Hostname: page-component-76fb5796d-vfjqv Total loading time: 0 Render date: 2024-04-26T23:28:14.050Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic divergence of human pathogens Nanophyetus spp. (Trematoda: Troglotrematidae) on the opposite sides of the Pacific Rim

Published online by Cambridge University Press:  01 December 2016

A. N. VORONOVA ,
G. N. CHELOMINA ,
V. V. BESPROZVANNYKH  and
V. V. TKACH
A. N. VORONOVA*
Affiliation:
Institute of Biology and Soil Science, Far Eastern Branch, Russian Academy of Sciences, 100–letiya Street, 159, Vladivostok 690022, Russia
G. N. CHELOMINA
Affiliation:
Institute of Biology and Soil Science, Far Eastern Branch, Russian Academy of Sciences, 100–letiya Street, 159, Vladivostok 690022, Russia Department of Biochemistry, Microbiology and Biotechnology, Far Eastern Federal University, Far Eastern Federal University, 690051 Vladivostok, Russia
V. V. BESPROZVANNYKH
Affiliation:
Institute of Biology and Soil Science, Far Eastern Branch, Russian Academy of Sciences, 100–letiya Street, 159, Vladivostok 690022, Russia
V. V. TKACH
Affiliation:
Department of Biology, University of North Dakota, 10 Grand Forks, ND 58202, USA
*
*Corresponding author. Institute of Biology and Soil Science, Far Eastern Branch, Russian Academy of Sciences, 100–letiya Street, 159, Vladivostok 690022, Russia. E-mail: avoronova92@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Human and animal nanophyetiasis is caused by intestinal flukes belonging to the genus Nanophyetus distributed on both North American and Eurasian coasts of Northern Pacific. In spite of the wide geographical distribution and medical and veterinary importance of these flukes, the intra-generic taxonomy of Nanophyetus spp. remains unresolved. The two most widely distributed nominal species, Nanophyetus salmincola and Nanophyetus schikhobalowi, both parasitizing humans and carnivorous mammals, were described from North America and eastern Eurasia, respectively. However, due to their high morphological similarity their interrelationships remained unclear and taxonomic status unstable. In this study, we explored genetic diversity of Nanophyetus spp. from the Southern Russian Far East in comparison with that of samples from North America based on the sequence variation of the nuclear ribosomal gene family (18S, internal transcribed spacers, ITS1-5·8S-ITS2 and 28S). High levels of genetic divergence in each rDNA region (nucleotide substitutions, indels, alterations in the secondary structures of the ITS1 and ITS2 transcripts) as well as results of phylogenetic analysis provided strong support for the status of N. salmincola and N. schikhobalowi as independent species.

Keywords

TrematodaNanophyetusITS18S rDNA28S rDNADNA secondary structuremolecular phylogenytaxonomy
Type
Research Article
Information
Parasitology , Volume 144 , Issue 5 , April 2017 , pp. 601 - 612
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Athokpam, V. D. and Tandon, V. (2015). A survey of metacercarial infections in commonly edible fish and crab hosts prevailing in Manipur, Northeast India. Journal of Parasitic Diseases 39, 429–440.Google Scholar
Bernhart, S. H., Hofacker, , Ivo, L., Will, S., Gruber, A. R. and Stadler, P. F. (2008). RNAalifold: improved consensus structure prediction for RNA alignments. BMC Bioinformatics 9, 474.Google Scholar
Besprozvannykh, V. V. (2002). Development of Paragonimus westermani ichunensis in a reservoir host. Parazitologiia 36, 427–429. (In Russian).Google Scholar
Bowman, D. D., Hendrix, C. M., Lindsay, D. S. and Stephen, C. B. (2008). Chapter 2. The Trematodes. In Feline Clinical Parasitology (ed. Barr, S. C. and Bowman, D. D.), pp.83–182. Iowa State University Press, A Blackwell Science Company, United States of America. Google Scholar
Brant, S. V. and Loker, E. S. (2009). Molecular systematics of the avian shistosome genus Trichobilharzia (Trematoda: Shistosomatidae) in North America. International Journal for Parasitology 95, 941–963.Google Scholar
Capriotti, E. and Marti-Renom, M. A. (2008). RNA structure alignment by a unit-vector approach. Bioinformatics 24, 112–118.Google Scholar
Chapin, E. A. (1926). A new genus and species of trematode, the probable cause of salmon–poisoning in dogs. Veterinary Clinics of North America 7, 36–37.Google Scholar
Chapin, E. A. (1928). Note. Journal of Parasitology 14, 60.Google Scholar
Coombs, I. (2006). Helminth species recovered from humans. In Handbook of Helminthiasis for Public Health (ed. Crompton, D. W. T. and Savioli, L.), pp. 12–24. CRC Press, Taylor & Francis Group, Boca Raton, Florida.Google Scholar
Curran, S. S., Tkach, V. V. and Overstreet, R. M. (2013). Molecular evidence for two cryptic species of Homalometron (Digenea: Apocreadiidae) in freshwater Fishes of the southeastern United States. Comparative Parasitology 80, 186–195.Google Scholar
Devi, K. R., Narain, K., Agatsuma, T., Blair, D., Nagataki, M., Wickramasinghe, S., Yatawara, L. and Mahanta, J. (2010). Morphological and molecular characterization of Paragonimus westermani in northeastern India. Acta Tropica 116, 31–38.Google Scholar
Dragomeretskaia, A. G., Zelia, O. P., Trotsenko, O. E. and Ivanova, I. B. (2014). Social bases for the functioning of nanophyetiasis foci in the Amur region. Meditsinskaia Parazitologiia 4, 23–28. (In Russian)Google Scholar
Dzikowski, R., Levy, M. G., Poore, M. F., Flowers, J. R. and Paperna, I. (2004). Use of rDNA polymorphism for identification of Heterophyidae infecting freshwater fishes. Diseases of Aquatic Organisms 59, 35–41.Google Scholar
Ermolenko, A. V., Bespozvannykh, V. V., Rumyantseva, E. E. and Voronok, V. M. (2015). Pathogens of human trematodiases in the Primorye territory. Meditsinskaia Parazitologiia 2, 6–10. (In Russian)Google Scholar
Filimonova, L. V. (1966). Distribution of nanophyetiasis in the territory of the Soviet Far East. Trudy Gelmintologicheskoi Laboratorii Akademii. Nauk USSR 17, 240–244. (In Russian)Google Scholar
Fischer, P. U., Curtis, K. C., Marcos, L. A. and Weil, G. J. (2011). Molecular characterization of the North American lung fluke Paragonimus kellicotti in Missouri and its development in Mongolian gerbils. American Journal of Tropical Medicine and Hygiene 84, 1005–1011.Google Scholar
Gebhardt, G. A. (1966). Studies on the molluscan and fish hosts of the “salmon poisoning” fluke, Nanophyetus salmincola (Chapin). Master's thesis. Oregon State University, Corvallis.Google Scholar
Ghatani, S., Shylla, J. A., Tandon, V., Chatterjee, A. and Roy, B. (2012). Molecular characterization of pouched amphistome parasites (Trematoda: Gastrothylacidae) using ribosomal ITS2 sequence and secondary structures. Journal of Helminthology 86, 117–124.Google Scholar
Greiman, S. E., Kent, M. L., Betts, J., Cochell, D., Sigler, T. and Tkach, V. V. (2016). Nanophyetus salmincola, vector of the salmon poisoning disease agent Neorickettsia helminthoeca, harbors a second pathogenic Neorickettsia species. Veterinary Parasitology 229, 107–109.CrossRefGoogle ScholarPubMed
Harrel, L. W. and Deardorf, T. L. (1990). Human nanophyetiasis: transmission by handing naturally infected Coho Salmon (Oncorhynchus kisutch). International Journal of Infectious Diseases 161, 146–148.CrossRefGoogle Scholar
Harris, J. M. (1992). Poly (ethylene glycol) Chemistry: Biotechnical and Biomedical Applications. Springer Science & Business Media, New York.CrossRefGoogle Scholar
Headley, S. A., Scorpio, D. G., Vidotto, O. and Dumler, J. S. (2011). Neorickettsia helminthoeca and salmon poisoning disease: a review. Veterinary Journal 187, 165–173.Google Scholar
Hofacker, I. L., Fontana, W., Stadler, P. F., Bonhoeffer, S., Tacker, M. and Schuster, P. (1994). Fast folding and comparison of RNA secondary structures. Monatshefte für Chemie 125, 167–188.Google Scholar
John, D. T. and Petri, A. Jr. (2006). Markell and Voge`s Medical Parasitology, 9th Edn. Saunders Elsevier, St. Louis, MO.Google Scholar
Jousson, O., Bartoli, P., Zaninetti, L. and Pawlowski, J. (1998). Use of the ITS rDNA for elucidation of some life–cycles of Mesometridae (Trematoda, Digenea). International Journal for Parasitology 28, 1403–1411.Google Scholar
Kasl, E. L., Fayton, T. J., Font, W. F. and Criscione, C. D. (2014). Alloglossidium floridense n. sp. (Digenea: Macroderoididae) from a spring run in North Central Florida. International Journal for Parasitology 100, 121–126.Google Scholar
Keiser, J. and Utzinger, J. (2009). Food-borne trematodiases. Clinical Microbiology 22, 466–483.Google Scholar
Kinne, O. (1980). Diseases of Marine Animals. VoL. IV. Pisces, Applied Aspects, Conclusions. Pitman Press, Great Britain.Google Scholar
Koetschan, C., Förster, F., Keller, A., Schleicher, T., Ruderisch, B., Schwarz, R., Müller, T., Wolf, M. and Schultz, J. (2010). The ITS2 database III — sequences and structures for phylogeny. Nucleic Acids Research 38, 275–279.Google Scholar
Krieger, J., Hett, A. K., Fuerst, P. A., Birstein, V. J. and Ludwig, A. (2006). Unusual intraindividual variation of the nuclear 18S rRNA gene is widespread within the Acipenseridae. Journal of Heredity 97, 218–225.Google Scholar
Littlewood, D. T. and Olson, P. D. (2001). Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise. Chapter 25. In Interrelationships of the Platyhelminthes (ed. Littlewood, D. T. J. and Bray, R. A.), pp. 262–278. Taylor & Francis, London, England.Google Scholar
Lockyer, A. E., Olson, P. D. and Littlewood, D. T. J. (2003). Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society 78, 155–171.Google Scholar
Lotfy, W. M., Brant, S. V., DeJong, R. J., Le, T. H., Demiaszkiewicz, A., Rajapakse, R. P. V. J., Mareka, M., Zouhara, M., Doudab, O., Mazakovaa, J. and Rysanek, P. (2010). Bioinformatics-assisted characterization of the ITS1–5·8S-ITS2 segments of nuclear rRNA gene clusters, and its exploitation in molecular diagnostics of European crop-parasitic nematodes of the genus Ditylenchus . Plant Pathology 59, 931–943.Google Scholar
Michot, B., Despres, L., Bonhomme, F. and Bachellerie, J. P. (1993). Conserved secondary structures in the ITS2 of trematode pre-rRNA. FEBS Letters 316, 247–252.Google Scholar
Millemann, R. E. and Knapp, S. E. (1970). Biology of Nanophyetus salmincola and “salmon poisoning” disease. Advances in Parasitology 8, 1–41.Google Scholar
Morgan, J. A. and Blair, D. (1995). Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collarspine group. Parasitology 111, 609–615.Google Scholar
Nolan, M. and Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology 60, 102–160.Google Scholar
Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A. and Littlewood, D. T. J. (2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.Google Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.Google Scholar
Razo-Mendivil, U., Vázquez-Domínguez, E., Rosas-Valdez, R., de León, G. P. P. and Nadler, S. A. (2010). Phylogenetic analysis of nuclear and mitochondrial DNA reveals a complex of cryptic species in Crassicutis cichlasomae (Digenea: Apocreadiidae), a parasite of Middle-American cichlids. International Journal for Parasitology 40, 471–486.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. BMC Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Sinovich, L. L. (1959). Nanophyetosis in the Soviet Far East. Proceedings of 10th Conference Parasitological Problems and Diseases with Natural Reservoirs. USSR Academy of Sciences 2, 410–411. (in Russian)Google Scholar
Snyder, S. D. and Tkach, V. V. (2011). Aptorchis kuchlingi n. sp. (Digenea: Plagiorchioidea) from the Oblong Turtle, Chelodina oblonga, (Pleurodira: Chelidae) in Western Australia. Comparative Parasitology 78, 280–285.Google Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.CrossRefGoogle ScholarPubMed
Tatonova, Y. V., Chelomina, G. N. and Besprosvannykh, V. V. (2012). Genetic diversity of nuclear ITS1-5. 8-ITS2 rDNA sequence in Clonorchis sinensis Cobbold, 1875 (Trematoda: Opistorchidae) from the Russian Far East. Parasitology International 61, 664–674.Google Scholar
Thaenkham, U., Dekumyoy, P., Komalamisra, C., Sato, M., Dung, D. T. and Waikagul, J. (2010). Systematics of the subfamily Haplorchiinae (Trematoda: Heterphyidae), based on nuclear ribosomal DNA genes and ITS2 region. Parasitology International 59, 460–465.Google Scholar
Thaenkham, U. and Waikagul, J. (2008). Molecular phylogenetic relationship of Paragonimus pseudoheterotremus . Southeast Asian Journal of Tropical Medicine and Public Health 39, 217–221.Google Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 11, 4673–4680.Google Scholar
Tkach, V. V. and Snyder, S. D. (2007). Aptorchis megacetabulus n. sp. (Platyhelminthes: Digenea) from the northern long-necked turtle, Chelodina rugosa (Pleurodira: Chelidae). Journal of Parasitology 93, 404–408.Google Scholar
Tkach, V. V. and Snyder, S. D. (2008). Aptorchis glandularis n. sp. (Digenea: Plagiorchioidea) from the Northwestern red-faced turtle, Emydura australis, (Pleurodira: Chelidae) in the Kimberley, Western Australia. Journal of Parasitology 94, 918–924.Google Scholar
Tkach, V. V., Pawlowski, J. and Sharpilo, V. P. (2000). Molecular and morphological differentiation between species of the Plagiorchis vespertilionis group (Digenea, Plagiorchiidae) occurring in European bats, with a redescription of P. vespertilionis (Muller, 1780). Systematic Parasitology 47, 9–22.Google Scholar
Tkach, V. V., Curran, S. S., Bell, J. A. and Overstreet, R. M. (2013). A new species of Crepidostomum (Digenea: Allocreadiidae) from Hiodon tergisus in Mississippi and molecular comparison with three congeners. Journal of Parasitology 99, 1114–1121.CrossRefGoogle ScholarPubMed
Truett, G. E., Heeger, P., Mynatt, R. L., Truett, A. A., Walker, J. A. and Warman, M. L. (2000). Preparation of PCR–quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Bio Techniques 29, 52–54.Google Scholar
Van Herwerden, L., Blair, D. and Agatsuma, T. (1999). Intra- and interindividual variation in ITS1 of Paragonimus westermani (Trematoda: Digenea) and related species: implications for phylogenetic studies. Molecular Phylogenetic and Evolution 2, 67–73.Google Scholar
Vaughan, J. A., Tkach, V. V. and Greiman, S. E. (2012). Neorickettsial endosymbionts of the Digenea: diversity, transmission and distribution. Advances in Parasitology 79, 253–297.CrossRefGoogle ScholarPubMed
Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31, 3406–3415.CrossRefGoogle ScholarPubMed
Supplementary material: File

Voronova supplementary material

Figure S1

Download Voronova supplementary material(File)
File 130.9 KB