Complete mitochondrial genome of Neochauliodes parasparsus (Megaloptera: Corydalidae) with phylogenetic consideration

Biochemical Systematics and Ecology 70 (2017) 192e199

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Complete mitochondrial genome of Neochauliodes parasparsus (Megaloptera: Corydalidae) with phylogenetic consideration Yanyu Zhao a, Hongli Zhang b, Yanhua Zhang c, * a

Department of Medical Genetics, Zunyi Medical University, Zunyi, China School of Life Sciences, Datong University, Datong, China c College of Life Sciences, Jiangsu Normal University, Xuzhou, China b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 13 September 2016 Received in revised form 25 November 2016 Accepted 4 December 2016 Available online 10 December 2016

We sequenced the complete mitochondrial genome (mitogenome) of Neochauliodes parasparsus. The 15,995-bp mitogenome contained the standard set of 13 protein-coding genes, 22 transfer RNA genes (tRNAs), 2 ribosomal RNA genes (rRNAs), and a putative control region, with a gene arrangement that was identical to that reported for most other megalopteran species. We also predicted the secondary structure of all the RNA genes and analysed the preferred codon usage of the protein-coding genes. The putative 1265-bp control region contained two tandem repeated regions and several microsatellite-like elements. The phylogenetic analysis of available neuropteridan mitogenomes, based on the 13 protein-coding genes, appeared to support the current view of the neuropteridan phylogeny, and among the Neochauliodes spp., N. parasparsus was the most closely related to N. punctatolosus. © 2016 Elsevier Ltd. All rights reserved.

Keywords: Neochauliodes parasparsus Corydalidae Mitogenome Phylogenetic analysis

1. Introduction The Neuropterida clade comprises three relatively small orders of holometabolous insects, including Megaloptera, Raphidioptera, and Neuroptera. Although these three orders contain fewer species than the four megadiverse holometabolous orders (Coleoptera, Diptera, Hymenoptera, and Lepidoptera), their basal phylogenetic positions indicate their importance in the early diversification of Holometabola. Within Megaloptera (dobsonflies, fishflies, and alderflies), which contains € ck, 2002), fishflies make up the subfamily Chauliodinae (Corydalidae, more than 300 described species worldwide (Aspo Megaloptera) and possess aquatic larvae that are useful as environmental stress indicators (Pennuto, 2009). The genus Neochauliodes Weele, 1909 is the largest group of the subfamily and comprises more than 30 species, which are distributed from far eastern to south-eastern Asia. To date, however, most studies have focused on the genus' biological properties,

Abbreviations: mitogenome, mitochondrial genome; PCGs, protein-coding genes; tRNA, transfer RNA; rRNA, ribosomal RNA; ML, maximum likelihood; BI, Bayesian inference; rrnL, large rRNA subunits; rrnS, small rRNA subunits; DmTTF, the transcription termination factor. * Corresponding author. College of Life Sciences, Jiangsu Normal University, Xuzhou, 221116, China. E-mail address: [email protected] (Y. Zhang). http://dx.doi.org/10.1016/j.bse.2016.12.002 0305-1978/© 2016 Elsevier Ltd. All rights reserved.

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morphology, and diversity (Hayashi, 2002; Liu and Yang, 2005; Liu et al., 2007), and little is known about the lineage's molecular data. Mitochondrial genomes (mitogenomes) have been widely used to elucidate phylogenetic relationships, the genetic structure of populations, and patterns of gene flow (Hirase et al., 2016; Wang et al., 2014). For most animals, the mitogenome is regarded as a suitable molecular marker for phylogenetic analysis, owing to its abundance in animal tissues, compact genome size, faster rate of evolution, low rate (or absence) of recombination, and evolutionary conserved gene products (Boore, 1999; Gissi et al., 2008). However, only five fishfly mitogenomes are currently available on GenBank, thus limiting both phylogenetic and population genetic studies within the Chauliodinae, as well as studies of the megalopteran mitogenome. Accordingly, we sequenced the complete mitochondrial genome of Neochauliodes parasparsus and compared the mitogenome's structure and composition to those of other available megalopteran mitogenomes. Moreover, we also analysed phylogenetic relationships within Megaloptera and evaluated the phylogenetic position of N. parasparsus, based on available mitogenome data. This new addition to the pool of megalopteran mitogenomes provides useful sequence information that can be used for population genetics studies of N. parasparsus and evolutionary studies of Corydalidae. 2. Materials and methods 2.1. Sample collection and DNA extraction A single N. parasparsus specimen was collected using a light trap at Ningshan County, Shaanxi Province, China, preserved in 95% ethanol, and stored at
20  C until DNA extraction. Total DNA was extracted using an Animal Genomic DNA Extraction Kit (Tiangen Biotech, Beijing, China), according to the manufacturer's protocol, and the quality of DNA was assessed by electrophoresis on a 1% agarose gel with ethidium bromide. 2.2. PCR amplification and sequencing The complete N. parasparsus mitogenome was amplified in overlapping fragments, using a combination of universal (Simon et al., 2006) and newly developed (Supplementary Table S1) primers. PCR was performed using TaKaRa LA Taq and the following conditions: an initial denaturation step of 1 min at 93  C; followed by 35 cycles of 15 s at 92  C, 30 s at 48e57  C, and 2e4 min at 72  C; and a final extension of 10 min at 72  C. The PCR products were electrophoresed on 0.8% agarose gels, purified, and then sequenced directly with the PCR primers and internal primers that were generated by primer walking. 2.3. Sequence analysis Raw sequence files were assembled into contigs, using the Staden Package v1.7.0 (Staden et al., 2000). Protein-coding genes (PCGs) were identified using ORF Finder, implemented on the NCBI website, with the invertebrate mitochondrial genetic codes. To ensure the accurate boundaries of PCGs and ribosomal RNA (rRNA) genes, the sequences were compared with published insect mitochondrial sequences using Clustal X 1.83 (Wang et al., 2012). Meanwhile, the transfer RNA (tRNA) genes were predicted using tRNAscan-SE (Lowe and Eddy, 1997), with invertebrate mitochondrial codon and a cove score cut off of 5. The base composition, codon usage, and nucleotide substitution were analysed using MEGA v5.1 (Tamura et al., 2011), and Tandem Repeat Finder v4.07 was used to identify tandem repeats in non-coding regions (Benson, 1999). Strand asymmetry was calculated with the following formulae: AT skew ¼ [A
T]/[AþT] and GC skew ¼ [G
C]/[GþC]. 2.4. Phylogenetic analysis A phylogenetic tree was reconstructed from the complete or nearly complete neuropteridan mitogenes available on GenBank. Due to the close relationship of the Neuropterida and Coleoptera, the beetles Bicellonychia lividipennis and Hapsodrilus ignifer were selected as outgroups (Amaral et al., 2016; Cameron et al., 2009). Sequence alignment was inferred from the amino acid alignment of 13 PCGs, using Clustal implemented in MEGA v5.1. The aligned sequences of individual genes were then concatenated for phylogenetic analysis. The best-fit model (GTRþIþG) for each codon site (Zhang et al., 2016) was selected using Akaike information criterion in jModelTest (Posada, 2008), and both MrBayes v3.1.1 (Ronquist and Huelsenbeck, 2003) and RAxML ver.7.2.8 (Stamatakis et al., 2005) were employed to analyse the data set. In the Bayesian Inference (BI) analysis, two simultaneous runs of 5,000,000 generations were conducted for the matrix. Each set was sampled every 100 generations, with a burn-in of 25%. In the Maximum likelihood (ML) analysis, the parameters were estimated during analysis, and the node support values were assessed by calculation from 1000 bootstrap resampling replicates. 3. Results and discussion 3.1. Genome organization and base composition Sequencing revealed that the full-length N. parasparsus mitogenome is a circular, double stranded molecule of 15,995 nucleotides in length (GenBank accession number KX821680), which is just slightly shorter than those of Dysmicohermes

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ingens (16,271 nt) and N. bowringi (16,064 nt) (Li et al., 2015; Wang et al., 2016) but longer than those of sequenced mitogenomes from other megalopteran species. The N. parasparsus mitogenome contained the whole set of 37 genes (13 PCGs, 22 tRNA genes, and 2 rRNA genes), as well as a putative control region, which is common in animal mitogenomes (Fig. 1 and Table 1). Although gene rearrangement has been reported in the Neuropterida (Yan et al., 2014), the gene order of the N. parasparsus mitogenome was similar to that of other megalopteran species, a pattern that is consistent with the gene order of the putative ancestral pancrustacean mitogenome. Twenty-three and 14 genes were distributed on the majority and minority strands, respectively (Table 1), and gene overlaps were found at 16 locations, with a total of 40 overlapping base pairs. Two conserved gene overlaps (ATGATAA and ATGTTAA) were observed in ATP8-ATP6 and ND4-ND4L, respectively, and the longest overlap (8 bp) was found in trnW-trnC and trnY-COI (Table 1). The N. parasparsus mitogenome exhibited a strong bias towards A and T nucleotides (38.4% A, 14.7% C, 37.7% T, and 9.2% G), with a total AþT content of 76.1%, which is very typical of invertebrate mitogenomes. The AþT content, AT-skew, and GC-skew are routine parameters for investigating the nucleotide-compositional behaviour of mitogenomes (Perna and Kocher, 1995). The results of the comparative analysis of the AþT%, AT- and GC-Skew within the sequenced megalopteran mitogenomes were shown in Table 2. The base composition patterns of megaloptera mitogenomes are similar, with the highest AþT content observed in the control region for all species, ranging from 84.4% in Protohermes concolorus to 93.2% in N. bowringi. Of the three gene types, the rRNA genes had a higher AþT content than the protein-coding and tRNA genes in most species. However, the AT- and GC-Skew values differed among species, and the AT-Skew of the protein-coding and rRNA genes was negative, whereas that of the tRNA genes was positive. The remaining regions demonstrate the different AT-Skews among species. Conversely, the GC-Skew of the control region and the whole genome exhibited a similar trend, but the protein-coding and rRNA genes exhibited various trends.

Fig. 1. Map of the Neochauliodes parasparsus mitogenome. L1, L2, S1, and S2 denote the trnLUUR, trnLCUN, trnSAGN, and trnSUCN genes, respectively.

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Table 1 Organization of the Neochauliodes parasparsus mitogenome. Gene (region)

trnI trnQ trnM ND2 trnW trnC trnY COI trnLUUR COII trnK trnD ATP8 ATP6 COIII trnG ND3 trnA trnR trnN trnSAGN trnE trnF ND5 trnH ND4 ND4L trnT trnP ND6 Cytb trnSUCN ND1 trnLCUN rrnL trnV rrnS AT-rich region

Strand

J N J J J N N J J J J J J J J J J J J J J J N N N N N J N J J J N N N N N e

Position

Codon

From

To

Start

1 61 134 203 1218 1275 1338 1395 2936 3008 3697 3767 3833 3985 4662 5453 5516 5868 5943 6005 6071 6139 6203 6268 7994 8056 9386 9679 9744 9815 10,324 11,459 11,540 12,489 12,553 13,871 13,942 14,731

63 129 202 1219 1282 1337 1402 2935 2999 3688 3767 3832 3991 4662 5450 5515 5869 5931 6005 6071 6139 6204 6267 7993 8056 9392 9676 9743 9809 10,324 11,460 11,525 12,487 12,552 13,870 13,941 14,730 15,995

ATT

Anticodon

Size (bp)

Intergenic nucleotides

GAT TTG CAT

63 69 69 1017 65 63 65 1541 64 681 71 66 159 678 789 63 354 64 63 67 69 66 65 1726 63 1337 291 65 66 510 1137 67 948 64 1318 71 789 1265

/
3 4 0
2
8 0
8 0 8 8
1 0
7
1 2 0
2 11
1
1
1
2 0 0
1
7 2 0 5
1
2 14 1 0 0 0 0

Stop

TAA TCA GCA GTA

ATT

TA

ATG

TAA

TAA CTT GTC ATT ATG ATG

TAA TAA TAA

ATT

TAG

TCC TGC TCG GTT GCT TTC GAA ATC

T

ATG ATG

TA TAA

GTG

TGT TGG ATC ATG

TAA TAA

TTG

TAA

TGA TAG TAC

Notes: J and N refer to the majority and minority strands, respectively.

Table 2 Nucleotide composition of the Neochauliodes parasparsus mitogenome. Taxon

whole genome AT% ATGCSkew Skew Neochauliodes parasparsus 76.1 0.009
0.233 Neochauliodes bowringi 76.6 0.037
0.277 Neochauliodes 76.4 0.017
0.249 punctatolosus Dysmicohermes ingens 78.5 0.001
0.173 Acanthacorydalis orientalis 76.8
0.009
0.215 Corydalus cornutus 74.9 0.014
0.262 Neoneuromus tonkinensis 76.3 0.005
0.228 Nevromus exterior 77.5
0.005
0.199 Protohermes concolorus 75.8
0.011
0.254 Sialis hamata 78.3 0.014
0.171 Sialis sp. 78.5 0.018
0.175

protein-coding genes AT% ATGCSkew Skew 73.6
0.153
0.005 73.6
0.153
0.014 74.0
0.152
0.002 76.4 74.8 72.7 74.5 75.8 74.1 76.1 76.6


0.140
0.160
0.173
0.172
0.166
0.165
0.151
0.141

0.036 0.012 0.004 0.004 0.038 0.007 0.024 0.026

Ribosomal RNA genes AT% ATGCSkew Skew 80.5
0.054 0.348 80.8
0.060 0.353 80.7
0.059 0.340 81.7 81.1 79.8 80.1 81.4 80.1 83.2 82.7


0.025
0.012
0.039
0.036
0.021
0.004
0.049
0.061

0.314 0.337 0.396 0.364 0.333 0.359 0.286 0.307

Transfer RNA AT% ATSkew 76.8 0.014 77.0 0.021 76.9 0.018 76.8 76.1 75.5 76.2 76.2 76.1 79.4 78.9

0.030 0.012 0.000 0.002 0.015 0.024 0.012 0.007

genes GCSkew 0.173 0.180 0.193 0.176 0.148 0.110 0.164 0.155 0.133 0.139 0.139

AþT-rich region AT% ATGCSkew Skew 89.3
0.009
0.378 93.2 0.060
0.378 91.2
0.008
0.461 90.7 88.8 87.9 87.5 88.7 84.4 91.6 91.7


0.010
0.046
0.007 0.008
0.022
0.044
0.035
0.048


0.338
0.281
0.385
0.252
0.409
0.537
0.265
0.286

3.2. Protein-coding genes and codon usage The total length of PCGs in the N. parasparsus mitogenome was 11,133 bp. The average AþT content of the PCGs was 73.6%, ranging from 66.6% (COI) to 82.2% (ND6). All the PCGs started with the common ATN codon (two with ATC, four with ATT, and six with ATG), with the exception of ND1, which possessed a TTG start codon. Meanwhile, 10 of the PCGs ended with stop

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codons of TAA or TAG, and the other three ended with incomplete stop codons (i.e., TA or T) (Table 1). Incomplete stop codons have been observed in many sequenced megalopteran mitogenomes and is also common in metazoan mitochondrial genes. A common interpretation of this phenomenon is that TAA termini are created on the corresponding transcripts via posttranscriptional polyadenylation (Ojala et al., 1981). Codon usage in the N. parasparsus mitogenome was analysed, using the typical invertebrate mitochondrial genetic code, and the results are presented in Supplementary Table S2. The most frequently used codons were TTA (Leu, 11.8%), ATT (Ile, 9.0%), TTT (Phe, 7.7%), and ATA (Met, 5.6%), which, together, accounted for 34.1% of the codons and contributed to the mitogenome's high AþT content; leucine (16.1%), isoleucine (10.2%), serine (9.4%), and phenylalanine (9.1%) were the most common amino acids in the predicted protein sequences. Furthermore, both two-fold degenerate codons and four-fold degenerate codons exhibited a bias towards A or T at the third codon position. These usage patterns have also been common among other megalopteran mitogenomes (Yan et al., 2014). 3.3. Transfer and ribosomal RNA genes All 22 tRNAs, which are typically found in the bilaterian mitochondrial genomes, were identified in the N. parasparsus mitogenome and ranged from 63 to 71 bp in length. Each tRNA gene exhibited the typical cloverleaf secondary structure, except for the trnSAGN gene, which lacks a stable stem-loop structure and forms a simple loop in the DHU arm. This characteristic has been observed in other insect mitogenomes, including those of neuropteridans (Jiang et al., 2015). In addition, 31 non-canonical base pairs were found in the N. parasparsus tRNAs, based on their secondary structure. Twenty-eight of these were G-U pairs, which form weak bonds, and the remaining were atypical pairings in the anticodon arm. Comparative analyses of the secondary structures of megalopteran tRNAs are shown in Fig. 2. Furthermore, among the 22 tRNAs, trnLUUR, trnW, and trnE exhibited high levels of nucleotide conservation, and trnSAGN, trnC, and trnP exhibited lower levels of conservation (Fig. 2). The large rRNA subunit gene (rrnL) was 1318 bp long, with an AþT content of 77.2%, whereas the small rRNA subunit gene (rrnS) was 789 bp long, with an AþT content of 76.9%; the features of both rrnL and rrnS were similar to those of most megalopteran species. The secondary structures of both these genes are provided in Supplementary Figs. S1 and S2. Our analysis also revealed that the rrnL and rrnS from N. parasparsus comprised five and three structural domains, respectively, and the sequence of rrnL was more highly conserved than that of rrnS, when compared to the secondary structures reported for the rrnL and rrnS genes from other megalopterans. Furthermore, in the N. parusparsus rrnS, domain III was conserved, but domains IV and VI exhibited the highest levels of conservation. 3.4. Non-coding regions Sequencing revealed that the longest non-coding region, the control region, is located between the rrnS and trnI genes and has a length of 1265 bp. The two tandem repeated regions (231 bp2 and 68 bp2) that were identified at the 50 end of the control region have also been reported to occur in other fishfly species (Chauliondinae), although the feature is lacking in dobsonflies (Corydalinae) (Jiang et al., 2015). In addition, microsatellite-like elements, such as (AT)6, (TA)7, (TAA)3 and (ATTA) 3, were abundant throughout the control region and represent potentially useful markers for the analysis of geographical population structure. Furthermore, although the control region is usually associated with the regulation of replication and transcription within the mitogenome, conserved motifs that are common among insect lineages were not observed. However, the 30 portion of the control region lacking repeated sequences possessed a fragment that was relatively conserved within the Corydalidae. Apart from the control region, nine other small non-coding intergenic spacers were identified. The largest intergenic spacer was found between trnSUCN and ND1, and all nine regions contained a highly conserved 7-bp motif (TACTWAA), which is observed in many pancrustacean lineages and may be a binding site for the transcription termination factor (DmTTF) (Baek et al., 2014; Ye et al., 2016). 3.5. Phylogenetic analysis Both the ML and BI phylogenetic trees of the concatenated PCGs exhibited similar topologies and high support values (Fig. 3), and the relationship among the Megaloptera, Raphidioptera, and Neuroptera was consistent with the current view of higher-level neuropteridan relationships (Raphidiopteraþ(Megalopteraþ Neuroptera)) (Misof et al., 2014; Peters et al., 2014). Within the Corydalidae, which is a relatively large family of Megaloptera, the Corydalinae subfamily formed a monophyletic lineage, and the phylogenetic relationships within Corydalinae were similar to those reported previously (Jiang et al., 2015). Meanwhile, in the Chauliodinae subfamily, four fishfly species were clustered in a monophyletic group. Three Asian species (Neochauliodes spp.) were grouped together and then placed as the sister group of the North American endemic fishfly Dysmicohermes ingens, and within the genus Neochauliodes, N. parasparsus was most closely related to N. punctatolosus. The overall molecular phylogeny of the Neuroptera did not conform to traditional views that are based on morphology. Osmylidae was placed as a basal clade, thus separated from other neuropterans, and Hemerobiiformia were nonmonophyletic (Zhao et al., 2013), whereas Myrmeleontiformia formed a monophyletic group with high support values. In addition, most species clustered with other members of their respective families, but Epacanthaclisis banksi and Myrmeleon immanis

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Fig. 2. Predicted secondary structures of the 22 transfer RNAs in the Neochauliodes parasparsus mitogenome.

(Myrmeleontidae) were recovered as paraphyly, which contains three species of Ascalaphidae. Although the topology of this branch differed among the BI and ML trees, the combined results could not support the monophyly of Myrmeleontidae, and due to the limited availability of mitogenomes from this group, the relationships within and between Myrmeleontidae and Ascalaphidae remain largely unresolved in our analysis. Therefore, to characterize clear and robust evolutionary relationships within Neochauliodes and Neuropterida, future studies will need to increase the taxonomic sampling of each representative group.

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Fig. 3. Phylogeny of 28 neuropteridan species, based on mitochondrial protein-coding genes. First values at the branches correspond to Bayesian posterior probabilities, and the second values indicate ML bootstrap support as percentage values.

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