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Carinotetraodon Travancoricus) Endemic to Southwest India and Its Implications in the Phylogeny of Tetraodontidae

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Carinotetraodon Travancoricus) Endemic to Southwest India and Its Implications in the Phylogeny of Tetraodontidae Journal of Genetics (2019) 98:105 Ó Indian Academy of Sciences https://doi.org/10.1007/s12041-019-1151-9 (0123456789().,-volV)(0123456789().,-volV) RESEARCH ARTICLE Mitogenome analysis of dwarf pufferfish (Carinotetraodon travancoricus) endemic to southwest India and its implications in the phylogeny of Tetraodontidae CHANDHINI SATHYAJITH1, YUSUKE YAMANOUE2, SHIN-ICHI YOKOBORI3, SUNESH THAMPY4 and REJISH KUMAR VATTIRINGAL JAYADRADHAN1* 1Department of Aquaculture, Kerala University of Fisheries and Ocean Studies, Panangad 682 506, India 2The University Museum, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan 3School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, Japan 4Planet Earth Aquarium, Mysuru 571 606, India *For correspondence. E-mail: [email protected]. Received 26 March 2019; revised 12 July 2019; accepted 23 August 2019; published online 15 November 2019 Abstract. The Tetraodontidae (pufferfishes), is primarily a family of marine and estuarine fishes with a limited number of freshwater species. Freshwater invasions can be observed in South America, Southeast Asia and central Africa. In the present study, we have analysed the complete mitogenome of freshwater pufferfish, Carinotetraodon travancoricus (dwarf pufferfish or Malabar pufferfish) endemic to southwest India. The genome is 16487 bp in length and consist of 13 protein-coding genes, 22 transfer RNA genes, two ribosomal RNA genes and one control region like all the other vertebrate mitogenomes. The protein-coding genes ranged from 165 bp (ATP synthase subunit 8) to 1812 bp (NADH dehydrogenase subunit 5) and comprised of 11310 bp in total, constituting 68.5% of the complete mitogenome. Some overlaps have been observed in protein-coding genes by a total of 7 bp. The AT skew (0.032166) and GC skew (-0.29746) of the mitogenome indicated that heavy strand consists equal amount of A and T, but the overall base composition was mainly C skewed. The noncoding D-loop region comprised 869 bp. The conserved motifs ATGTA and its complement TACAT associated with thermostable hairpin structure formation were identified in the control region. The phylogenetic analysis depicted a sister group relationship of C. travancoricus with euryhaline species Dichotomyctere nigroviridis and D. ocellatus with 100% bootstrap value rather than with the other freshwater members of Carinotetraodon species from Southeast Asia. The data from this study will be useful for proper identification, genetic differentiation, management and conservation of the dwarf Indian pufferfish. Keywords. dwarf pufferfish; Malabar pufferfish; mitogenome; phylogenetic analysis; Tetraodontidae; Carinotetraodon travancoricus. Introduction million years ago (Alfaro et al. 2007). Various evolutionary studies have been conducted to elucidate the causes of Tetraodontiforms are widely distributed in freshwater, deep diversification of pufferfishes (Yamanoue et al. 2011; Santini sea, coastal, open water pelagic and reef habitat, especially et al. 2013). Tetraodontid pufferfishes have caught the across the tropical seas of South America, central Africa and attention of many researchers in various fields, because of Southeast Asia. They consist of 10 extant families and 349 their morphological peculiarity, tetrodotoxin and as a model species in which Tetraodontidae family (pufferfish) is rep- organism in molecular biology research (Hedges 2002). resented by 29 genera with 191 species (Tyler 1980; Although several studies on pufferfish phylogeny have been Yamanoue et al. 2011; Matsura 2015). Tetraodontids were conducted, the phylogenetic status of many species is still said to have diverged from diodontids between 89 and 139 obscure. Exploring mitochondrial genome sequencing of Electronic supplementary material: The online version of this article (https://doi.org/10.1007/s12041-019-1151-9) contains supplementary material, which is available to authorized users. 1 105 Page 2 of 11 S. Chandhini et al. pufferfish has significant implications in investigating its Long AMP Taq DNA polymerase. The library was prepared evolutionary aspects because of its unique mitochondrial by NEB Next Ultra DNA library prep kit. The product was features (Boore 1999; Boore et al. 2005). Yamanoue et al. then sequenced on HiSeq 2500 in Rapid Run V2 Chemistry (2011) performed whole mitochondrial genome sequencing (2 x 250 bp PE). A total of 366,252 reads were generated of 50 tetraodontid species and described four main lineages, and processed before performing de novo whole genome two of which included freshwater fishes from different assembly. First, the Illumina adapter sequences were continent. Southeast Asian freshwater pufferfishes con- removed from the reads using Cutadapt, further, low-quality sist *21 species and are represented by four lineages bases (Phred score, Q [ 20) were trimmed using sickle, and Carinotetraodon spp. (south India to Sunda Islands), Aur- duplicate reads were removed from the data using FastUniq. iglobus spp. (Indochina, Malay peninsula and Sunda The preprocessed paired end reads were assembled using Islands), Tetraodon cutcutia (east India to Myanmar), and IVA 1.0.8 (Hunt et al. 2015). Then SEQuel (Ronen et al. other Tetraodon species (Indochina, Malay peninsula and 2012) was used for correcting errors (i.e. insertions, dele- Sunda Islands) (Ebert 2001). Among the freshwater puffer- tions and substitutions) in the assembled contigs. fishes, Carinotetraodon imitator, C. travancoricus and Te- traodon cutcutia are endemic to Indian subcontinent (Yamanoue et al. 2011). Mitogenome analysis The Carinotetraodon is a genus of small freshwater South Asian pufferfishes consisting of six species: C. borneensis, The assembled mitochondrial genome was annotated using C. imitator, C. irrubesco, C. lorteti, C. salivator and C. MITOS Webserver (Bernt et al. 2013). Annotation of the travancoricus. Among them, C. travancoricus and C. imi- transfer RNA (tRNA) was conducted using tRNA scan-SE tator are endemic to southwest India. C. travancoricus is (Lowe and Chan 2016). The codon usage of the 13 protein- mainly distributed in Chalakudy, Pamba, Periyar, Kabani, coding genes was summarized using MEGA 7 (Kumar et al. Bharathapuzha and Muvattupuzha rivers (Beevi and 2016). Statistical analysis of distributions and visualization of Ramachandran 2009), lake Vembanad and kole wetlands of codon usage was performed with heatmapper (Babicki et al. Thrissur, Kallar stream and Neyyar wildlife sanctuary of 2016). The AT-skew [(A - T)/ (A ? T)] and GC-skew south Kerala (Prasad et al. 2012). Due to its ovoid body [(G - C)/ (G ? C)] values were used to calculate the shape, colour and puppy dog eyes, this fish has been mar- nucleotide compositional differences among the genes. Sum- keted as aquarium fish (Jayalal and Ramachandran 2013), mary statistics including gene boundaries and length, strand, but due to the overexploitation and habitat loss IUCN has nucleotide composition, intergenic nucleotides and the number categorized it as ‘vulnerable’ (Dahanukar 2011). The present of genes were analysed. The conserved motif in the noncoding study undertook sequencing and analyses of the complete region and P genetic distance were studied using MEGA7. mitochondrial genome of freshwater dwarf Indian pufferfish, AlongwiththeC. travancoricus mitogenome, complete C. travancoricus, to get a deeper insight into mitochondrial mitogenomes of C. lorteti and C. salivator were obtained from genome structure, evolution, phylogeny and conservation. NCBI which were used for comparative analysis. The mitochondrial genome data could be useful to establish the proper phylogenetic position of C. travancoricus. Phylogenetic analysis Materials and methods The complete mitochondrial sequences of C. travancoricus was added to those of 50 tetraodontids plus three outgroups, Amplification and sequencing of the mitogenome a triodontid Triodon macropterus and two molids, Mola mola and Ranzania laevis, all were used in Yamanoue et al. The C. travancoricus collected from Periyar river, Kerala, (2011) (table 1 in electronic supplementary material at http:// India was used for the analysis. Total genomic DNA was www.ias.ac.in/jgenet/). The dataset was aligned using extracted from the fins using the DNeasy tissue kit (Qiagen, MAFFT v.7 (Katoh and Standley 2013) and the aligned Germany). Long polymerase chain reaction (PCR) was sequences were trimmed using trimAL (Capella-Gutie´rrez carried out to elucidate the complete mitogenome sequence et al. 2009). Based on the patterns of sequence variations, of C. travancoricus. Different homology-degenerate primers the dataset with the third codon positions converted by RY- were designed based on the aligned mitogenome sequences coding (12n3rRTn) was expected to effectively remove the of C. lorteti (GenBank: AP011918) and C. salivator (Gen- likely noise from quickly saturated transitional changes in Bank: AP011918). Approximately 100 ng of DNA sample the third codon positions (Phillips and Penny 2003). was used for PCR. The PCR cycle consisted of an initial Accordingly, two datasets of 123nRTn and 12n3rRTn were denaturation step at 94°C for 30 s, followed by 30 cycles of prepared and subjected to the phylogenetic analysis. Phy- denaturation at 94°C for 20 s, annealing at 59°C for 30 s and logenetic relationships were inferred using maximum like- extension at 65°C for 7 min. A final extension was carried lihood method (ML) by RAxML v.8 (Stamatakis 2014) with out at 65°C for 10 min. Amplification
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