maximum likelihood (ML) method based on 13 mitochondrial PCGs. The ML trees resulting from nucleotide and amino acid datasets recover both the monophyly of Meloe and Epicauta and the polyphyly comprising Hycleus and Mylabris. This study provides the first description of a mitochondrial genome belonging to the genus Meloe. The mitochondrial genome sequence and its characteristics are expected to be conducive to future studies on taxonomy, systematics, and molecular phylogenetics of the family Meloidae.
Keywords
Genome feature, meloid, mitogenome, oil beetle, phylogenetic relationship
Introduction
The oil beetle Meloe proscarabaeus Linnaeus, 1758 is a characteristic species of the meloid genus Meloe Linnaeus, 1758, which comprises about 155 species in 16 subgenera and is mainly distributed in the Holarctic region (Sánchez-Vialas et al. 2021; Pan and Bologna 2021). Oil beetles are well known for the oily fluid of hemolymph released from their leg joints, which contains the poison cantharidin that causes blistering and swelling of the skin (Muzzi et al. 2020; Du et al. 2021). Additionally, oil beetles are distinguished by their hypermetamorphic development and cleptoparasitic habits in bee nests (Saul-Gershenz and Millar 2006; Saul-Gershenz et al. 2018).
The taxonomy and phylogeny of the genus Meloe are based on morphological characteristics and molecular data (Di Giulio et al. 2002, 2014; Muzzi et al. 2020; Pan and Bologna 2021; Sánchez-Vialas et al. 2021). The genus is considered monophyletic, but more detailed molecular phylogenetic studies are necessary to solve the phylogenetic relationships within the genus. With the simple genetic structure, the high rate of evolution, and the advantage in acquiring methods, the mitochondrial genome has been used widely in many phylogenetic studies of animals (Avise 1994; Cameron 2014; Du et al. 2020). There are 15 meloid species in five genera that have had their complete mitochondrial genomes published in the GenBank database. Previous studies have utilised mitochondrial genome sequences to infer the phylogeny of Meloidae, but without data on the genus Meloe due to the absence of mitochondrial genomes for the genus (Du et al. 2017; Liu et al. 2020).
In this study, we determine the complete mitochondrial genome of M. proscarabaeus using next-generation sequencing, and we describe its genomic characteristics. Furthermore, we reconstruct the phylogenetic trees based on the nucleotide and amino acid sequences from all available mitochondrial genomes to analyse the phylogenetic relationships among the family Meloidae. The sequence and phylogenetic inferences of M. proscarabaeus mitochondrial genome will be a significant increase in furthering the study on coleopteran mitochondrial genome architecture and phylogenetics.
Materials and methods
Sample and genomic DNA extraction
The adults of Meloe proscarabaeus were collected from a hill slope in Dongsheng, Inner Mongolia, China (39°45.33'N, 110°01.83'E). The fresh samples were immediately preserved in 100% ethanol and stored in a −20 °C refrigerator. We identified the specimens according to the morphological characters that descried by Pan and Bologna (2021). Total genomic DNA was extracted from a frozen adult using Tianamp Genomic DNA kit following the manufacturer’s protocol. The quality of DNA was determined using 1% agarose gel electrophoresis.
Next-generation sequencing and genomic assembly
The library was constructed using an Illumina TruSeq Library Preparation kit with an insert size of 250 bp and sequenced using the paired-end strategy on an Illumina HiSeq 2500 platform. A total of 4.4 Gb raw data was yielded with an average read length of 150 bp. The raw data were trimmed and filtered using fastp with parameters of phred quality ≥ 30 and unqualified percent < 20 to remove adapters and low-quality reads (Chen et al. 2018). Then the clean data were used to assemble the mitochondrial genome of M. proscarabaeus by MITObim v. 1.9.1 with the default settings (Hahn et al. 2013). The mitochondrial genome of Lytta caraganae (GenBank accession number NC_033339.1; Du et al. 2017) was employed as a reference sequence. The assembled sequence was aligned with other meloid mitochondrial genomes described by Du et al. (2017) to ensure the assembling quality.
Gene annotation and sequence analysis
The complete mitochondrial genome of M. proscarabaeus was automatically annotated by the software MitoZ (Meng et al. 2019) and manually compared with other meloid mitochondrial genomes. Of these, PCGs were checked by the identification of open reading frames and aligning with mitochondrial PCGs of other meloids. The annotated mitochondrial genome was analysed its genome characteristics, including nucleotide composition, the composition of skewness, codon usages, and relative synonymous codon usage (RSCU), using MEGA6 (Tamura et al. 2013). All available mitochondrial genomes of 15 meloid species were used to calculate the genetic distances within and between genera in Meloidae. P-distances were calculated using MEGA6 with the bootstrap method of 1,000 replications for the variance estimation.
Phylogenetic analysis
To infer the phylogenetic relationships among the family Meloidae, all available mitochondrial genomes of 15 meloid species, including the M. proscarabaeus, were employed to reconstruct the maximum-likelihood (ML) trees with the Tribolium castaneum (GenBank accession number NC_003081.2; Friedrich and Muqim 2003) as the outgroup. According to GenBank annotations, the nucleotide and amino acid sequences of 13 mitochondrial PCGs from each species were extracted and stop codons removed. Orderly combined sequences were aligned using MAFFT with the default settings (Katoh and Standley 2013) and the gaps and ambiguous sites removed to concatenate into consensus sequences including a 10,934 bp nucleotide and a 3,633 amino acid dataset, respectively. IQ-Tree was employed to estimate the best-fit models of partitioning schemes (Nguyen et al. 2015). The nucleotide and the corresponding amino acid datasets were partitioned for 13 genes individually. The best-fitting models of partitioning schemes were selected with the greedy search algorithm, under the Bayesian information criterion. The ML trees of both datasets were also reconstructed using IQ-Tree with 1000 bootstraps to assess the node support.
Results
Genome structure and composition
The 5.4 Gb raw data was yielded by the next-generation sequencing with 36,048,728 reads, and the 4.9 Gb (95.06%) clean data was obtained after filtering. The complete mitochondrial genome of M. proscarabaeus was assembled using 1,160,002 reads, and the average depth of coverage was assessed at 7,635.95 X. The mitochondrial genome was annotated and then submitted to the GenBank under the accession number OL840851. The complete mitochondrial genome of M. proscarabaeus is 15,653 bp in length, which is of moderate length among mitochondrial genomes within Meloidae (Du et al. 2016, 2017; Zhou et al. 2021).
The complete mitochondrial genome of M. proscarabaeus is a circular DNA molecule consisting of 13 protein-coding genes, 22 transport RNAs, two ribosomal RNAs, and a control region (Fig. 1). The length of rrnL and rrnS were determined to be 1,329 bp and 816 bp, respectively, and the control region was 1,013 bp in length. The nucleotide base composition of the mitochondrial genome was 37.5% A, 31.6% T, 19.1% C, and 11.9% G. The total A + T content was 69.1%, and the AT skew was 0.0854.
Protein-coding gene and codon usage
The total length of the 13 mitochondrial protein-coding genes in M. proscarabaeus is 11,127 bp, accounting for 71.10% of the total length of the genome, encoding 3,711 codons in total. All 13 protein-coding genes start using regular initiation codons, including ATT and ATG, and ATA (Table 1), which were commonly used as start codons in insect mitochondrial genomes. Most protein-coding genes terminated with conventional stop codons (such as TAA or TAG), except cox3, nad5, and nad4 stopped with T (Table 1).
Annotation of the Meloe proscarabaeus mitogenome.
Gene |
Location |
Inc |
Size |
Strand |
Anticodon |
Start codon |
Stop codon |
trnI
|
1–66 |
|
66 |
J |
GAU |
|
|
trnQ
|
64–132 |
-3 |
69 |
N |
UUG |
|
|
trnM
|
132–201 |
-1 |
70 |
J |
CAU |
|
|
nad2
|
220–1215 |
18 |
996 |
J |
|
ATT |
TAA |
trnW
|
1214–1279 |
-2 |
66 |
J |
UCA |
|
|
trnC
|
1279–1341 |
-1 |
63 |
N |
GCA |
|
|
trnY
|
1344–1408 |
2 |
65 |
N |
GUA |
|
|
cox1
|
1401–2948 |
-8 |
1548 |
J |
|
ATT |
TAA |
trnL2
|
2944–3007 |
-5 |
64 |
J |
UAA |
|
|
cox2
|
3008–3695 |
0 |
688 |
J |
|
ATA |
T* |
trnK
|
3696–3766 |
0 |
71 |
J |
CUU |
|
|
trnD
|
3767–3831 |
0 |
65 |
J |
GUC |
|
|
atp8
|
3832–3993 |
0 |
171 |
J |
|
ATT |
TAA |
atp6
|
3984–4655 |
-10 |
672 |
J |
|
ATG |
TAA |
cox3
|
4655–5437 |
-1 |
783 |
J |
|
ATG |
TAA |
trnG
|
5441–5503 |
3 |
63 |
J |
UCC |
|
|
nad3
|
5504–5857 |
0 |
354 |
J |
|
ATA |
TAG |
trnA
|
5856–5918 |
-2 |
64 |
J |
UGC |
|
|
trnR
|
5919–5982 |
0 |
64 |
J |
UCG |
|
|
trnN
|
5983–6049 |
0 |
67 |
J |
GUU |
|
|
trnS
|
6050–6108 |
0 |
59 |
J |
UCU |
|
|
trnE
|
6109–6169 |
0 |
61 |
J |
UUC |
|
|
trnF
|
6168–6231 |
-2 |
64 |
N |
GAA |
|
|
nad5
|
6232–7942 |
0 |
1711 |
N |
|
ATT |
T* |
trnH
|
7943–8006 |
0 |
64 |
N |
GUG |
|
|
nad4
|
8007–9339 |
0 |
1333 |
N |
|
ATG |
T* |
nad4l
|
9333–9620 |
-7 |
288 |
N |
|
ATG |
TAA |
trnT
|
9623–9685 |
2 |
63 |
J |
UGU |
|
|
trnP
|
9686–9748 |
0 |
63 |
N |
UGG |
|
|
nad6
|
9751–10242 |
2 |
492 |
J |
|
ATT |
TAA |
cob
|
10242–11381 |
-1 |
1140 |
J |
|
ATG |
TAA |
trnS2
|
11380–11447 |
-2 |
68 |
J |
UGA |
|
|
nad1
|
11465–12415 |
17 |
951 |
N |
|
ATT |
TAG |
trnL
|
12416–12479 |
0 |
65 |
N |
UAG |
|
|
rrnL
|
12442–13769 |
-38 |
1328 |
N |
|
|
|
trnV
|
13757–13825 |
-13 |
69 |
N |
UAC |
|
|
rrnS
|
13824–14638 |
-2 |
815 |
N |
|
|
|
CR |
14639–15653 |
0 |
1015 |
J |
|
|
|
The A + T bias is also manifested in the codon usage of protein-coding genes (Fig. 2). Relatively synonymous codon usages, excluding stop codons, showed that the third position of synonymous codons always has more frequency with A or T than G or C. Additionally, the first three frequently used codons UUA (Leu2), UCU (Ser2), GUU (Val), and some other frequently used codons, including AUU (Ile), UUU (Phe) AAU (Asn), etc. are comprised of two or three A and/or T nucleotides.
RNAs and control regions
All 22 transfer RNAs were annotated in the mitochondrial genome of M. proscarabaeus. Their length ranged from the shortest trnS with 59 bp to the longest trnK with 71 bp (Table 1). The maldistribution of transfer RNAs was also found in the mitochondrial genome. For example, there are two clusters comprising six transfer RNAs (trnA-trnR-trnN-trnS-trnE-trnF) between nad3 and nad5 genes and three transfer RNAs (trnW-trnC-trnY) between nad2 and cox1. The remaining RNAs are dispersed among other genes in a single or double way (Fig. 1). Two ribosomal RNAs mitochondrial genome of M. proscarabaeus were aligned with these of other meloid and assigned to the blanks between neighbouring genes. The rrnL gene was located between trnL and trnV with a length of 1,328 bp, the rrnS was located between tnrV and the control region with a length of 815 bp (Table 1). The control region was located between rrnS and trnI with 1,015 bp in length (Table 1; Fig. 1).
Genetic distances
The genetic distances within and between genera were calculated using the nucleotide and amino acid data of 13 mitochondrial PCGs among 15 meloid taxa. The result from the nucleotide data showed that the p-distances within genera for Hycleus, Epicauta, and Mylabris are 0.167, 0.173, and 0.232, respectively, with an average of 0.191, while the p-distances between genera ranged from 0.234 to 0.281 with an average of 0.258 (Fig. 3). The result from the amino acid data showed that the p-distances within genus of these three genera are 0.124, 0.107, and 0.163, respectively, with the mean of 0.115, and the p-distance between genera ranging from 0.173 to 0.226 with the mean of 0.187 (Fig. 3). The p-distances within genus are significantly lower than between genera from both datasets (p < 0.01). The p-distance between M. proscarabaeus and M. poggii was 0.116 and 0.064 from the nucleotide and the amino acid data, and far less than the corresponding distances between genera.
Phylogenic relationship
The phylogenetic relationships within the family Meloidae were inferred by using maximum likelihood methods, based on the nucleotide and amino acid data from mitogenomes of 15 meloid taxa. The best-fit partitioning schemes and corresponding substitution models are shown in Table 2. Log likelihoods of consensus trees constructed from 1000 bootstrap trees are −88,585.1106 and −32,785.8864 for the nucleotide and amino acid data, respectively.
The best-fit schemes and evolutionary models for two datasets from mitochondrial genomes.
Dataset |
Subset |
Best model |
Partition names |
nucleotide |
1 |
TIM+F+I+G4 |
nad2
|
2 |
GTR+F+I+G4 |
cox1
|
3 |
HKY+F+I+G4 |
cox2, apt6, nad3, nad4, nad4l, nad6
|
4 |
TPM3+F+G4 |
apt8
|
5 |
TIM2+F+I+G4 |
cox3, cob
|
6 |
TPM3+F+I+G4 |
nad5
|
7 |
K3Pu+F+I+G4 |
nad1
|
Amino acid |
1 |
mtMet+G4 |
nad2, cox2, apt8, nad3, nad6
|
2 |
mtZOA+G4 |
cox1
|
3 |
mtVer+G4 |
apt6
|
4 |
mtMAM+G4 |
cox3
|
5 |
mtInv+I+G4 |
nad5
|
6 |
mtInv+G4 |
nad4, nad4l
|
7 |
mtMAM+I+G4 |
cob
|
8 |
mtART+G4 |
nad1
|
The ML trees resulting from both datasets strongly support the monophyly of Meloe and Epicauta, whereas the genera Hycleus and Mylabris are not monophyletic (Fig. 4). The monophyletic Meloe, including M. proscarabaeus and M. poggii, sisters with Lytta into a branch in both phylogenetic trees, but the branch clusters with Epicauta or Hycleus in the ML tree from nucleotide or amino acid data, respectively (Fig. 4).
Discussion
The first mitochondrial genome of an oil beetle Meloe proscarabaeus was sequenced and annotated in this study. The gene arrangement and orientation were the same as the common ancestor for the Insecta (Boore et al. 1998; Taanman 1999). The A + T content and AT skew of M. proscarabaeus is the moderate level within Meloidae, and the biased usage of A and T nucleotides is also exhibited in mitochondrial PCGs, because the A + T bias is a common phenomenon in insect mitochondrial genomes (Du et al. 2017). Incomplete stop codons commonly exist in mitochondrial genomes of insects (Du et al. 2016; 2017). It is usual that the single T was employed as the stop codon in many insect mitochondrial genomes, and the incomplete stop codon could be functional in polycistronic transcription cleavage and polyadenylation processes (Ojala et al. 1981). The control region was located between rrnS and trnI with 1,015 bp in length, which is similar to that of other meloid mitochondrial genomes (Du et al. 2017). It is a noncoding region and a functional region that controls the replication and transcription of the mitochondrial genome and is the biggest region in which variations occurred to affect both sequence and the length of the entire mitochondrial genome (Andrews et al. 1999).
The genetic distance within and between genera was calculated to confirm the taxonomic status of M. proscarabaeus. The p-distances within genus are significantly lower than between genera from both datasets (p < 0.01), but the p-distance within Mylabris was a little higher than that between Hycleus and Mylabris (Fig. 3), which may be because of too a few Mylabris taxa and also discussed in some fishes and birds (Ma et al. 2020; Du et al. 2020). The p-distances resulting from the nucleotide and the amino acid data between M. proscarabaeus and M. poggii were both far less than the corresponding distances between genera. This indicates there exist a significant distinction in genetic distance within and between genera, and subsequently confirm the taxonomic status of M. proscarabaeus.
Phylogenetic analysis within Meloidae recover the monophyly of Meloe and Epicauta, and a polyphyly comprising Hycleus and Mylabris. Within the polyphyly, both trees based on the nucleotide and the amino acid datasets show that M. calida Pallas, 1782 clustered with H. chodschenticus Ballion, 1878 rather than M. aulica Menetries, 1832 (Fig. 4). The polyphyly of Mylabrini was also recovered by other studies utilising partial genes (mitochondrial 16S and nuclear ITS2 sequences) and complete mitochondrial PCGs (Bologna et al. 2008; Du et al. 2017). It may be caused by the high similarity between Hycleus and Mylabris and the inadequate number of taxa available for molecular phylogenetic studies. Previous studies also recovered the different topology (Bologna et al. 2008; Du et al. 2017), which might be limited by the lack of enough taxon sampling. To date, no phylogeny has definitively inferred the phylogenetic relationships within the families. In consideration of the diverse meloid species, the increasingly published information would help achieve more convincing conclusions for the phylogeny of the family.
Conclusion
The mitochondrial genome of M. proscarabaeus was assembled and described. The genome descriptions provide an informative reference for mitochondrial genomes of Meloe beetles. The mitochondrial genome sequence and its characteristics would be beneficial for future studies on taxonomy, molecular phylogenetics, and systematics of meloid insects.
Acknowledgements
This study was supported by the Technology Innovation and Entrepreneurship Seedling Project (2020JDRC0128), the Natural Science Foundation of Inner Mongolia (2021ms03023), and the Research Program of Science and Technology at Universities of Inner Mongolia Autonomous Region (NJZY22018).
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