Characterization of the complete mitochondrial genome of Metastrongylus salmi (M. salmi) derived from Tibetan pigs in Tibet, China
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Kun Li
Abstract
The present study was designed to determine and analyze the mt genomes of Metastrongylus salmi (M. salmi), and reveal the phylogenetic relationships of this parasite using mt DNA sequences. Results showed that the complete mt genome of M. salmi was 13722 bp containing 12 protein-coding genes (cox1-3, nad1-6, nad4L, atp6 and cytb), 22 transfer RNA genes, and 2 ribosomal RNA genes (rrnL and rrnS). The overall A+T content was 73.54% and the nucleotide composition was A (23.52%), C (6.14%), G (19.60%), T (50.02%), and N (UCAG) (0.73%). A total of 4237 amino acids are encoded from the Tibetan isolates of M. salmi mt genomes. The ATA was predicted as the most common starting codon with 41.7% (5/12 protein genes); and 11 of the 12 protein genes were found to have a TAG or TAA translation termination codon. By clustering together the phylogenetic trees of Tibetan M. salmi and Austrian M. salmi, the M. salmi isolated from Tibetan pigs was found to be highly homological with that stemmed from Austrian one. This information provides meaningful insights into the phylogenetic position of the M. salmi China isolate and represents a useful resource for selecting molecular markers for diagnosis and population studies.
Acknowledgments
The current research was supported by the Key Science Fund of Science and Technology Agency of Tibet Autonomous Region and projects in the National Science & Technology Pillar Program during the 12th Five-year Plan Period (2012BA D3B03). Kun Li is supported by China Scholarship Council under Grant No. 201706760018.
Conflict of interest: The authors state that there are no competing interests.
Ethics statement: All procedures were performed in accordance with the laws, regulations, and strict guidelines of the Laboratory Animals Research Centre of Hubei province, P. R. China. Samples were collected with the permission of the relevant institutions and by following the parameters as set by the ethics committee of Huazhong Agricultural University (Permit number: 4200695757).
References
Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215, 403–41010.1016/S0022-2836(05)80360-2Suche in Google Scholar PubMed
Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. 2000. Gene Ontology: tool for the unification of biology. Nature Genetics, 25, 25–2910.1038/75556Suche in Google Scholar PubMed PubMed Central
Benson G. 1999 Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research, 27, 573–58010.1093/nar/27.2.573Suche in Google Scholar PubMed PubMed Central
Borgstrom E., Lundin S., Lundeberg J. 2011. Large scale library generation for high throughput sequencing. PLoS One, 6, e19119. DOI: 10.1371/journal.pone.001911910.1371/journal.pone.0019119Suche in Google Scholar PubMed PubMed Central
Chiaromonte F., Yap V.B., Miller W. 2002. Scoring pairwise genomic sequence alignments. Pacific Symposium on Biocomputing, 7, 115–12610.1142/9789812799623_0012Suche in Google Scholar PubMed
Cronn R., Liston A., Parks M., Gernandt D.S., Shen R.K. 2008. Multiplex sequencing of plant chloroplast genomes using Solexa sequencing-by-synthesis technology. Nucleic Acids Research, 36, e12210.1093/nar/gkn502Suche in Google Scholar PubMed PubMed Central
Durent L., Mouchiroud D. 1999. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila and Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 96, 4482–448710.1073/pnas.96.8.4482Suche in Google Scholar PubMed PubMed Central
García-González Á.M., Pérez-Martín J.E., Gamito-Santos J.A., Calero-Bernal R., Alonso M.A., Carrión E.M. 2013. Epidemiologic study of lung parasites (Metastrongylus spp.) in wild boar (Sus scrofa) in southwestern Spain. Journal of Wildlife Disease, 49, 157–162. 10.7589/2011-07-217Suche in Google Scholar PubMed
Gassó D., Rossi L., Mentaberre G., Casas E., Velarde R., Nosal P., et al. 2014. An identification key for the five most common species of Metastrongylus. Parasitology Research, 113, 3495–3500. 10.1007/s00436-014-4001-ySuche in Google Scholar PubMed
Helfenbein K.G., Brown W.M., Boore J.L. 2001. The complete mitochondrial genome of the articulate brachiopod Terebratalia transversa. Molecular Biology and Evolution, 18, 1734–174410.1093/oxfordjournals.molbev.a003961Suche in Google Scholar PubMed
Hu M., Chilton N.B., Gasser R.B. 2003. The mitochondrial genome of Strongyloides stercoralis (Nematoda)-idiosyncratic gene order and evolutionary implications. International Journal of Parasitology, 33, 1393–140810.1016/S0020-7519(03)00130-9Suche in Google Scholar
Humbert J.F., Drouet J. 1990. Enquête épidémiologique sur la métastrongylose du sanglier (Sus scrofa) en France. Gibier Faune Sauvag, 7, 67–84. (In French)Suche in Google Scholar
Jex A.R., Hall R.S., Littlewood D.T., Gasser R.B. 2010. An integrated pipeline for next-generation sequencing and annotation of mitochondrial genomes. Nucleic Acids Research, 38, 522–533 Kanehisa M. 1997. A database for post-genome analysis. Trends in Genetics, 13, 37510.1093/nar/gkp883Suche in Google Scholar PubMed PubMed Central
Kanehisa M., Goto S., Hattori M., Aoki-Kinoshita K.F., Itoh M., Kawashima S., et al. 2006. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Research, 34, D354–D35710.1093/nar/gkj102Suche in Google Scholar PubMed PubMed Central
Kanehisa M., Goto S., Kawashima S., Okuno Y., Hattori M. 2004. The KEGG resource for deciphering the genome. Nucleic Acids Research, 32, D277–D28010.1093/nar/gkh063Suche in Google Scholar PubMed PubMed Central
Kurtz S., Phillippy A., Delcher A.L., Smoot M., Shumway M., Antonescu C., Salzberg S.L. 2004. Versatile and open software for comparing large genomes. Genome Biology, 5, R1210.1186/gb-2004-5-2-r12Suche in Google Scholar PubMed PubMed Central
Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., et al. 2009. The Sequence Alignment/Map (SAM) format and SAMtools. Bioinformatics, 25, 2078–207910.1093/bioinformatics/btp352Suche in Google Scholar PubMed PubMed Central
Li K., Lan Y.F., Luo H.Q., Shahzad M., Zhang H., Wang L., et al.2017a. Prevalence of three Oesophagostomum spp. from Ti-betan pigs analyzed by genetic markers of nad1, cox3 and ITS1. Acta Parasitologica, 62, 90–96. 10.1515/ap-2017-0010Suche in Google Scholar PubMed
Li K., Luo H.Q., Zhang H., Lan Y.F., Han Z.Q., Shahzad M., et al.2016. First report of Metastrongylus pudendotectus by the genetic characterization of mitochondria genome of cox1 in pigs from Tibet, China. Veterinary Parasitology, 223, 91–95. 10.1016/j.vetpar.2016.04.036Suche in Google Scholar PubMed
Li K., Zhang L.H., Zhang H., Lei Z.X., Luo H.Q., Mehmood K., et al.2017b. Epidemiology investigation and risk factors of Echinococcus granulosus in yaks (Bos grunniens), Tibetan pigs and Tibetans on the Qinghai Tibetan plateau. Acta Tropica 173, 147–152. 10.1016/j.actatropica.2017.06.019Suche in Google Scholar PubMed
Li M.W., Lin R.Q., Song H.Q., Wu X.Y., Zhu X.Q. 2008. The complete mitochondrial genomes for three Toxocara species of human and animal health significance. BMC Genomics, 9, 22410.1186/1471-2164-9-224Suche in Google Scholar PubMed PubMed Central
Li R., Zhu H., Ruan J., Qian W., Fang X., Shi Z., et al. 2010. De novo assembly of human genomes with massively parallel short read sequencing. Genome Research, 20, 265–27210.1101/gr.097261.109Suche in Google Scholar PubMed PubMed Central
Li X.R. (Ed.) 2011. Color atlas of animal parasitosis (2nd Edition). Beijing: China Agriculture PressSuche in Google Scholar
Lin R.Q., Liu G.H., Hu M., Song H.Q., Wu X.Y., Li M.Y., et al.2012. Oesophagostomum dentatum and Oesophagostomum quadrispinulatum: characterization of the complete mitochondrial genome sequences of the two pig nodule worms. Experimental Parasitology 131, 1–7. 10.1016/j.exp-para.2012.02.015Suche in Google Scholar PubMed
Lohse M., Drechsel O., Bock R. 2007. Organellar Genome DRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Current Genetics, 52, 267–27410.1007/s00294-007-0161-ySuche in Google Scholar PubMed
Magrane M. 2011. UniProt. Knowledgebase: a hub of integrated protein data. Databases-Oxford, 2011, 9. 10.1093/data-base/bar009Suche in Google Scholar
Marruchella G., Paoletti B., Speranza R., Di Guardo G. 2012. Fatal bronchopneumonia in a Metastrongylus elongatus and Porcine circovirus type 2 co-infected pig. Research in Veterinary Science, 93, 310–312. 10.1016/j.rvsc.2011.05.016Suche in Google Scholar PubMed
Romero H., Zavala A., Musto H. 2000. Codon usage in Chlamydia trachomatis is the result of strand-specific mutational biases and a complex pattern of selective force. Nucleic Acids Research, 28, 2084–209010.1093/nar/28.10.2084Suche in Google Scholar PubMed PubMed Central
Saha S., Bridges S., Magbanua Z.V., Peterson D.G. 2008. Empirical comparison of ab initio repeat finding programs. Nucleic Acids Research, 36, 2284–229410.1093/nar/gkn064Suche in Google Scholar PubMed PubMed Central
Singer G.A., Hickey D.A. 2000. Nucleotide bias causes a genomewide bias in the amino acid composition of proteins. Molecular Biology and Evolution, 17, 1581–158810.1093/oxfordjournals.molbev.a026257Suche in Google Scholar PubMed
Sorensen M., Sanz A., Gómez J., Pamplona R., Portero-Otín M., Gredilla R., Barja G. 2006. Effects of fasting on oxidative stress in rat liver mitochondria. Free Radical Research, 40, 339–34710.1080/10715760500250182Suche in Google Scholar PubMed
Tannistha N., Catherine O., Arvind P.S., Boddey J., Atkins T., Sarkar-Tyson M., et al. 2010. A genomic survey of positive selection in Burkholderia pseudomallei provides insights into the evolution of accidental virulence. PLoS Pathogens, 6, 1–1510.1371/journal.ppat.1000845Suche in Google Scholar PubMed PubMed Central
Tatusov R.L., Fedorova N.D., Jackson J.D., Jacobs A.R., Kiryutin B., Koonin E.V., et al. 2003. The COG database: an updated version includes eukaryotes. BMC Bioinformatics, 4, 4110.1186/1471-2105-4-41Suche in Google Scholar PubMed PubMed Central
Tatusov R.L., Koonin E.V., Lipman D.J. 1997. A genomic perspective on protein families. Science, 278, 631–63710.1126/science.278.5338.631Suche in Google Scholar PubMed
Wyman S.K., Jansen R.K., Boore J.L. 2004. Automatic annotation of organellar genomes with DOGMA. Bioinformatics, 20, 3252–325510.1093/bioinformatics/bth352Suche in Google Scholar PubMed
Zhang N.Z., Zhou D.H., Huang S.Y., Wang M., Shi X.C., Ciren D.B., Zhu X.Q. 2014. Seroprevalence and risk factors associated with Haemophilus parasuis infection in Tibetan pigs in Tibet. Acta Tropica, 132, 94–97. 10.1016/j.actatropica.2013.12.021Suche in Google Scholar PubMed
Zhao G.H., Hua B., Cheng W.Y., Jia Y.Q., Li H.M., Yu S.K., Liu G.H. 2013. The complete mitochondrial genomes of Oesophagostomum asperum and Oesophagostomum columbianum in small ruminants. Infection. Infection Genetics and Evolution, 19, 205–211. 10.1186/1756-3305-7-319Suche in Google Scholar PubMed PubMed Central
© 2018 W. Stefański Institute of Parasitology, PAS
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