Abstract
The taxonomy and classification of the family Opisthorchiidae have been revised by several authors with the exclusion or synonymization of some genera. The genus Hepatiarius Feizullaev, 1961 accommodated two species: Hepatiarius sudarikovi Feizullaev, 1961 and H. longissimus Linstow, 1883. Recently, some experts have suppressed Hepatiarius as a junior synonym of Opisthorchis Blanchard, 1895 based on morphological features alone. Prior to the present study, no molecular data either from nuclear or from mitochondrial DNA was available for any species of this genus. In the present study, four specimens of H. sudarikovi Feizullaev, 1961 were recovered from the bile ducts of the little egret, Egretta garzetta. The complete sequences of the internal transcribed spacers (ITS-1 and ITS-2) of ribosomal DNA (rDNA) and the nearly complete mitochondrial genome sequences were determined and the phylogenetic relationship of H. sudarikovi with related taxa was assessed based on the mitochondrial (mt) DNA sequences. The sequence similarity in the ITS rDNA between H. sudarikovi and Opisthorchis felineus was higher (97.62% in ITS-1 and 96.22% in ITS-2) than with other opisthorchiids. Phylogenetic analysis using Bayesian inference (BI) based on the concatenated amino acid sequences of 12 protein-coding genes (PCGs) clustered H. sudarikovi into the clade of opisthorchiids, with O. felineus being the closest related species, which supports the affinity of H. sudarikovi with trematodes in the genus Opisthorchis. This is the first avian liver fluke whose nearly complete mitochondrial genome was sequenced. The mtDNA sequences of H. sudarikovi, in combination with its rDNA sequences, provide novel resources of genetic markers for the identification, species differentiation, and systematic studies of H. sudarikovi with other avian opisthorchiid flukes.
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References
Barker FD (1911) The trematode genus Opisthorchis R. Blanchard, 1895. Paris, Asselin et Houzeau 14:513–561
Bowles J, McManus DP (1993) Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method. Mol Biochem Parasitol 57:231–239
Bowles J, Blair D, McManus DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54:165–173
Bray RA, Gibson DI, Jones A (2008) Keys to the Trematoda, vol Volume 3. CABI Publishing and the Natural History Museum, New York
Cai XQ, Liu GH, Song HQ, Wu CY, Zou FC, Yan HK, Yuan ZG, Lin RQ, Zhu XQ (2012) Sequences and gene organization of the mitochondrial genomes of the liver flukes Opisthorchis viverrini and Clonorchis sinensis (Trematoda). Parasitol Res 110:235–243
Castoe TA, Parkinson CL (2006) Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes). Mol Phylogenet Evol 39:91–110
Chen YY, Chen S, Kang J, Fang H, Dao H, Guo W, Lai C, Lai M, Fan J, Fu L, Andrieu JM, Lu W (2014) Evolving molecular epidemiological profile of human immunodeficiency virus 1 in the southwest border of China. PLoS One 9:e107578
Choudhary K, Agrawal N (2017) Ribosomal DNA analysis of isolates of the liver fluke Opisthorchis pedicellata (Verma, 1927) from two siluroid fish species in India. J Helminthol 91:302–311
Doanh PN, Nawa Y (2016) Clonorchis sinensis and Opisthorchis spp. in Vietnam: current status and prospects. Trans R Soc Trop Med Hyg 110:13–20
Feizullaev NA (1961) Hepatiarius n. g, n. sp., a new trematode genus of Opisthorchidae Braun, 1901. Dokl Akad Nauk SSSR 17:635–640
Filimonova L (2000) [Taxonomic review of the two subfamilies (Opisthorchiinae (Looss, 1899)) and Plotnikoviinae (Skrjabin, 1945) family Opisthorchiidae (Looss, 1899) of Russian fauna]. Actual problems of general parasitology. Moscow, Hayкa
Gasser RB, Hu M, Chilton NB, Campbell BE, Jex AJ, Otranto D, Cafarchia C, Beveridge I, Zhu XQ (2007) Single strand conformation polymorphism (SSCP) for the analysis of genetic variation. Nat Protoc 1:3121–3128
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser (Oxf) 41:95–98
Hughes T, O’Connor T, Techasen A, Namwat N, Loilome W, Andrews RH, Khuntikeo N, Yongvanit P, Sithithaworn P, Taylor-Robinson SD (2017) Opisthorchiasis and cholangiocarcinoma in Southeast Asia: an unresolved problem. Int J Gen Med 10:227–237
Hung N, Madsen H, Fried B (2013) Global status of fish-borne zoonotic trematodiasis in humans. Acta Parasitol 58:231–258
King S, Scholz T (2001) Trematodes of the family Opisthorchiidae: a minireview. Korean J Parasitol 39:209–221
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Le TH, Blair D, McManus DP (2002) Mitochondrial genomes of parasitic flatworms. Trends Parasitol 18:206–213
Lun ZR, Gasser RB, Lai DH, Li AX, Zhu XQ, Yu XB, Fang YY (2005) Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect Dis 5:31–41
Lutz HL, Tkach VV, Weckstein JD (2017) Methods for specimen-based studies of avian symbionts. In: Webster MS (ed) The extended specimen: emerging frontiers in collections-based ornithological research. Studies in avian biology (no. 50). CRC Press, Boca Raton, FL, pp 157–183
Mordvinov VA, Mardanov CA, Ravin NV, Shekhovtsov SV, Demakov SА, Katokhin CA, Kolchanov NА, Skryabin KG (2009) Complete sequencing of the mitochondrial genome of Opisthorchis felineus, causative agent of Opisthorchiasis. Acta Nat 1:99–104
Mordvinov VA, Yurlova NI, Ogorodova LM, Katokhin AV (2012) Opisthorchis felineus and Metorchis bilis are the main agents of liver fluke infection of humans in Russia. Parasitol Int 61:25–31
Morgan JAT, Blair D (1995) Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collar-spine group. Parasitology 111:609–615
Pakharukova MY, Mordvinov VA (2016) The liver fluke Opisthorchis felineus: biology, epidemiology and carcinogenic potential. Trans R Soc Trop Med Hyg 110:28–36
Ronquist F, Huelsenbeck JP (2003) MrBayes 3. Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Sanpool O, Aung WPP, Rodpai R, Maleewong W, Intapan PM (2018) Human liver fluke Opisthorchis viverrini (Trematoda, Opisthorchiidae) in Central Myanmar: new records of adults and metacercariae identified by morphology and molecular analysis. Acta Trop 185:149–155
Scholz T (2008) Family Opisthorchiidae Looss, 1899. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CABI Publishing and the Natural History Museum, London, U.K, pp 9–49
Shekhovtsov SV, Katokhin AV, Kolchanov NA, Mordvinov VA (2010) The complete mitochondrial genomes of the liver flukes Opisthorchis felineus and Clonorchis sinensis (Trematoda). Parasitol Int 59:100–103
Sripa B, Brindley PJ, Mulvenna J, Laha T, Smout MJ, Mairiang E, Bethony JM, Loukas A (2012) The tumorigenic liver fluke Opisthorchis viverrini–multiple pathways to cancer. Trends Parasitol 28:395–407
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882
von Linstow OFB (1883) Nematoden, Trematoden und Acanthocephalen, gesammelt von Prof. Fedtschenko in Turkestan. Arch f Nat 49:274-314
Yamaguti S (1971) Synopsis of digenetic trematodes of vertebrates, vol I, II. Keigaku Publishing Co, Japan
Yang X, Gasser RB, Koehler AV, Wang L, Zhu K, Chen L, Feng H, Hu M, Fang R (2015) Mitochondrial genome of Hypoderaeum conoideum–comparison with selected trematodes. Parasit Vectors 8:97
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Project support was provided by the National Natural Science Foundation of China (Grant No. 31702225), the International Science and Technology Cooperation Project of Gansu Provincial Key Research and Development Program (Grant No. 17JR7WA031), the Elite Program of Chinese Academy of Agricultural Sciences, and the Agricultural Science and Technology Innovation Program (ASTIP) (Grant No. CAAS-ASTIP-2016-LVRI-03).
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Suleman, Ma, J., Khan, M.S. et al. Mitochondrial and nuclear ribosomal DNA dataset suggests that Hepatiarius sudarikovi Feizullaev, 1961 is a member of the genus Opisthorchis Blanchard, 1895 (Digenea: Opisthorchiidae). Parasitol Res 118, 807–815 (2019). https://doi.org/10.1007/s00436-019-06227-8
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DOI: https://doi.org/10.1007/s00436-019-06227-8