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Molecular characterization of Opisthorchis noverca (Digenea: Opisthorchiidae) based on nuclear ribosomal ITS2 and mitochondrial COI genes

Published online by Cambridge University Press:  15 October 2015

R. Sahu ,
D.K. Biswal ,
B. Roy  and
V. Tandon
R. Sahu
Affiliation:
Department of Zoology, North-Eastern Hill University, Shillong-793022, Meghalaya, India
D.K. Biswal
Affiliation:
Department of Zoology, North-Eastern Hill University, Shillong-793022, Meghalaya, India
B. Roy
Affiliation:
Department of Zoology, North-Eastern Hill University, Shillong-793022, Meghalaya, India
V. Tandon*
Affiliation:
Department of Zoology, North-Eastern Hill University, Shillong-793022, Meghalaya, India
*
*E-mail: tandonveena@gmail.com
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Abstract

Opisthorchiasis is a public health problem in South-East Asian countries and Eastern Europe. The infection implicates mainly two species of Opisthorchis, namely O. viverrini and O. felineus, that occur mostly in fish-eating mammals and humans, although there are rare reports of human cases involving two other species, O. noverca and O. guayaquilensis. Opisthorchis noverca has been reported frequently in dogs and pigs from the Indian subcontinent, with rare reports from cattle and human subjects. With a view to supplementing morphology-based identification of this species, the present study aimed to provide molecular characterization of O. noverca, using rDNA internal transcribed spacer 2 (ITS2) and mitochondrial cytochrome oxidase I (mt COI) markers so as to determine its genetic correlation with other species of Opisthorchiidae, and also to generate a taxon-specific molecular marker based on the ITS2 region. The phylogenetic relationship between O. noverca and other species of the genus was determined using molecular sequence data. To strengthen the result, secondary structure sequence analyses of ITS2 with hemi-compensatory base changes (hCBCs), and amino acid sequence analyses, were also evaluated. Our results confirm that O. noverca is a distinct and valid species.

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 5 , September 2016 , pp. 607 - 614
Copyright
Copyright © Cambridge University Press 2015 

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References

Ando, K., Sithithaworn, P., Nuchjungreed, C., Tesana, S., Srisawangwong, T., Limviroj, W. & Chinzei, Y. (2001) Nucleotide sequence of mitochondrial COI and ribosomal ITS II genes of Opisthorchis viverrini in northeast Thailand. Southeast Asian Tropical Medicine and Public Health 32, 17–22.Google Scholar
Attwood, S.W., Fatih, F.A. & & Upatham, E.S. (2008) DNA-sequence variation among Schistosoma mekongi populations and related taxa; phylogeography and the current distribution of Asian schistosomiasis. PLoS Neglected Tropical Disease 2, e200. doi:10.1371/journal.pntd.0000200.Google Scholar
Bazsalovicsova, E., Kralova–Hromadova, I., Spakulova, M., Reblanova, M. & Oberhauserova, K. (2010) Determination of ribosomal internal transcribed spacer (ITS2) interspecific markers in Fasciola hepatica, Fascioloides magna, Dicrocoelium dendriticum and Paramphistomum cervi (Trematoda), parasites of wild and domestic ruminants. Helminthologia 47, 76–82.Google Scholar
Bhalerao, G.D. (1931) Trematode parasites of pigs in Bengal. Records of the Indian Museum 475–482.Google Scholar
Bowles, J., Hope, M., Tiu, W.U., Liu, X. & McManus, D.P. (1993) Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum . Acta Tropica 55, 217–229.Google Scholar
Bowles, J., Blair, D. & McManus, D.P. (1995) A molecular phylogeny of the human schistosomes. Molecular Phylogenetics and Evolution 4, 103–109.Google Scholar
Brown, W.M., George, M. Jr & Wilson, A.C. (1979) Rapid evolution of animal mitochondrial DNA. Proceedings of the National Academy of Sciences, USA 76, 1967–1971.Google Scholar
Brusentsov, I.I., Katokhin, A.V., Brusentsova, I.V., Shenkhovtsov, S.V., Borovikov, S.N., Goncharenko, G.G., Lider, L.A., Romashov, B.V., Rusinek, O.T., Shibitov, S.K., Suleymanov, M.M., Yevtushenko, A.V. & Mordvinov, V.A. (2013) Low genetic diversity in wide-spread Eurasian liver fluke Opisthorchis felineus suggests special demographic history of this trematode species. PloS ONE 8, e62453 doi:10.1371/journal.pone.0062453.Google Scholar
Caisova, L., Marin, B. & Melkonian, M. (2011) A close up view on ITS2 evolution and speciation – a case study in the Ulvophyceae (Chlorophyta Viridiplantae). BMC Evolutionary Biology 11, 262.Google Scholar
Coleman, A.W. (2003) ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends in Genetics 19, 370–375.Google Scholar
Hall, T.A. (1999) Bioedit: a user-friendly biological sequence alignment editor and analyses program for windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Harrington, M.G., Biffin, E. & Gadek, P.A. (2009) Comparative study of the evolution of nuclear ribosomal spacers incorporating secondary structure analyses within Dodonaeoideae, Hippocastanoideae and Xanthoceroideae (Sapindaceae). Molecular Phylogenetics and Evolution 50, 364–375.Google Scholar
Hwang, U.W. & Kim, W. (1999) General properties and phylogenetic utilities of nuclear ribosomal DNA and mitochondrial DNA commonly used in molecular systematics. Korean Journal of Parasitology 37, 215–228.Google Scholar
Kaewkes, S. (2003) Taxonomy and biology of liver flukes. Acta Tropica 88, 177–186.Google Scholar
Katokhin, V., Shekhovtsov, S.V., Konkow, S., Yurlova, N.I., Serbina, E.A., Vodianitskaia, S.N., Fedorov, K.P., Loktev, V.B., Muratov, I.V., Ohyama, F., Makhneva, T.V., Pel'tek, S.E. & Mordvinov, V.A. (2008) Assessment of the genetic distinctions of O. felineus from O. viverrini and C. sinensis by ITS2 and COI sequences. Doklady Biochemistry and Biophysics 421, 214–217.CrossRefGoogle Scholar
Keiser, J. & Utzinger, J. (2009) Food borne trematodiases. Clinical Microbiology Reviews 22, 466–483.Google Scholar
Keller, A., Schleicher, T., Schultz, J., Muller, T., Dandekar, T. & Wolf, M. (2009) 5.8S–28S rRNA interaction and HMM–based ITS2 annotation. Gene 430, 50–57.Google Scholar
Kostadinova, A., Herniou, E.A., Barrett, J. & Littlewood, D.T. (2003) Phylogenetic relationships of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) and related genera reassessed via DNA and morphological analyses. Systematic Parasitology 54, 159–176.Google Scholar
Lymbery, A.J. & Thompson, R.C.A. (2012) The molecular epidemiology of parasite infections: tools and applications. Molecular and Biochemical Parasitology 181, 102–116.Google Scholar
Mas-Coma, S. & Bargues, M.D. (1997) Human liver flukes: a review. Research and Reviews in Parasitology 57, 145–218.Google Scholar
Mehra, H.R. (1980) Fauna of India and the adjacent countries, Platyhelminthes (Vol I) Trematoda. 418 pp. Kolkatta, India, Zoological Survey of India.Google Scholar
Mordvinov, V.A., Yurlova, N.I., Ogorodova, L.M. & Katokhin, A.V. (2011) Opisthorchis felineus and Metorchis bilis are the main agents of liver fluke infection of humans in Russia. Parasitology International 61, 25–31.Google Scholar
Park, G.M. (2007) Genetic comparison of liver flukes, Clonorchis sinensis and Opisthorchis viverrini, based on rDNA and mtDNA gene sequences. Parasitology Research 100, 351–357.Google Scholar
Prasad, P.K., Tandon, V., Chatterjee, A. & Bandyopadhyay, S. (2007) PCR-based determination of internal transcribed spacer (ITS) regions of ribosomal DNA of giant intestinal fluke, Fasciolopsis buski (Lankester, 1857) Looss, 1899. Parasitology Research 101, 1581–1587.CrossRefGoogle Scholar
Prasad, P.K., Tandon, V., Biswal, D.K., Goswami, L.M. & Chatterjee, A. (2009) Use of sequence motifs as barcodes and secondary structures of internal transcribed spacer 2 (ITS2, rDNA) for identification of the Indian liver fluke, Fasciola (Trematoda: Fasciolidae). Bioinformation 3, 314–320.Google Scholar
Roy, B. & Tandon, V. (1992) Opisthorchis noverca Braun, 1902: first record from a bovine host and a comparative stereosan study of the surface topography of flukes of swine and cattle origin. Acta Parasitologica 37, 179–181.Google Scholar
Ruhl, M.W., Wolf, M. & Jenkins, T.M. (2010) Compensatory base changes illuminate morphologically difficult taxonomy. Molecular Phylogenetics and Evolution 54, 664–669.Google Scholar
Sahai, B.N. (1969) A survey of the helminth parasites of stray dogs around Bareilly, Uttar Pradesh. Indian Veterinary Journal 46, 734.Google Scholar
Sahai, B.N. & Srivastava, H.D. (1978) Morphology and life history of Opisthorchis noverca trematode parasite of dogs and pigs in India. Indian Journal of Animal Sciences 48, 113–122.Google Scholar
Sambrook, J. & Russell, D.W. (2001) Preparation and analyses of eukaryotic genomic DNA. pp. 1.51–1.54 in Molecular cloning: A laboratory manual. 3rd edn. Cold Spring Harbor, Cold Spring Harbor Laboratory Press.Google Scholar
Schulenburg, H. & Ewbank, J.J. (2004) Diversity and specificity in the interaction between Caenorhabditis elegans and the pathogen Serratia marcescens . BMC Evolutionary Biology 4, 49.Google Scholar
Schultz, J., Maisel, S., Gerlach, D., Muller, T. & Wolf, M. (2005) A common core of secondary structure of the internal transcribed spacer 2 (ITS2) throughout the eukaryota. RNA 11, 361–364.Google Scholar
Seemann, E.S., Menzel, K.P., Backofen, R. & Gorodkin, J. (2011) The PETfold and PETcofold web servers for intra- and intermolecular structures of multiple RNA sequences. Nucleic Acids Research 39, 107–111.CrossRefGoogle ScholarPubMed
Seibel, P.N., Muller, T., Dandekar, T., Schultz, J. & Wolf, M. (2006) 4SALE – a tool for synchronous RNA sequence and secondary structure alignment and editing. BMC Bioinformatics 7, 498.Google Scholar
Shylla, J.A., Ghatani, S., Chatterjee, A. & Tandon, V. (2011) Secondary structure analyses of ITS2 in the rDNA of three Indian paramphistomid species found in local livestock. Parasitology Research 108, 1027–1032.Google Scholar
Sinha, B.K. (1968) Opisthorchis noverca Braun 1902 in the pancreas of domestic pigs (Sus scrofa domestica) in Bihar. Current Science 37, 22–23.Google Scholar
Sripa, B., Sithithaworn, P. & Sirisinha, S. (2003) Opisthorchis viverrini and opisthorchiasis: the 21st century review. Acta Tropica 88, 169–170.Google Scholar
Sripa, B., Kaewkes, S., Sithithaworn, P., Mairiang, E., Laha, T., Smout, M., Pairojkul, C., Bhudhisawasdi, V., Tesana, S., Thinkamrop, B., Bethony, J.M., Loukas, A. & Brindley, P.J. (2007) Liver fluke induces cholangiocarcinoma. PLoS Medicine 4, e201 doi:10.1371/journal.pmed.0040201.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular Evolutionary Genetics Analyses using Maximum Parsimony methods. Molecular Phylogenetics and Evolution 28, 2731–2739.Google Scholar
Tandon, V., Biswal, D.K., Prasad, P.K. & Malsawmtluangi, C. (2011) Reconstructing the phylogenetic relationship of the cyclophyllidean cestodes: a case study using ITS2 rDNA and sequence-structure alignment. pp. 309–321 in Fred, A., Filipe, J. & Gamboa, H. (Eds) Biomedical Engineering Systems and Technologies. BIOSTEC 2010. Valencia, Spain. Communications in Computer and Information Science.CrossRefGoogle Scholar
Tatonova, Y.V., Chelomina, G.N. & Besprosvannykh, V.V. (2012) Genetic diversity of nuclear ITS1–5.8S–ITS2 rDNA sequence in Clonorchis sinensis Cobbold, 1875 (Trematoda: Opisthorchiidae) from the Russian Far East. Parasitology International 61, 664–674.CrossRefGoogle ScholarPubMed
Thaenkham, U., Nuamtanong, S., Vonghachack, Y., Yoonuan, T., Sanguankiat, S., Dekumyoy, P., Prommasack, B., Kobayashi, J. & Waikagul, J. (2011) Discovery of Opisthorchislobatus (Trematoda: Opisthorchiidae): a new record of small liver flukes in the Greater Mekong Sub-Region. Journal of Parasitology 97, 1152–1158.Google Scholar
Untergasser, A., Nijveen, H., Rao, X., Bisseling, T., Geurts, R. & Leunissen, J.A.M. (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Research 35, W71–W74.CrossRefGoogle ScholarPubMed
Wiemers, M., Keller, A. & Wolf, M. (2009) ITS2 secondary structure improves phylogeny estimation in a radiation of blue butterflies of the subgenus Agrodiaetus (Lepidoptera: Lycaenidae: Polyommatus). BMC Evolutionary Biology 9, 300.CrossRefGoogle Scholar
Wolf, M., Ruderisch, B., Dandekar, T. & Müller, T. (2008) ProfdistS: (Profile-) Distance based phylogeny on sequence structure alignment. Bioinformatics 24, 2401–2402.Google Scholar
Yamaguti, S. (1971) Synopsis of digenetic trematodes of vertebrates. Vols I and II. 1074 pp. Tokyo, Keigaku Publishing Corporation.Google Scholar
Yamaguti, S. (1975) A synoptical review of life histories of digenetic trematodes of vertebrates. 590 pp. Tokyo, Keigaku Publishing Corporation.Google Scholar
Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31, 3406–3415.CrossRefGoogle ScholarPubMed