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Mitochondrial genome of Chthamalus challengeri (Crustacea: Sessilia): gene order comparison within Chthamalidae and phylogenetic consideration within Balanomorpha
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Panpan Chen1, 2, Jun Song1, 2, Xin Shen1, 2, *, Yuefeng Cai1, Ka Hou Chu3, Yongqi Li1, Mei Tian1, 2, *
Acta Oceanologica Sinica | 2019, 38(6) : 25 - 31
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Acta Oceanologica Sinica | 2019, 38(6): 25-31
• Marine Biology •
Mitochondrial genome of Chthamalus challengeri (Crustacea: Sessilia): gene order comparison within Chthamalidae and phylogenetic consideration within Balanomorpha
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Panpan Chen1, 2, Jun Song1, 2, Xin Shen1, 2, *, Yuefeng Cai1, Ka Hou Chu3, Yongqi Li1, Mei Tian1, 2, *
Affiliations
  • 1 Jiangsu Key Laboratory of Marine Bioresources and Environment/Jiangsu Key Laboratory of Marine Biotechnology, Huaihai Institute of Technology, Lianyungang 222005, China
  • 2 Co-Innovation Center of Jiangsu Marine Bio-industry Technology, Lianyungang 222000, China
  • 3 Simon F. S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong, China
Published: 2019-06-25 doi: 10.1007/s13131-019-1355-0
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Acorn barnacles are important model species in researches on intertidal ecology, larval development and bio-fouling. At present, with the development of mitochondrial genomics, it is helpful to understand the phylogenetic relationship from the mitogenomic level. The complete mitochondrial genome of Chthamalus challengeri was presented. The genome is a circular molecule of 15 358 bp. Compared with other species in Balanomorpha, the non-coding region is longer, while the length of the genes is similar to the other species. The overall A+T content of the mitochondrial genome of C. challengeri is 70.5%. There are variations of initiation and stop codons in the known Balanomorpha mitochondrial genomes. The C. challengeri and C. antennatus within the same genus share the identical gene arrangement. However, the gene arrangement of different genera in Chthamalidae is different, as there is a translocation between two tRNA genes and an inversion involving a large gene block. In particular, both srRNA and lrRNA of the two species in Chthamalus are encoded in the heavy strand, differing from the former Balanomorpha species. The topology and gene arrangement in Chthamalidae support each other. Phylogenetic analysis indicates that the Chthamalidae is monophyletic, while the Balanidae and Archaeobalanidae are polyphyletic.

Balanomorpha  /  Chthamalus challengeri  /  mitochondrial genome  /  gene rearrangement  /  phylogeny
Panpan Chen, Jun Song, Xin Shen, Yuefeng Cai, Ka Hou Chu, Yongqi Li, Mei Tian. Mitochondrial genome of Chthamalus challengeri (Crustacea: Sessilia): gene order comparison within Chthamalidae and phylogenetic consideration within Balanomorpha[J]. Acta Oceanologica Sinica, 2019 , 38 (6) : 25 -31 . DOI: 10.1007/s13131-019-1355-0
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1 Introduction
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Acorn barnacles (Crustacea: Balanomorpha) are important model species in invertebrate larval biology, intertidal ecology, and anti-fouling research (Shen et al., 2017; Tsang et al., 2017). However, despite their important ecological and evolutionary role, there is a lack of thorough understanding on the phylogeny of this group (Chan et al., 2017). Over the past decade, the use of molecular markers and techniques (nuclear gene fragments, mitochondrial genes, etc.) leads to rapid development of barnacle research. As a genetic material outside the nucleus, the mitochondrial genome is relatively compact and easy to be sequenced, and thus is regarded as an important source of information for resolving metazoan phylogeny (Boore, 1999; Shen et al., 2016c). In the present study, the mitochondrial genome is a molecular marker which is helpful to analyze the phylogeny of metazoa from the genome level, and can be used for multi-directional molecular evolution studies from mitochondrial sequence information, gene composition and gene arrangement (Corradi and Bonen, 2012). Thus the complete mitochondrial genome sequence is a powerful tool for the study of animal molecular phylogeny (Boore, 1999; Zhang and Zhang, 2012).
Chthamalus challengeri is one of the common barnacles along the coast of Yellow Sea and Bohai Sea in northern China, distributed in supratidal zone and the intertidal rocky shore. It can withstand long-term periodic drying and has strong adaptability (Liu and Ren, 2007). Here we present the complete mitochondrial genome of the C. challengeri, including its gene content, protein-coding genes, codon usage, gene arrangement and phylogenetic relationship with other Balanomorpha species.
2 Materials and methods
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2.1 Sample collection and DNA extraction
The specimen of C. challengeri was obtained from the intertidal of Ganyu District (34°35′49.05″N, 119°12′17.45″E), Lianyungang, Jiangsu Province, China. Total genomic DNA was extracted from the muscle tissue, using TIANamp Marine Animal DNA Kit (TIANGEN) following the manufacturer's protocol.
2.2 PCR amplification and sequencing
Initially, we used universal primers and specific primers to amplify the cox1 and lrRNA gene segments (Table 1). The reaction mixture for amplifying cox1 and lrRNA gene segments, in a total volume of 20 μL, contained 7.4 μL sterile distilled H2O, 1 μL each primer, 10 μL Extaq polymerase and 0.6 μL DNA template. The PCR amplifications were performed with the following cycling parameters: initial denaturation at 94°C for 3 min, 35 cycles of denaturation at 94°C for 30 s, annealing at 55°C for 30 s, elongation at 72°C for 30 s, and a final extension at 72°C for 10 min.
The reaction mixture for amplifying cox1-lrRNA/lrRNA-cox1 gene segments, in a total volume of 20 μL, contained 11.7 μL sterile distilled H2O, 2.0 μL 10× PCR buffer, 3.2 μL dNTP mix (2.5 mmol/L), 1 μL each primer, 0.1 μL TaKaRa LA Taq polymerase, and 1 μL DNA template. The cycling parameters of PCR were as follows: initial denaturation at 94°C for 3 min, 35 cycles of denaturation at 94°C for 30 s, annealing at 55°C for 30 s, elongation at 68°C for 8 min, and a final extension at 68°C for 10 min. PCR products were purified (GeneMark), cloned (pGEMT easy, Promega) and sequenced (MAP BIOTECH in Shanghai).
2.3 Gene identification and genome analysis
In this study, the MITOS Webserver (http://mitos.bioinf.uni-leipzig.de/index.py) online software (Bernt et al., 2013) was used to predict the mitochondrial genes of C. challengeri, including 13 PCGs, 2 ribosomal RNAs and 22 transfer RNAs, which was a convenient, rapid and accurate way of annotating mitochondrial genomes (Shen et al., 2015b). Gene map of C. challengeri mitochondrial genome was drawn by OGDraw 1.2 (Lohse et al., 2013). In addition, codon usage in the 13 PCGs of the mitochondrial genome was estimated with DnaSP 5.10.01 (Librado and Rozas, 2009). The genomic analysis included general features, base composition and skew, gene arrangement, and protein-coding genes.
2.4 Phylogenetic analysis
Along with newly obtained mitochondrial genome sequence of C. challengeri, the 21 mitochondrial genomes currently available from Balanomorpha and Pendunculata were used in phylogenetic analysis, including 17 genomes from Balanomorpha: Acasta sulcata, Striatobalanus amaryllis (Tsang et al., 2015), Armatobalanus allium, Amphibalanus amphitrite (Shen et al., 2015a), Megabalanus volcano, Megabalanus ajax (Shen et al., 2016b), Balanus balanus (Shen et al., 2016d), Chelonibiate studinuria, Nobia grandis (Shen et al., 2016a), Chthamalus antennatus, Notochthamalus scabrosus (Wares, 2015), Octomeris sp. BKKC-2014, Tetraclita japonica, Tetraclita serrata (Shen et al., 2015b), Tetraclitella divisa, Epopella plicata (Shen et al., 2017) and Savignium sp. BKKC-2014, and four from Pedunculata including Capitulum mitella (Lim and Hwang, 2006), Pollicipes polymerus (Lavrov et al., 2004), Lepas anserifera and Lepas australis.
Nucleotide sequences of the 13 PCGs from these mitochondrial genomes were aligned using MEGA 7.0.25 (Kumar et al., 2016) with the default settings. To determine the best fitting mode, maximum likelihood (ML) method was performed using PhyML 3.0 (Guindon et al., 2010) and MEGA 7.0.25 (Kumar et al., 2016) with 100 bootstrap replicates, respectively.
3 Results and discussion
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3.1 General features
The mitochondrial genome of C. challengeri is a circular molecule of 15 358 bp, similar to the sizes for the other acorn barnacles (Liu et al., 2016). It encodes 13 PCGs, 2 rRNA genes, and 22 tRNA genes. The heavy and light strands contain 30 and 7 genes, respectively (Fig. 1, Table 2). Five instances of gene overlaps are found in mitochondrial genome of C. challengeri. One 7-bp overlap is found between nad4L and nad4 gene, and there are four other overlaps ranging from 1 to 5 bp. Non-coding regions make up 836 bp, with the longest one speculated as the control region (321 bp), which is located between srRNA and trnK (Table 2). Some non-coding regions of the C. challengeri genes are relatively longer than the other 21 species mentioned in this paper. The A+T content on the heavy strand of the mitochondrial genome of C. challengeri is 70.5%, which is the comparable values reported for the other 17 sessile barnacles (ranging from 65.4% to 73.4%). The entire C. challengeri mitochondrial genome sequence was deposited in GenBank with accession number KJ865097.
3.2 Protein-coding genes and codon usage
In C. challengeri mitochondrial genome, two PCGs (cob and nad6) are encoded on the light strand while the other 11 PCGs are located on the heavy strand. In the 18 mitochondrial genomes of the Sessilia species, the number of amino acids in the three PCGs (cox2, cox3 and atp8) is the same, respectively. However, there are differences in gene length among the remaining 10 PCGs. In addition, among the four species of Chthamalidae (C. challengeri, C. antennatus, Octomeris sp. BKKC-2014 and N. scabrosus), the number of amino acids in four PCGs (atp6, nad4, cob and nad2) is also the same. As previously reported, metazoan mitochondrial PCGs often use several ATN alternatives as start codons (Shen et al., 2009, 2012, 2015b). All 13 PCGs in C. challengeri start with ATD (ATA, ATG or ATT) (Table 2). In the 18 mitochondrial genomes of the Balanomorpha species, cox2, cox3, cob and nad4 (except for B. balanus) genes start with “ATG”. The start codons of nad4L, nad5, nad6, nad1 and nad2 genes start with “GTG” or “TTG”. The initiation codons of the cox1 gene are diverse. Three protein-coding genes (nad3, nad1 and nad4) in C. challengeri end with incomplete stop codon (T-), and the remaining PCGs use stop codons (TAA or TAG). Meanwhile, all the complete stop codons of A. sulcata, A. allium, N. grandis, E. plicata and N. scabrosus are “TAA”.
The pattern of codon usage in the C. challengeri mitochondrial genome was studied with DnaSP 5.10.01 (Librado and Rozas, 2009). There are 3 681 codons in all 13 PCGs (excluding the incomplete termination). The most frequently used amino acids were Leu (14.47%), Ser (10.28%), Phe (9.72%) and Ile (9.21%), while Gln and Arg were used least, at 1.72% and 1.55%, respectively (Table 3). The A+T composition of the first and second codon in the 13 PCGs of C. challengeri is 63.0% and 64.4%, respectively. Yet the value for the third codon position elevates to 81.3%, which is within the range of 17 other Balanomorpha species (ranging from 62.0% to 87.9%).
3.3 Base composition and skew
The bias of the base composition in each gene can be described by skewness (Perna and Kocher, 1995) that measures the relative numbers of A to T (AT skew) and G to C (GC skew), and is calculated as (A%−T%)/(A%+T%) and (G%−C%)/(C%+G%), respectively. The heavy strand in the C. challengeri mitochondrial genome consists of 34.9% A, 22.2% C, 12.5% G and 30.5% T. AT and GC skews of the whole genome are –0.130 and 0.092, respectively. The A+T contents of 13 PCGs range from 65.6% (cox1) to 79.2% (atp8), and those of srRNA and lrRNA are 68.1% and 75.0%, respectively. All 13 PCGs consist of 27.4% A, 14.7% C, 15.8% G, and 42.2% T bases. AT skew and GC skew are –0.214 and 0.036, respectively. All 13 PCGs have skews of T vs. A (AT skew between –0.046 and –0.288). However, both RNAs have A skew of 0.027 and 0.022, respectively. On the other hand, there are six PCGs have skews of G vs. C (ranging from 0.020 to 0.241), and the other 7 PCGs have skews of C vs. G (between –0.025 and –0.255). In addition, both rRNAs have skew of G vs. C for srRNA and lrRNA (0.190 and 0.220, respectively; Table 4).
3.4 Ribosomal and transfer RNA genes
The length of srRNA and lrRNA is 758 and 1 310 bp, respectively, which are similar to length in the other barnacle mitochondrial genomes (srRNA ranges from 751 to 825 bp; lrRNA ranges from 1 290 to 1 374 bp) (Shen et al., 2015b; Wares, 2015). The two rRNAs, located between trnL1 and the control region, are separated by one tRNA gene (trnV). The length of 22 tRNA genes in the C. challengeri is similar to other Balanomorpha species, ranging from 58 (trnS1) to 70 (trnS2) nucleotides (Shen et al., 2015b).
3.5 Gene arrangement
Gene arrangement is often used as a supplementary means to help us understand the evolutionary and phylogenetic relationships among species. In recent years, more and more data show that although pancrustaceans generally exhibit ancestral mitochondrial gene arrangement, the mitochondrial gene order in Balanomorpha species is not conserved, with differences in gene blocks or individual genes.
The two species (C. challengeri and C. antennatus) in Chthamalus share the identical gene order. However, the gene orders of different genera in Chthamalidae are different and there are translocation and inversion in genes or gene blocks (Fig. 2). Between N. scabrosus and Octomeris sp. BKKC-2014, there is translocation between trnI and trnQ. However, comparing with the two species in Chthamalus, there is an inversion of a large gene block (nad5-H-nad4-nad4L-P-T-nad6-cob-S2-Y-C-nad1-L1-lrRNA-V-srRNA-K), which is a considerable rearrangement among different genera in Chthamalidae. In addition, both lrRNA and srRNA in Chthamalus are encoded on the heavy strand, which is different from the other 16 Balanomorpha species (mentioned above), in which both lrRNA and srRNA are encoded on the light strand. This is the biggest difference found on the rRNA so far, and the reason needs further analysis and research. Gene rearrangement appears to have occurred frequently in Chthamalidae.
According to the above comparison and analysis, it is found that the gene arrangement between each of the two species pairs (C. challengeri and C. antennatus; Octomeris sp. BKKC-2014 and N. scabrosus) are similar. The gene arrangement of N. scabrosus is found to be closest to the pancrustacean ground pattern, so that this species can be presumed to close to basal in Chthamalidae. The gene arrangement of C. challengeri appears to be most derived. Yet, the pattern of the evolutionary changes in the gene arrangement of Chthamalidae requires data based on extensive taxon coverage from the family.
3.6 Phylogeny analysis
A ML tree was constructed using amino acid sequences of 13 PCGs from 22 complete mitochondrial genomes (Fig. 3). Within Balanomorpha, members from Archaeobalanidae, Balanidae and Pyrgomatidae are grouped together (Bootstrap, BP=100), but their interrelationships are poorly resolved other than the groupings of the two Megabalanus species (BP=100) and the two species from Pyrgomatidae (BP=90). As the existing data and documents, with the increase and supplement of data, it is supposed that Balanidae and Archaeobalanidae are non-monophyly (Shen et al., 2015b; Tsang et al., 2014, 2017). Four species of Tetraclitidae cluster with C. testudinaria of Coronulidae (BP=100), inferring their close relationship. The N. scabrosus is located at the basal of Chthamalidae, clustering with Octomeris sp. BKKC-2014 and the two species (C. challengeri and C. antennatus) in Chthamalus, and the topology is the same with the relationship inferred based on gene arrangement. In conclusion, the topology and gene arrangement in Chthamalidae support each other. Phylogenetic analysis indicates that the Balanidae and Archaeobalanidae are polyphyletic. From the topology of the current phylogenetic tree, Chthamalidae is monophyletic. Yet, more data and research will be needed to reveal the phylogeny within Balanomorpha and its constituent families, including Chthamalidae.
Funding
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  • The National Natural Science Foundation of China (NSFC) under contract No. 41876147; the Jiangsu Priority Academic Program Development (PAPD); the Graduate Research and Innovation Projects under contract Nos KYCX18_2570 and KYCX18_2566; Jiangsu Qinglan; Jiangsu 333; Jiangsu Six Talent Peaks and Lianyungang 521 Talent Projects.
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Year 2019 volume 38 Issue 6
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Article Info
doi: 10.1007/s13131-019-1355-0
  • Receive Date：2017-04-16
  • Online Date：2026-04-01
  • Published：2019-06-25
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History
  • Received：2017-04-16
  • Accepted：2017-06-19
Funding
The National Natural Science Foundation of China (NSFC) under contract No. 41876147; the Jiangsu Priority Academic Program Development (PAPD); the Graduate Research and Innovation Projects under contract Nos KYCX18_2570 and KYCX18_2566; Jiangsu Qinglan; Jiangsu 333; Jiangsu Six Talent Peaks and Lianyungang 521 Talent Projects.
Affiliations
    1 Jiangsu Key Laboratory of Marine Bioresources and Environment/Jiangsu Key Laboratory of Marine Biotechnology, Huaihai Institute of Technology, Lianyungang 222005, China
    2 Co-Innovation Center of Jiangsu Marine Bio-industry Technology, Lianyungang 222000, China
    3 Simon F. S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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