Journal of Oceanology and Limnology   2023, Vol. 41 issue(1): 267-279     PDF       
http://dx.doi.org/10.1007/s00343-021-1319-z
Institute of Oceanology, Chinese Academy of Sciences
0

Article Information

LI Jiasheng, PENG Ying, ZHANG Shufei, LIU Yifan, ZHANG Kun, CHEN Jian, ZHANG Hua, ZHANG Chi, LIU Bingjian
The complete mitochondrial genome of Parachiloglanis hodgarti and its phylogenetic position within Sisoridae
Journal of Oceanology and Limnology, 41(1): 267-279
http://dx.doi.org/10.1007/s00343-021-1319-z

Article History

Received Oct. 12, 2021
accepted in principle Nov. 22, 2021
accepted for publication Dec. 29, 2021
The complete mitochondrial genome of Parachiloglanis hodgarti and its phylogenetic position within Sisoridae
Jiasheng LI1, Ying PENG1, Shufei ZHANG3, Yifan LIU1, Kun ZHANG1, Jian CHEN1, Hua ZHANG4, Chi ZHANG2, Bingjian LIU1     
1 National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, Zhoushan 316022, China;
2 Institute of Fisheries Science, Tibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa 850000, China;
3 Guangdong Provincial Key Laboratory of Fishery Ecology and Environment; South China Sea Fisheries Research Institute, Chinese Academy of Fisheries Sciences, Guangzhou 510300, China;
4 Key Laboratory of Tropical Marine Bio-resources and Ecology, Chinese Academy of Sciences, Guangzhou 510301, China
Abstract: The complete mitogenome of Parachiloglanis hodgarti was sequenced and characterized, which is the first mitogenome of the genus Parachiloglanis within Sisoridae. The mitogenome is 16 511-bp long and included 13 protein-coding genes, 22 transfer RNAs, two ribosomal RNAs, and one control region. The genome composition was A+T biased (58.64%) and exhibited a positive AT-skew (0.095) and a negative GC-skew (-0.283). Compared with other Sisoridae fishes, the characteristics of nucleotide skews, codon usage, and amino acid usage of the P. hodgarti mitogenome are more similar to those of non-Glyptosternoid fishes. Furthermore, the phylogenetic trees show that Sisoridae fishes fall into four major clades and P. hodgarti (Clade Ⅰ) is basal to the Sisoridae family, forming a sister clade to the Glyptosternoids (Clade Ⅳ). The topological structures constructed in this study raised doubts over the traditional classification system. These results will help better understand the features of the P. hodgarti mitogenome and provide a reference for further phylogenetic research on Sisoridae species.
Keywords: Parachiloglanis hodgarti    mitogenomes    Sisoridae    glyptosternoids    phylogenetic relationship    
1 INTRODUCTION

The mitochondrion, the main site of oxidative phosphorylation, and ATP production in eukaryotic cells can directly convert organic matter into energy to support the biological activity of cells (Goodsell, 2010). Mitochondrial DNA (mtDNA), a closed double-stranded circular present in the mitochondrion, is a relatively independent replication unit featured by small genome size, simple structure, maternal inheritance, high mutation rate, and limited recombination (Gyllensten et al., 1991; Clayton, 2000; Sato and Sato, 2013). Recent advances in sequencing technology, especially the next-generation sequencing technology, have facilitated the sequencing of fish mtDNA, providing a clearer picture of complete mitochondrial genome (mitogenome) (Fendt et al., 2009; Li et al., 2019). Besides, ribosomal RNA (rRNA), transfer RNA (tRNA), and protein-coding gene (PCG) are greatly conserved, and the spacing and lengths of genes vary in species (Gray, 1989; Ruan et al., 2020). Therefore, complete mitogenome is becoming a powerful tool for comparative genomics, evolutionary genomics, and reconstruction of phylogenetic relationships (Lu et al., 2020; Sharma et al., 2020; Sun et al., 2021).

Sisoridae, belonging to Siluriformes, is one of three broad fish lineages (including the schizothoracines and Triplophysa) commonly found in the Qinghai-Tibetan Plateau (Ma et al., 2015), which plays an important ecological role in plateau ecosystem. Most of the Sisoridae species and genera are highly adapted to the environment of the plateau (He et al., 2001). Glyptosternoid fishes, a natural group of Sisoridae, are limited to the rivers of the Qinghai-Tibetan Plateau and circumjacent regions, which are inhabitants of higher altitudes and adapt to the rapids. The historical biogeography of a lineage reflects aspects of the history in the region where the lineage is located (Montoya-Burgos, 2003; Chiachio et al., 2008). It is reported that the speciation of Glyptosternoids has a relationship with the three uplift intervals of the Qinghai-Tibet Plateau (He et al., 2001). Therefore, Sisoridae is an excellent biological model for studying the process of plateau uplift on the formation of water systems and the species differentiation process in complicated water systems by reconstructing the phylogenetic relationship (Peng et al., 2006).

Due to the extreme ecological diversity and high morphological similarity, classi fication, and phylogenetic relationships within this family are complicated and controversial (Norman, 1923; Hora and Silas, 1952; Ng, 2004; Kong et al., 2007), although previous studies have recovered species-level relationships in this family at molecular level (Guo et al., 2004, 2005). Unfortunately, several aspects of previously reported phylogenies are inconsistent. For example, Yu and He (2012) reported that the genus Pseudecheneis is basal to the Sisoridae family, but it is not consistent with the result that Pseudecheneis clusters with Glyptosternoids studied by Guo et al. (2007). Additionally, with the construction of a large number of hydropower stations and water conservancy projects, the ecological environment of rivers has been affected, including the living conditions of Sisoridae species (Zhou and Li, 2006). Therefore, more researches are needed for the development of genomic resources for source management and conservation of Sisoridae.

At present, no complete mitogenome from Parachiloglanis (Siluriformes: Sisoridae) has ever been reported. Most studies of Parachiloglanis focused on the classi fication based on morphological features (Thoni and Gurung, 2014), and there were few types of research on molecular level about this genus. In this study, the first complete mitogenome sequence of Parachiloglanis hodgarti was sequenced, annotated, and characterized. Additionally, the most comprehensive phylogenetic tree was constructed including 13 genera of Sisoridae and two species as outgroups based on 13 PCGs. The complete mitogenome of P. hodgarti will be of bene fit to understanding the phylogenetic relationships within Sisoridae.

2 MATERIAL AND METHOD 2.1 Sample collection and DNA extraction

An individual specimen of P. hodgarti was collected from Yarlung Zangbo River, Motuo, Tibet, China. The individual was morphologically identi fied by an experienced fisheries researcher. Muscle tissue was extracted and preserved in 95% ethanol until DNA extraction. Total genomic DNA was extracted using the salting-out method and the extracted DNA was stored at -20 ℃ until needed for PCR ampli fication.

2.2 Mitogenome sequencing and assembly

The next-generation sequencing was used to sequence the complete mitogenome of P. hodgarti. Briefly, an Illumin library with an insertion length of 400 bp was constructed. Then, the library was sequenced on an Illumina HiSeq X Ten platform to obtain 2×150-bp reads. FastQC (Andrews, 2010) and Trimmomatic (Bolger et al., 2014) were used to assess and clean the raw reads, respectively. Finally, we used the NOVOPlasty software (Dierckxsens et al., 2017) to de novo assemble the clean data without sequencing adapters. To examine the accuracy of the assembled sequence, the complete mitogenome of P. hodgarti was compared with other Sisoridae species by NCBI-BLAST searches (https://blast.ncbi.nlm.nih.gov/Blast.cgi) (Johnson et al., 2008).

2.3 Sequence annotation and analysis

Compared with other Sisoridae species, the assembled mitochondrial genes were annotated using the software of Sequin (version 13.70, http://www.ncbi.nlm.nih.gov/Sequin). The tRNA genes and their potential cloverleaf structures were identi fied using the online tool MITOS (http://mitos2.bioinf.uni-leipzig.de/index.py) (Bernt et al., 2013). The boundaries of rRNA genes were performed using NCBI-BLAST (http://blast.ncbi.nlm.nih.gov) (Johnson et al., 2008). The graphical map of mitogenome features of P. hodgarti was generated using the online tool CGView Server (Grant and Stothard, 2008). The nucleotide composition and the relative synonymous codon usage (RSCU) were analyzed by MEGA (version 10.1.8) (Kumar et al., 2018). The bias of nucleotide composition was calculated according to the following formulas: AT-skew=(A−T)/(A+T); GC-skew=(G−C)/(G+C) (Perna and Kocher, 1995).

2.4 Phylogenetic analysis

To reconstruct the phylogenetic relationships among Sisoridae, the complete mitogenome sequences of Sisoridae species were downloaded from the GenBank database (https://www.ncbi.nlm.nih.gov/genbank/), and two Cypriniformes species (Gymnocypris chui and Triplophysa baotianensis) are served as the outgroup (Table 1). We used the sequences of 13 PCGs of each mitogenome to construct maximum likelihood (ML) and Bayesian inference (BI) phylogenetic trees. The 13 PCGs are aligned through MAFFT (Katoh et al., 2002) and optimized by MACSE using default settings (Ranwez et al., 2011). The obtained alignment results are imported into Gblocks (Talavera and Castresana, 2007) to eliminate ambiguous sequences. Then the concatenated PCGs were performed for ML analysis with 10 000 bootstrap replicates in the software IQ-TREE and the most suitable model for building the ML tree was automatically determined by ModelFinder in the IQ-TREE package (Nguyen et al., 2015). Meanwhile, the best-fit evolutionary model is GTR+F+I+G4, which was selected for BI analysis using ModelFinder based on Bayesian Information Criterion (BIC) (Kalyaanamoorthy et al., 2017), and then BI tree was constructed using MrBayes 3.2.6 (Nylander et al., 2004) with the following conditions: two independent runs of 100 000 generations were conducted with sampling trees every 100 generations, four independent Markov chains, with the first 25% of samples discarded as burn-in. The resulting phylogenetic trees were visualized through the online tool iTOL (https://itol.embl.de/) (Letunic and Bork, 2021).

Table 1 Species analyzed in this study with their GenBank accession numbers
3 RESULT AND DISCUSSION 3.1 Genome organization and base composition

The closed-circular mitogenome of P. hodgarti is 16 511-bp long, including 13 PCGs, 22 tRNAs, two rRNAs, and one putative control region (D-loop) (Fig. 1). Among these 37 genes, the ND6 gene and eight tRNA genes (tRNA-Gln, Ala, Asn, Cys, Tyr, Ser, Glu, and Pro) are encoded on the light (L-) strand and the other genes are located in the heavy (H-) strand. Like other vertebrate mtDNAs, there are overlapping and non-coding bases among genes (Table 2) (Shao et al., 2016; Li, 2017; Zhu et al., 2019). The structure of the mitogenome of P. hodgarti is consistent with the Sisoridae family without gene rearrangement (Zhou et al., 2012; Li et al., 2016; Huang et al., 2017). The overall base composition of the mitogenome is as follows: A=32.11%, T=26.53%, G=14.82%, and C=26.54%, with highly A+T biased (58.64%). The mitogenome of P. hodgarti show a positive AT-skew value (+0.095) and a negative GC-skew value (-0.283) (Table 3), which is consistent with other Sisoridae fishes (Fig. 2a). Based on the result of nucleotide skewness of whole mitogenomes of the Sisoridae family, P. hodgarti is more similar to the non-Glyptosternoid fishes (Fig. 2a).

Fig.1 Circular mitochondrial genome map of P. hodgarti The larger circle indicates the gene arrangement and distribution. Genes encoded by the H-strand and L-strand are displayed in outside and inner rings, respectively. The smaller circle indicates GC- and AT-skew distribution using a 50-bp sliding window.
Table 2 Features of the mitochondrial genome of P. hodgarti
Table 3 Nucleotide composition and skewness of P. hodgarti
Fig.2 Nucleotide skews, amino acid usage, and codon usage of the Sisoridae family a. comparison of nucleotide skews of whole genomes; b. comparison of nucleotide skews of protein-coding genes (PCGs); c. principal component analysis (PCA) of amino acid usage in the PCGs; d. PCA of relative synonymous codon usage (RSCU) in PCGs.
3.2 Protein-coding genes and codon usage

The total length of the PCGs is 11 407 bp, accounting for 69.09% of P. hodgarti mitogenome. The A+T content of the PCGs is 58.47%, and the individual PCGs range 53.83% (cytochrome c oxidase subunit 3 (COIII))–65.48% (ATP8) (Table 3). The AT-skew and GC-skew values of the PCGs are +0.013 and -0.271, respectively, which is in correspondence with those of other Sisoridae species (Fig. 2b). Most of these PCGs start with an ATG initiation codon, except for cytochrome c oxidase subunit 1 (COI) with a GTG (Table 2). As for the stop codon, nine PCGs performed the routine termination codon (TAA or TAG), whereas four other PCGs (COII, COIII, ND4, and Cyt b) stopped with an incomplete stop codon T (Table 2). The truncated stop codons are commonly recognized in the vertebrate mitogenomes, which would become complete stop codons upon subsequent polyadenylation (Ki et al., 2010; Temperley et al., 2010).

A total of 3 792 amino acids were encoded in the PCGs of P. hodgarti mitogenome (Table 2). The amino acid usage pattern analysis of PCGs showed that Leu (16.43%), Thr (8.70%), Ala (8.65%), and Ile (7.89%) are the most frequently used, while the least amino acids are Cys (0.71%), Arg (1.95%), Asp (1.95%), and Lys (2.22%) (Fig. 3a). The RSCU is a widely used measurement for each codon usage bias of each amino acid, and an RSCU value > 1 indicates that there is a bias for that codon (Sharp and Li, 1986). As shown in Fig. 3b, the usage of synonymous codons is biased for most amino acids. Signi ficantly, the RSCU values of CGA (Arg), CUA (Leu), and UCA (Ser) are greater than 2. Previous studies show that codon usage is related to gene length, gene expression level, and protein sequences (Sharp and Matassi, 1994; Gustafsson et al., 2004). Hence, the differences in codon usage frequency might be correlated with natural selection among species. The principal component analyses (PCA) of amino acid usage and RSCU suggest that the codon usage pattern of Glyptosternoid fishes is different from those of non-Glyptosternoid fishes, and the codon usage pattern of P. hodgarti is more similar to those of non-Glyptosternoid fishes (Fig. 2cd).

Fig.3 Amino acid composition (a) and relative synonymous codon usage (RSCU) (b) in P. hodgarti mitogenome
3.3 Transfer RNAs and ribosomal RNAs

The 22 tRNAs (total length 1 566 bp) were identi fied in the mitogenome of P. hodgarti, ranging from 67 bp (tRNA-Cys) to 75 bp (tRNA-Leu) in length and presenting a regular AT bias (58.05%) (Tables 23). The AT-skew and GC-skew of total tRNAs are +0.032 and +0.020, respectively, showing a slight bias toward the use of As and Gs (Table 3). The anticodons of all the tRNAs recognized in the mitogenome of P. hodgarti are identical to most bony fishes (Wang et al., 2016; Rui et al., 2018). Additionally, two types of anticodons (UAA, UAG) determined the Leu and two types of anticodons (UGA, GCU) determined the Ser, which are commonly detected in bony fishes (Cui et al., 2017; Siva et al., 2018). All of the tRNAs could be folded into canonical cloverleaf secondary structures except for tRNA-Ser 2 (GCU), which lacks the entire dihydrouridine arm (Fig. 4). The unusual structure of the tRNA-Ser is commonly witnessed in other vertebrate mitogenomes (Yang et al., 2018; Zhang et al., 2019). The 12S rRNA and 16 rRNA genes are 954 bp and 1 666 bp, respectively, which are typically separated by tRNA-Val (Fig. 1). The total A+T content of two rRNAs is 57.48%, and the AT-skew and GC-skew are +0.226 and -0.111, respectively (Table 3), indicating more As and Cs than Ts and Gs.

Fig.4 Predicted secondary cloverleaf structure of the 22 tRNAs Yellow: adenine (A); blue: Uracil (U); red: guanine (G); green: cytosine (C).
3.4 Phylogenetic analysis

The phylogenetic relationship of Sisoridae has always been controversial. The morphology-only phylogeny of the sisorid fishes indicates that the Sisoridae is composed of two monophyletic clades: Glyptosternoids and Sisorinae (non-Glyptosternoids) (Ng, 2015). However, the monophyly of Sisoridae is supported by analyses of 16S rRNA (Guo et al., 2004), RAG2 nuclear gene + COI (Ng and Jiang, 2015), 12 mitochondrial genes (excluding ND6) + two rRNA genes (Ma et al., 2015), and 13 mitochondrial genes (Lv et al., 2018). In this study, two phylogenetic trees (ML and BI) were constructed based on the sequences of 13 PCGs including 13 genera in the Sisoridae (37 species) and two outgroup species. The results show that both ML and BI trees are largely congruent in the topological structure, and Sisoridae and Glyptosternoids are strongly supported to form the monophyly, respectively (Fig. 5), suggesting that the uplift of the Qinghai-Tibetan Plateau had a crucial impact on Sisoridae speciation (Peng et al., 2006). Interestingly, the phylogenetic trees show that the Sisoridae family falls into four major clades (Fig. 5). P. hodgarti fell separately into Clade Ⅰ, which is basal to the Sisoridae. The Clade Ⅱ includes the genus Pseudecheneis, and the Clade Ⅲ includes the genera Glyptothorax, Gagata, and Bagarius. The Glyptosternoid fishes, genera Glyptosternon, Glaridoglanis, Chimarrichthys, Pareuchiloglanis, Oreoglanis, Pseudexostoma, Exostoma, and Creteuchiloglanis, cluster into Clade Ⅳ.

Fig.5 Phylogenetic trees inferred from the nucleotide sequences of 13 mitogenomes protein-coding genes (PCGs) based on maximum likelihood (ML) analysis (left) and Bayesian inference (BI) analysis (right) The number after the species name is the GenBank accession number. P. hodgarti was indicated with a red star. *: the sequence (KT983411) identi fied as Bagarius yarrelli was changed to the sequence of B. rustilus since the specimen was collected from the Honghe River, and only B. rutilus is known from the Red River (Yuanjiang River) drainage (Du et al., 2016). Besides, B. yarrelli is demonstrated a junior synonym of B. bagarius (Ng and Kottelat, 2021); **: the genus name Euchiloglanis is corrected because Euchiloglanis is a junior synonym of Chimarrichthys (Kottelat, 2013).

The real systematic classi fication of P. hodgarti still remains controversial. In 1923 (Norman, 1923), P. hodgarti was classi fied into the genus Glyptosternon and later classi fied into the genus Euchiloglanis in 1952 (Hora and Silas, 1952). Subsequently, Wu et al. (1981) classi fied P. hodgarti into a new genus Parachiloglanis, and both Yang (2006) and Ng (2015) supported that P. hodgarti was one of Glyptosternoid fishes in morphology. However, the phylogenetic trees shows that the P. hodgarti (Clade Ⅰ) forms a sister clade to Glyptosternoids (Clade Ⅳ) (Fig. 5), which presents an inconsistent viewpoint in the traditional classi fication system, rejecting the arrangement that P. hodgarti is one of Glyptosternoids. The characteristics of nucleotide skews, codon usage, and amino acid usage of P. hodgarti mitogenome analyzed in this study also indicate that P. hodgarti has a closer relationship with the non-Glyptosternoid fishes (Fig. 2). In addition, we revealed that the basal species of the Sisoridae family is the P. hodgarti, which is inconsistent with previous studies that the genus Pseudecheneis is basal to the Sisoridae (Ma et al., 2015; Lv et al., 2018). The genus Pseudecheneis is regarded as one of Glyptosternoid fishes based on the most comprehensive sampling of morphological characters in the Sisoridae to date (Ng, 2015) and nuclear and mtDNA sequences (Ng and Jiang, 2015). However, the placement of the two genera Pseudecheneis and Parachiloglanis inferred from sequences is unstable in tree topology (Ng and Jiang, 2015). In our analyses, Parachiloglanis (Clade Ⅰ) and Pseudecheneis (Clade Ⅱ) are strongly recovered as sister taxa, and Pseudecheneis (Clade Ⅱ) forms a sister clade to Glyptosternoid fishes (Clade Ⅳ), suggesting that the genus Pseudecheneis should be considered as non-Glyptosternoids. In Clade Ⅲ, Gagata dolichonema and the genus Glyptothorax cluster, which is inconsistent with previous studies that the genus Gagata is monophyletic and forms a sister clade to the genus Glyptothorax (Ng, 2015; Ng and Jiang, 2015). In clade Ⅳ, Glyptosternon maculatum is basal to the remainder of the Glyptosternoids. Besides, these species of genera Glaridoglanis, Pareuchiloglanis, Chimarrichthys, and Pseudexostoma cluster, indicating that these genera may require an elaborate taxonomic revision. Compared with the study of Ng and Jiang (2015), the taxon sampling analyzed in this study is limited. Insufficient taxon sampling is often cited as a signi ficant source of error in phylogenetic studies. For example, it may cause unrelated branches to incorrectly group together (Nei, 1996). On the other hand, longer sequences could better improve the accuracy of phylogenetic inferences rather than extensive sampling (Rosenberg and Kumar, 2001). In summary, our results provide a new insight into the understanding of phylogenetic relationships of Sisoridae based on 13 PCGs. Morphology-based phylogeny of Sisoridae fishes may be not robust as these species are morphologically similar. Therefore, more complete mitogenomes of Sisoridae are required to sequence, which is important to resolve the phylogeny of Sisoridae.

4 CONCLUSION

Having sequenced and characterized the complete mitogenome of P. hodgarti, the first mitogenome of the genus Parachiloglanis within Sisoridae, we find that the mitogenome of P. hodgarti is 16 511 bp in length and the genome features are similar to non-Glyptosternoid fishes. Based on 13 PCGs, both ML and BI phylogenetic trees show a four-clade topological structure of the Sisoridae family. P. hodgarti (Clade Ⅰ) is basal to the Sisoridae family and formed a sister clade to the Glyptosternoids (Clade Ⅳ), which is inconsistent with the traditional classi fication system. In addition, the phylogenetic trees indicate that the Glyptosternoid species may require an elaborate taxonomic revision. The complete mitogenome of P. hodgarti would be a valuable source for further studies on molecular taxonomy, phylogenetic relationship, genetic diversity, and species conservation within the Sisoridae family.

5 DATA AVAILABILITY STATEMENT

The genome sequence data that support the findings of this study are openly available in GenBank of NCBI at (https://www.ncbi.nlm.nih.gov/nuccore/MW715684) under the accession number: MW715684.

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