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Complete Mitochondrial Genome of Threatened Mahseer Tor Tor (Hamilton 1822) and Its Phylogenetic Relationship Within Cyprinidae Family

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Complete Mitochondrial Genome of Threatened Mahseer Tor Tor (Hamilton 1822) and Its Phylogenetic Relationship Within Cyprinidae Family c Indian Academy of Sciences RESEARCH ARTICLE Complete mitochondrial genome of threatened mahseer Tor tor (Hamilton 1822) and its phylogenetic relationship within Cyprinidae family A. PAVAN-KUMAR1∗, SUDHANSHU RAMAN1, PRAKASH G. KORINGA2, NAMRATA PATEL2, TEJAS SHAH2, RAJEEV K. SINGH3, GOPAL KRISHNA1,C.G.JOSHI2, P. GIREESH-BABU1 and APARNA CHAUDHARI1 1Fish Genetics and Biotechnology Division, ICAR-Central Institute of Fisheries Education (Deemed University) ICAR, Mumbai 400 061, India 2Department of Animal Biotechnology, College of Veterinary Science and Animal Husbandry, Anand Agricultural University, Anand 388 110, India 3ICAR-National Bureau of Fish Genetic Resources, Canal Ring Road, Dilkusha PO, Lucknow 226 002, India Abstract The mahseers (Tor, Neolissochilus and Naziritor) are an important group of fishes endemic to Asia with the conservation status of most species evaluated as threatened. Conservation plans to revive these declining wild populations are hindered by unstable taxonomy. Molecular phylogeny studies with mitochondrial genome have been successfully used to reconstruct the phylogenetic tree and to resolve taxonomic ambiguity. In the present study, complete mitochondrial genome of Tor tor has been sequenced using ion torrent next-generation sequencing platform with coverage of more than 1000×. Compar- ative mitogenome analysis shows higher divergence value at ND1 gene than COI gene. Further, occurrence of a distinct genetic lineage of T. tor is revealed. The phylogenetic relationship among mahseer group has been defined as Neolissochilus hexagonolepis ((T. sinensis (T. putitora, T. tor), (T. khudree, T. tambroides)). [Pavan-Kumar A., Raman S., Koringa P. G., Patel N., Shah T., Singh R. K., Krishna G., Joshi C. G., Gireesh-Babu P. and Chaudhari A. 2016 Complete mitochondrial genome of threatened mahseer Tor tor (Hamilton 1822) and its phylogenetic relationship within Cyprinidae family. J. Genet. 95, 853–863] Introduction Taxonomically, mahseers are defined as carps with big head and scales, two pairs of barbles, fleshy lips that are con- Tor mahseer, Tor tor (Hamilton 1822) is one of the most tinuous at the angles of the mouth with an interrupted fold or important food and game fishes of India. It inhabits rivers groove across the lower jaw (Desai 2003). Initially, Hamilton of ‘Tor region’ (600–1200 m) and plains with rocky bot- (1822) classified mahseers under the genus ‘Cyprinus’, but tom (Singh and Kumar 2000). This species has been reported later, Gray (1834) proposed new genus ‘Tor’forthese from the Indus, Ganga (including sub-Himalayan range), species. Rainboth (1996) classified Tor species under the Brahmaputra, Godavari and Krishna riverine systems and family Cyprinidae, subfamily Cyprininae, tribe Cyprinini. forms major fishery in Narmada river (Desai 2003; Jayaram Thai et al. (2007) placed Tor species under tribe Barbini 2005; Lal et al. 2013). However, due to overfishing, habi- (interchangeably referred to as subfamily Barbinae by vari- tat destruction and other anthropogenic activities, the natural ous authors). The tribe name became more contentious after populations of this species are declining and the conserva- Yang et al. (2010) showed the polyphyletic nature of tribe tion status is evaluated as ‘near threatened’ (IUCN 2015). For Barbini within Cyprininae. formulating effective management and conservation mea- In India, information on mahseer genetic resources is sures, organisms need to be identified/delimited accurately. inconclusive and several studies using limited markers (COI But conversely, the systematics of mahseer fishes are highly and D-loop) showed misapplication of different species names ambiguous due to phenotype plasticity leading to taxonomic to diverse morphotypes of conspecific individuals (Laskar instability (Mohindra et al. 2007; Khare et al. 2014). et al. 2013; Khare et al. 2014). As a first step to address the taxonomic ambiguity of mahseer species, several studies have briefly described complete mitochondrial genomes of ∗ For correspondence. E-mail: [email protected]. T. putitora (Sati et al. 2014), T. khudree (Raman et al. 2015) and Keywords. mahseer; next generation sequencing; phylogeny; mitochondrial genome. Journal of Genetics, DOI 10.1007/s12041-016-0706-2, Vol. 95, No. 4, December 2016 853 A. Pavan-Kumar et al. T. tor (Kumar et al. 2015) with limited phylogenetic analysis. Amplicon sequencing by ion torrent NGS platform However, molecular phylogeny with more number of charac- DNA (amplicon) quality and quantity were measured using ters would generate accurate phylogenetic tree than limited Qubit 2.0 fluorometer. Around 500 ng of amplified product number of characters. Kumar et al. (2015) reported complete was digested using ultrasonification to get the desired frag- mitochondrial genome of T. tor, but their study was limited ment size of 400 bp. The fragment’s quality and quantity to brief description of mitogenome and partial phylogeny. were verified by Bioanalyzer and were purified by AMPure Further, molecular phylogeny with conspecific individuals bead purification. Adapter ligation, size selection, nick repair from different geographical locations would give insight on and amplification were performed as described in the ion tor- speciation and evolution of genetic lineages. Additionally, rent protocol. Library preparation was carried out using the comparative analysis of mitogenome could provide leads on Ion XpressTM Fragement Library kit (ThermoFisher Scientfic, pattern of amino acid usage and gene evolution among mah- MA, USA), with 500 ng of DNA and a different barcode seer fishes. With this back ground, the present study was adaptor was used for each library (barcode series 53 and 54 carried with an objective of characterizing complete mito- for T. tor specimens 1 and 2, respectively). After appropriate chondrial genome of T. tor to infer its phylogenetic position dilution, the two libraries were pooled in equimolar concen- within mahseer group. tration. Emulsion PCR and enrichment steps were carried out using the Ion XpressTM Template kit and associated proto- Materials and methods col. Libraries were sequenced using 314 chip and the reads obtained from ion torrent sequencer were grouped according Sample collection to their barcodes into two separate files. Two samples of T. tor (Hamilton 1822) (figure 1 in elec- tronic supplementary material at http:www.ias.ac.in/jgenet/) Data analysis were collected from Narmada river (Hoshangabad, 77◦74E, ◦ After checking the quality, raw reads were trimmed, aligned 22 76 N) during the month of April 2015. The species were identified at the field by observing morphological and meris- to contigs and the resulted contigs were mapped against tic characters (Desai 2003). Voucher specimens were pre- T. putitora reference mitogenome (GenBank: NC_021755.1), pared by preserving the specimen in absolute alcohol with using CLC Genomic Workbench ver. 5.0. Assembled mitogeno- proper labelling. Fins were collected under aseptic condi- me was annotated using MITOFISH (MitoAnnotator) online tions and preserved in absolute alcohol and kept at −80◦Cfor mitochondrial genome annotation server (Iwasaki et al. 2013). further analysis. For phylogenetic and comparative analyses, The ribosonal RNA (rRNA) gene boundaries were con- reported mitochondrial DNA sequences of mahseer species firmed by alignment with other reported fish mitogenomes. were downloaded from NCBI, GenBank. The transfer RNA (tRNA) structures were predicted using ‘tRNAscan’ web server (Schattner et al. 2005) with a search mode ‘tRNAscan only’ using vertebrate mitochon- DNA extraction and long PCR amplification drial genetic code. The origin of replication on L strand OL Total genomic DNA was isolated from the fins using region was predicted using online ‘Mfold’ software (Zuker standard phenol/chloroform method. Whole mitochondrial 2003). The sequences were analysed for base composition, genome was amplified in two amplicons using two sets of variation using MEGA6 (Tamura et al. 2013). The DAMBE5 reported primers L-1231-Leu: 5-GGTCTTAGGAACCAA software was used to test the sequence substitution satura- AAACTCTTGGTGCAA-3 and S-LA-16S-H: 5-TGCAC tion (Xia 2013), and DnaSp5 software was used to calculate CATTAGGATGTCCTGATCCAACATC-3; H-12321-Leu: the divergence between mitogenomes using sliding window 5-TTGCACCAAGAGTTTTTGGTTCCTAAGACC-3 and analysis (Rozas 2009). Codon usage analysis was done S-LA-16S-L: 5-GATGTTGGATCAGGACATCCCAATGG using MEGA6 and the heatmap of codon usage was pre- TGCA-3 (Kim and Lee 2004). Long range polymerase chain pared using online tool ‘CIMminer’ (http://discover.nci.nih. reaction (PCR) was carried out in a 20 μL reaction mix- gov/cimminer/home.do). The evolutionary models were esti- ture containing 9.7 μL sterile distilled water, 2 μLof10× mated using jModelTest 2 software (Guindon and Gascuel clean α-Taq reaction buffer, 4 μLof5× HQ buffer, 2 μL 2003; Darriba et al. 2012). PAUP ver. 4.0 (Swofford 2003) of dNTPs mix, 1 μL of each primer and 0.3 μL of clean was used to reconstruct the phylogenetic tree using parsi- α-Taq DNA polymerase (Krishgen Biosystems, USA) and mony (MP), maximum likelihood (ML) and neighbour join- 2 μL of template DNA using a Bio-Rad iCycler PCR ing (NJ) methods. Nonparametric bootstrap support for each machine in 0.2 mL PCR tubes. The thermocycler was pro- node of the tree was estimated using 100 heuristic boot- grammed for initial denaturation at 95◦C for 3 min, followed strap replicates. Bayesian inference (BI) was implemented by 40 cycles of 95◦C
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