Parasitology Research

, 105:429 | Cite as

Morphological differences and molecular similarities between Paragonimus bangkokensis and P. harinasutai

  • Pham Ngoc Doanh
  • Akio Shinohara
  • Yoichiro Horii
  • Shinichiro Yahiro
  • Shigehisa Habe
  • Nanthasane Vannavong
  • Michel Strobel
  • Satoshi Nakamura
  • Yukifumi Nawa
Original Paper
First Online:
Received:
Accepted:

Abstract

Paragonimus bangkokensis and Paragonimus harinasutai were found one after another in the same crab host, Potamon smithianus, in Thailand in 1967 and 1968. Both species were also recently found in China and Lao People's Democratic Republic (PDR). Those two Paragonimus spp. are distinguishable from each other by morphological features of metacercariae and adults. However, recently, the DNA sequences of second internal transcribed spacer region (ITS2) and cytochrome oxidase subunit 1 (CO1) genes of those two species in Thailand were reported to be highly similar to each other. In the present study, we collected P. bangkokensis in two provinces in Vietnam (the first record in Vietnam) and both P. bangkokensis and P. harinasutai in Lao PDR for the morphological and molecular phylogenetic analyses to clarify the mutual relationship between the two species. The results show that P. bangkokensis and P. harinasutai were distinguishable from each other by morphology such as the size of metacercariae and the arrangement of cuticular spines of adult worms. However, the molecular phylogenetic analyses of ITS2 and CO1 genes clearly indicate that P. bangkokensis and P. harinasutai make a monophyletic group.

Keywords

Adult Worm Indochina Peninsula Chinese Isolate Cuticular Spine Likelihood Base Test 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
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Notes

Acknowledgements

This study was partially supported by the Japanese Society for Promotion of Science (JSPS) under Ronpaku Fellowship no. NCST-10430 for Pham Ngoc Doanh, and by the Project for Zoonosis Education and Research, University of Miyazaki.

References

  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723CrossRefGoogle Scholar
  2. Blair D, Agatsuma T, Watanobe T (1997) Molecular evidence for the synonymy of three species of Paragonimus, P. ohirai Miyazaki, 1939, P. iloktsuenensis Chen, 1940 and P. sadoensis Miyazaki et al., 1968. J Helminthol 71:305–310CrossRefPubMedGoogle Scholar
  3. Blair D, Xu ZB, Agatsuma T (1999a) Paragonimiasis and the genus Paragonimus. Adv Parasitol 42:113–222CrossRefPubMedGoogle Scholar
  4. Blair D, Wu B, Chang ZS, Gong X, Agatsuma T, Zhang YN, Chen SH, Lin JX, Chen MG, Waikagul J, Guevara AG, Feng Z, Davis GM (1999b) A molecular perspective on the genera Paragonimus Braun, Euparagonimus Chen and Pagumogonimus Chen. J Helminthol 73:295–299PubMedGoogle Scholar
  5. 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. Syst Parasitol 60:1–21CrossRefPubMedGoogle Scholar
  6. Blair D, Agatsuma T, Wang WL (2007) Paragonimiasis. In: Murrell KD, Fried B (eds) Food-borne parasitic zoonoses. Fish and plant-borne parasites. World class parasites, vol 11. Springer, New York, pp 117–150Google Scholar
  7. Bowles J, McManus DP (1993) Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method. Mol Biochem Parasitol 57:231–240CrossRefPubMedGoogle Scholar
  8. Bowles J, Hope M, Tiu WU, Liu SX, McManus DP (1993) Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Trop 55:217–229CrossRefPubMedGoogle Scholar
  9. Cui AL, Chang ZS, Chen MG, Blair D, Chen SH, Zhang YN, Feng Z (2003) Taxonomic status in DNA sequences of five species of genus Paragonimus. Chin J Parasitol Parasitic Dis 21:27–30 (in Chinese with English abstract)Google Scholar
  10. Doanh PN, Shinohara A, Horii Y, Habe S, Nawa Y, The DT, Le NT (2007a) Morphological and molecular identification of two Paragonimus spp., of which metacercariae concurrently found in a land crab, Potamiscus tannanti, collected in Yenbai Province, Vietnam. Parasitol Res 100:1075–1082CrossRefPubMedGoogle Scholar
  11. Doanh PN, Shinohara A, Horii Y, Habe S, Nawa Y, Le NT (2007b) Description of a new lung fluke species, Paragonimus vietnamensis sp. nov. (Trematoda: Paragonimidae), found in northern Vietnam. Parasitol Res 101:1495–1501CrossRefPubMedGoogle Scholar
  12. Doanh PN, Shinohara A, Horii Y, Habe S, Nawa Y, Le NT (2008) Discovery of Paragonimus proliferus in northern Vietnam and their molecular phylogenetic status among genus Paragonimus. Parasitol Res 102:677–683CrossRefPubMedGoogle Scholar
  13. Doanh PN, Shinohara A, Horii Y, Habe S, Nawa Y (2009) Discovery of Paragonimus westermani in Vietnam and its molecular phylogenetic status in P. westermani complex. Parasitol Res. doi: 10.1007/s00436-008-1302-z
  14. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–374CrossRefPubMedGoogle Scholar
  15. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 36:783–791CrossRefGoogle Scholar
  16. Habe S, Lai KPF, Agatsuma T, Ow-Yang CK, Kawashima K (1993) Crab hosts for Paragonimus westermani (Kerbert, 1878) in Malaysia. Jpn J Trop Med Hyg 21:137–142Google Scholar
  17. He LY, Zhong HL, Gao PZ, Li HH, Xu ZB (1982) Preliminary studies on chromosomes of 9 species and subspecies of lung flukes in China. Chin Med J 95:404–408PubMedGoogle Scholar
  18. Iwagami M, Rajapakse RPVJ, Paranagama W, Okada T, Kano S, Agatsuma T (2008) Ancient divergence of Paragonimus westermani in Sri Lanka. Parasitol Res 102:845–852CrossRefPubMedGoogle Scholar
  19. Kino H, De NV, Vien HV, Chuyen LT, Sano M (1995) Paragonimus heterotremus Chen et Hsia, 1964 found from a dog in Vietnam. Jpn J Parasitol 44:470–472Google Scholar
  20. Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 29:170–179CrossRefPubMedGoogle Scholar
  21. Le TH, De NV, Blair D, McManus DP, 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 Trop 98:25–33CrossRefPubMedGoogle Scholar
  22. Li YS (1999) Species index table for the adult and metacercaria of Chinese Paragonimus. Chin J Vet Parasitol 7:59–62 (in Chinese with English abstract)Google Scholar
  23. Miyazaki I (1974) Lung flukes in the world: morphology and life history. In: Sasa M, Tanaka H, Kurihara T (eds) A symposium on epidemiology of parasitic diseases. International Medical Foundation of Japan, Tokyo, pp 101–135Google Scholar
  24. Miyazaki I (1991) An illustrated book of helminthic zoonoses. International Medical Foundation of Japan, Tokyo, pp 76–146Google Scholar
  25. Miyazaki I, Vajrasthira S (1967) On a new lung fluke, Paragonimus bangkokensis sp. nov. in Thailand (Trematoda: Troglotrematidae). Jpn J Med Sci Biol 20:243–249PubMedGoogle Scholar
  26. Miyazaki I, Vajrasthira S (1968) On a new lung fluke found in Thailand, Paragonimus harinasutai sp. nov. (Trematoda, Troglotrematidae). Ann Trop Med Parasitol 62:81–87PubMedGoogle Scholar
  27. Odermatt P, Habe S, Manichanh S, Tran DS, Duong V, Zhang W, Phommathet K, Nakamura S, Barennes H, Strobel M, Dreyfuss G (2007) Paragonimiasis and its intermediate hosts in a transmission focus in Lao People's Democratic Republic. Acta Trop 103:108–115CrossRefPubMedGoogle Scholar
  28. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests. System Biol 53:793–808CrossRefGoogle Scholar
  29. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  30. Qian BZ, Waikagul J, Dekumyoy P, Yoonuan T, Komalamisra C (2005) Occurrence of Paragonimus harinasutai in Zhejiang, China. J Trop Med Parasitol 28:22–25Google Scholar
  31. Qian BZ, Sugiyama H, Waikagul J, Zhu ZH (2006) Sequence analysis of ITS2 and CO1 genes of Paragonimus harinasutai. Chin J Parasitol Parasitic Dis 24:119–121 (in Chinese with English abstract)Google Scholar
  32. Rangsiruji A, Sugiyama H, Morishima Y, Kameoka Y, Donsakul T, Binchai S, Ketudat P (2006) A new record of Paragonimus other than P. westermani in southern Thailand. Southeast Asian J Trop Med Public Health 37(Suppl. 3):57–61PubMedGoogle Scholar
  33. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116Google Scholar
  34. Song CC, Qian BJ, Shou GC, Zhou DH, Li ZA (1990) First discovery of Paragonimus harinasutai in China. Acta Zhejiang Provincial Acad Med Sci 12:1–4 (in Chinese)Google Scholar
  35. Sugiyama H, Morishima Y, Rangsiruji A, Binchai S, Ketudat P, Kawanaka M (2006) Application of multiplex PCR for species discrimination using individual metacercariae of Paragonimus occurring in Thailand. Southeast Asian J Trop Med Public Health 37(Suppl. 3):48–52PubMedGoogle Scholar
  36. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  37. Zhou BJ (2004) Studies on Paragonimus proliferus. Chin J Parasitol Parasitic Dis 22:109–112 (in Chinese with English abstract)Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Pham Ngoc Doanh
    • 1
  • Akio Shinohara
    • 2
  • Yoichiro Horii
    • 3
  • Shinichiro Yahiro
    • 4
  • Shigehisa Habe
    • 5
  • Nanthasane Vannavong
    • 6
  • Michel Strobel
    • 6
  • Satoshi Nakamura
    • 7
  • Yukifumi Nawa
    • 8
  1. 1.Department of Parasitology, Institute of Ecology and Biological ResourcesVietnamese Academy of Science and TechnologyHanoiVietnam
  2. 2.Department of Bio-resources, Frontier Science Research CenterUniversity of MiyazakiMiyazakiJapan
  3. 3.Laboratory of Veterinary Parasitic Diseases, Faculty of AgricultureUniversity of MiyazakiMiyazakiJapan
  4. 4.Sigma ClinicFukuokaJapan
  5. 5.Department of Microbiology and Immunology, School of MedicineFukuoka UniversityFukuokaJapan
  6. 6.Institut de la Francophonie pour la Medicine TropicaleVientianeLaos
  7. 7.Research InstituteInternational Medical Center of JapanTokyoJapan
  8. 8.Division of Parasitology, Department of Infectious Diseases, Faculty of MedicineUniversity of MiyazakiMiyazakiJapan

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