Hostname: page-component-76fb5796d-wq484 Total loading time: 0 Render date: 2024-04-27T01:28:54.864Z Has data issue: false hasContentIssue false
  • English
  • Français

Metacercarial polymorphism and genetic variation of Paragonimus heterotremus (Digenea: Paragonimidae), and a re-appraisal of the taxonomic status of Paragonimus pseudoheterotremus

Published online by Cambridge University Press:  14 November 2013

P.N. Doanh ,
U. Thaenkham ,
P.T. An ,
H.V. Hien ,
Y. Horii  and
Y. Nawa
P.N. Doanh
Affiliation:
Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, Hanoi, Viet Nam
U. Thaenkham
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
P.T. An
Affiliation:
Noibai Animal Quarantine Station, Department of Veterinary, Ministry of Agricultural and Rural Development, Vietnam
H.V. Hien
Affiliation:
Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, Hanoi, Viet Nam
Y. Horii*
Affiliation:
Laboratory of Veterinary Parasitic Diseases, Faculty of Agriculture, University of Miyazaki, Miyazaki, Japan
Y. Nawa
Affiliation:
Research Affairs, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand
*
*Fax: +81-0985-58-7276 E-mail: horii@cc.miyazaki-u.ac.jp
Get access Rights & Permissions [Opens in a new window]

Abstract

Paragonimus heterotremus, which is an important pathogen for human paragonimiasis in Asia, is recognized as having the smallest metacercariae (maximum diameter < 300 μm) of any previously reported Paragonimus species. Recently, P. pseudoheterotremus has been described from Thailand as a new species having metacercariae (about 200 μm) slightly smaller than those of Thai P. heterotremus. In fact, the small size of P. pseudoheterotremus metacercariae is compatible with those of P. heterotremus from India and China. In this study in Vietnam, we found variably sized small metacercariae which are expected to consist of both P. heterotremus and P. pseudoheterotremus. Contrary to expectation, the adult flukes obtained by separate infection of experimental cats with different sized metacercariae were all identified as P. heterotremus, using both morphological and molecular characteristics. The molecular analyses of an extensive collection of P. heterotremus/P. pseudoheterotremus isolates from Asian countries also indicated that genetic distances between different populations of P. heterotremus are even larger than that between P. pseudoheterotremus and P. heterotremus. The haplotype network showed that all P. heterotremus and P. pseudoheterotremus isolates formed a P. heterotremus complex consisting of three groups with strong geographical origins. In addition, the Indian P. heterotremus group is the root of the other P. heterotremus and P. pseudoheterotremus populations. Based on the observed metacercarial polymorphisms and genetic variation in P. heterotremus,P. pseudoheterotremus should be considered a geographically isolated population of the P. heterotremus complex.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 2 , March 2015 , pp. 182 - 188
Copyright
Copyright © Cambridge University Press 2013 

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

Blair, D., Xu, Z.B. & Agatsuma, T. (1999) Paragonimiasis and the genus Paragonimus. Advances in Parasitology 42, 113–222.Google Scholar
Blair, D., Chang, Z., Chen, M., Cui, A., Wu, B., Agatsuma, T., Iwagami, M., Corrlis, D., Fu, C. & Zhan, X. (2005) Paragonimus skrjabini Chen, 1959 (Digenea: Paragonimidae) and related species in eastern Asia: a combined molecular and morphological approach to identification and taxonomy. Systematic Parasitology 60, 1–21.Google Scholar
Bowles, J., Hope, M., Tiu, W.U., Liu, S.X. & McManus, D.P. (1993) Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Tropica 55, 217–229.CrossRefGoogle ScholarPubMed
Bowles, J., Blair, D. & McManus, D.P. (1995) A molecular phylogeny of the human schistosomes. Molecular Phylogenetic Evolution 4, 103–109.Google Scholar
Chung, H.L., Ho, L.Y., Cheng, L.T. & Ts'ao, W.C. (1964) The discovery in Yunnan province of two new species of lung flukes – Paragonimus tuanshanensis sp. nov and P. menglaensis sp. nov. Chinese Medical Journal 83, 641–659.Google Scholar
Chung, H.L., Ho, L.Y., Ts'ao, W.C., Hsu, C.P. & Kao, P.C. (1975) On the metacercariae of some Paragonimus species and other trematodes found in Chinese freshwater crabs. Acta Zoologica Sinica 21, 155–165.Google Scholar
Devi, K.R., Naraina, K., Bhattacharya, T., Negmub, K., Agatsuma, T., Blair, D., Wickramashinghe, S. & Mahanta, J. (2007) Pleuropulmonary paragonimiasis due to Paragonimus heterotremus: molecular diagnosis, prevalence of infection and clinicoradiological features in an endemic area of northeastern India. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 786–792.Google Scholar
Devi, K.R., Narain, K., Mahanta, J., Nirmolia, T., Blair, D., Saikia, S.P. & Agatsuma, T. (2013) Presence of three distinct genotypes within the Paragonimus westermani complex in northeastern India. Parasitology 140, 76–86.Google Scholar
Doanh, P.N., Shinohara, A., Horii, Y., Habe, S., Nawa, Y. & Le, N.T. (2007a) Description of a new lung fluke species, Paragonimus vietnamensis sp. nov. (Trematoda: Paragonimidae), found in northern Vietnam. Parasitology Research 101, 1495–1501.Google Scholar
Doanh, P.N., Shinohara, A., Horii, Y., Habe, S., Nawa, Y., The, D.T. & Le, N.T. (2007b) Morphological and molecular identification of two Paragonimus spp., of which metacercariae concurrently found in a land crab, Potamiscus tannanti, collected in Yenbai Province, Vietnam. Parasitology Research 100, 1075–1082.Google Scholar
Doanh, P.N., Shinohara, A., Horii, Y., Habe, S., Nawa, Y. & Le, N.T. (2008) Discovery of Paragonimus proliferus in northern Vietnam and their molecular phylogenetic identification among genus Paragonimus. Parasitology Research 102, 677–683.CrossRefGoogle Scholar
Doanh, P.N., Shinohara, A., Horii, Y., Habe, S. & Nawa, Y. (2009) Discovery of Paragonimus westermani in Vietnam and their molecular phylogenetic status among P. westermani complex. Parasitology Research 104, 1149–1155.Google Scholar
Doanh, P.N., Hien, H.V., Nonaka, N., Horii, Y. & Nawa, Y. (2012) Co-existence of Paragonimus harinasutai and Paragonimus bangkokensis metacercariae in fresh water crab hosts in central Viet Nam with special emphasis on their close phylogenetic relationship. Parasitology International 61, 399–404.Google Scholar
Doanh, P.N., Hien, H.V., Nonaka, N., Horii, Y. & Nawa, Y. (2013) Discovery of Paragonimus skrjabini in Vietnam and its phylogenetic status in the Paragonimus skrjabini complex. Journal of Helminthology in press. DOI: 10.1017/S0022149X1200065X.CrossRefGoogle ScholarPubMed
Hu, W. (1998) Study on the life cycle of Paragonimus heterotremus. Chinese Journal of Parasitology and Parasitic Diseases 16, 347–352(in Chinese with English abstract).Google Scholar
Huson, D.H. & Bryant, D. (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23, 254–267.Google Scholar
Intapan, P.M., Sanpool, O., Thanchomnang, T., Imtawil, K., Pongchaiyakul, C., Nawa, Y. & Maleewong, W. (2012) Molecular identification of a case of Paragonimus pseudoheterotremus infection in Thailand. American Journal of Tropical Medicine and Hygiene 87, 706–709.Google Scholar
Kunz, W. (2002) When is a parasite species a species. Trends in Parasitology 18, 121–124.Google Scholar
Le, T.H., De, N.V., Blair, D., McManus, D.P., Kino, H. & Agatsuma, T. (2006) Paragonimus heterotremus Chen and Hsia (1964), in Vietnam: a molecular identification and relationships of isolates from different hosts and geographical origins. Acta Tropica 98, 25–33.CrossRefGoogle Scholar
Pariyanonda, S., Maleewong, W., Pipitgool, V., Wongkham, C., Morakote, N. & Intapan, P. (1990) Serodiagnosis of human paragonimiasis caused by Paragonimus heterotremus. Southeast Asian Journal of Tropical Medicine and Public Health 21, 103–107.Google Scholar
Singh, T.S., Sugiyama, H., Rangsiruji, A. & Devi, K.R. (2007) Morphological and molecular characterizations of Paragonimus heterotremus, the causative agent of human paragonimiasis in India. Southeast Asian Journal of Tropical Medicine and Public Health 38, 82–86.Google Scholar
Sugiyama, H., Morishima, Y., Binchai, S., Rangsiruji, A. & Ketudat, P. (2007) New form of Paragonimus westermani discovered in Thailand: morphological characteristics and host susceptibility. Southeast Asian Journal of Tropical Medicine and Public Health 38, 87–91.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.Google Scholar
Thaenkham, U. & 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. & 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 22, 4673–4680.CrossRefGoogle ScholarPubMed
Waikagul, J. (2007) A new species of Paragonimus (Trematoda: Troglotrematidae) from a cat infected with metacercariae from mountain crabs Larnaudia larnaudii. Journal of Parasitology 93, 1496–1500.CrossRefGoogle ScholarPubMed
Yahiro, S., Habe, S., Duong, V., Odermatt, P., Barennes, H., Strobel, M. & Nakamura, S. (2008) Identification of the human paragonimiasis causative agent in Lao People's Democratic Republic. Journal of Parasitology 94, 1176–1177.Google Scholar