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Parasitology research
Nov 05, 2024;123 (11): 368.

Nuclear ribosomal transcription units in Asian Paragonimus species (Paragonimidae: Platyhelminthes): genetic characteristics, polymorphism, and implications for intersuperfamilial phylogeny.

Khue Thi Nguyen, Huong Thi Thanh Doan, Linh Thi Khanh Pham, Do Thi Roan, Takeshi Agatsuma, Pham Ngoc Doanh, Thanh Hoa Le
Author Information
  1. Khue Thi Nguyen: Immunology Department, Institute of Biotechnology (IBT), Vietnam Academy of Science and Technology (VAST), 18. Hoang Quoc Viet Rd, Cau Giay, Hanoi, Vietnam.
  2. Huong Thi Thanh Doan: Immunology Department, Institute of Biotechnology (IBT), Vietnam Academy of Science and Technology (VAST), 18. Hoang Quoc Viet Rd, Cau Giay, Hanoi, Vietnam.
  3. Linh Thi Khanh Pham: Immunology Department, Institute of Biotechnology (IBT), Vietnam Academy of Science and Technology (VAST), 18. Hoang Quoc Viet Rd, Cau Giay, Hanoi, Vietnam.
  4. Do Thi Roan: Immunology Department, Institute of Biotechnology (IBT), Vietnam Academy of Science and Technology (VAST), 18. Hoang Quoc Viet Rd, Cau Giay, Hanoi, Vietnam.
  5. Takeshi Agatsuma: Department of Environmental Health Sciences, Kochi Medical School, Kohasu, Oko-Cho 185-1, Nankoku, Kochi, 783-8505, Japan.
  6. Pham Ngoc Doanh: Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam.
  7. Thanh Hoa Le: Immunology Department, Institute of Biotechnology (IBT), Vietnam Academy of Science and Technology (VAST), 18. Hoang Quoc Viet Rd, Cau Giay, Hanoi, Vietnam. imibtvn@gmail.com.
PMID: 39496997 DOI: 10.1007/s00436-024-08391-y

Abstract

The entire transcribed sequences (from the 5' terminus of 18S to the 3' terminus of 28S rRNA genes) of the ribosomal transcription units (rTU*) of five Asian Paragonimus species were obtained and characterized. The rTU* length was 7661 bp for P. heterotremus (LC strain, Vietnam), 7422 bp for P. iloktsuenensis (Amami strain, Japan), 6932 bp for P. skrjabini miyazakii (OkuST1 strain, Japan), 7422 bp for P. ohirai (Kino strain, Japan), and three strains of P. westermani: 8616 bp (Megha strain, India), 7292 bp (Bogil strain, South Korea), and 7052 bp (QT2 strain, Vietnam) without intergenic spacer region (IGS). All seven Asian Paragonimus strains' genetic characteristics were described, including the length of individual genes/regions, repeat polymorphism, base composition, and skewness. To investigate the superfamilial relationships in the Xiphidiata, with a focus on the Troglotrematoidea and its associated superfamilies, we used the PhyML software package to create three comprehensive maximum-likelihood phylogenies. The datasets used were 83 concatenated 28S + 18S, 83 single complete 18S, and 157 single, partial 28S rDNA sequences, respectively, from entire rTUs and/or accessible ribosomal sequences of the same species from the suborders Xiphidiata, Echinostomata, and Haplosplanchnata, with a Schistosoma sequence as an outgroup. Three phylogenetic trees revealed that Echinostomata and Haplosplanchnata are monophyletic, while Xiphidiata is polyphyletic and contains the monophyletic Troglotrematoidea. The concatenated 18S + 28S and single 18S phylogenies revealed well-bootstrap supported seven superfamilies (Troglotrematoidea, Haploporoidea, Gorgoderoidea, Brachycladioidea, Microphalloidea, Plagiorchioidea, and Opecoeloidea) that are monophyletic in the Xiphidiata. The Haploporoidea was a basal superfamily nested close to the Gorgoderoidea and Troglotrematoidea and was not supported as a distinct suborder Haploporata. Six of seven xiphidiatan superfamilies were monophyletic in the partial 28S phylogeny, with the exception of Opecoeloidea, which was separated into two different subclades: Opecoelidae and Stenakridae/Zdzitowieckitrematidae. The monophyletic Haploporoidea/Haploporata was separated from the Gorgoderoidea associates and placed in a marginal group in Xiphidiata. There were two notable clusters in the Paragonimidae: mixed-Paragonimus, which included a fairly compact group of P. heterotremus strains, and P. westermani/siamensis, which was divided into geographical/country strain groups. In conclusion, combined ribosomal rDNA sequences were more effective than single rDNA markers in resolving interfamilial and familial relationships. The ribosomal datasets presented here will be useful for taxonomic reassessment, as well as evolutionary and population genetics research in the Troglotrematoidea and other superfamilies in the Xiphidiata and the class Trematoda.

Keywords

Paragonimus ITS1 Intersuperfamilial Paragonimidae Phylogeny Polymorphism Repeat units Ribosomal transcription unit Troglotrematoidea Xiphidiata

References

  1. Agatsuma T, Habe S (1985) Interspecific hybridization in three species, Paragonimus ohirai, P. iloktsuenensis and P. sadoensis, with special reference to isozyme patterns in F1 hybrids. Jpn J Parasitol 34:389–394
  2. Agatsuma T, Habe S (1986) Genetic variability and differentiation of natural populations in three Japanese lung flukes, Paragonimus ohirai, Paragonimus iloktsuenensis and Paragonimus sadoensis (Digenea: Troglotrematidae). J Parasitol 72:417–433 [DOI: 10.2307/3281682]
  3. Agatsuma T, Iwagami M, Sato Y, Iwashita J, Hong SJ, Kang SY, Ho LY, Su KE, Kawashima K, Abe T (2003) The origin of the triploid in Paragonimus westermani on the basis of variable regions in the mitochondrial DNA. J Helminthol 77(4):279–285. https://doi.org/10.1079/joh2003185 [DOI: 10.1079/joh2003185]
  4. Atopkin DM, Semenchenko AA, Solodovnik DA, Ivashko YI (1971) Vinnikov KA (2021) First next-generation sequencing data for Haploporidae (Digenea: Haploporata): characterization of complete mitochondrial genome and ribosomal operon for Parasaccocoelium mugili Zhukov. Parasitol Res 120(6):2037–2046. https://doi.org/10.1007/s00436-021-07159-y [DOI: 10.1007/s00436-021-07159-y]
  5. Atopkin DM, Semenchenko AA, Solodovnik DA, Ivashko YI, Vinnikov KA (2021) First next-generation sequencing data for Haploporidae (Digenea: Haploporata): characterization of complete mitochondrial genome and ribosomal operon for Parasaccocoelium mugili Zhukov, 1971. Parasitol Res 120(6):2037–2046. https://doi.org/10.1007/s00436-021-07159-y
  6. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580. https://doi.org/10.1093/nar/27.2.573 [DOI: 10.1093/nar/27.2.573]
  7. Berman JJ (2019) Taxonomic guide to infectious diseases: understanding the biologic classes of pathogenic organisms. 2nd edn. Academic, London, UK. ISBN: 978–0–12–817576–7. https://www.elsevier.com/books-and-journals
  8. Blair D (2022) Lung flukes of the genus Paragonimus: ancient and re-emerging pathogens. Parasitology 149:1286–1295. https://doi.org/10.1017/S0031182022000300 [DOI: 10.1017/S0031182022000300]
  9. Blair D (2008) Family paragonimidae dollfus. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CAB international and natural history museum, London, pp 271–273 (1939)
  10. Blair D, Nawa Y, Mitreva M, Doanh PN (2016) Gene diversity and genetic variation in lung flukes (genus Paragonimus). Trans R Soc Trop 110(1):6–12. https://doi.org/10.1093/trstmh/trv101 [DOI: 10.1093/trstmh/trv101]
  11. 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 71:305–310. https://doi.org/10.1017/s0022149x00016114
  12. Blair D (2006) Ribosomal DNA variation in parasitic flatworms. In: Maule A (ed) Parasitic flatworms: molecular biology, biochemistry, immunology and control. CAB International, pp 96–123.  https://doi.org/10.1079/9780851990279.009
  13. Blair D (2019) Paragonimiasis. In: Toledo R, Fried B (eds) Digenetic trematodes. Springer, Switzerland, Springer Nature Switzerland AG, pp 105–138. https://doi.org/10.1007/978-3-030-18616-6_5
  14. Briscoe AG, Bray RA, Brabec J, Littlewood DT (2016) The mitochondrial genome and ribosomal operon of Brachycladium goliath (Digenea: Brachycladiidae) recovered from a stranded minke whale. Parasitol Int 65(3):271–275. https://doi.org/10.1016/j.parint.2016.02.004 [DOI: 10.1016/j.parint.2016.02.004]
  15. Cerqueira AV, Lemos B (2019) Ribosomal DNA and the Nucleolus as keystones of nuclear architecture, organization, and function. Trends Genet 35(10):710–723. https://doi.org/10.1016/j.tig.2019.07.011 [DOI: 10.1016/j.tig.2019.07.011]
  16. Chai JY, Jung BK (2018) Paragonimus spp. In: Rose JB, Jiménez-Cisneros B (eds) Global water pathogen project. http://www.waterpathogens.org (Robertson L (eds) Part 4 Helminths) http://www.waterpathogens.org/book/paragonimus Michigan State University, E. Lansing, MI, UNESCO
  17. Chai JY, Jung BK (2019) Epidemiology of trematode infections: an update. In: Toledo R and Fried B (eds) Digenetic trematodes. Adv Exp Med Biol 1154:359–409. Available at. https://doi.org/10.1007/978-3-030-18616-6_12
  18. Devi KR, Narain K, Mahanta J, Nirmolia T, Blair D, Saikia SP, Agatsuma T (2013) Presence of three distinct genotypes within the Paragonimus westermani complex in northeastern India. Parasitology 140(1):76–86. https://doi.org/10.1017/S0031182012001229 [DOI: 10.1017/S0031182012001229]
  19. 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 104(5):1149–1155. https://doi.org/10.1007/s00436-008-1302-z
  20. Dubey JP (2022) Endemic Paragonimus kellicotti infections in animals and humans in USA and Canada: review and personal perspective. Food Waterborne Parasitol 30:e00184. https://doi.org/10.1016/j.fawpar.2022.e00184 [DOI: 10.1016/j.fawpar.2022.e00184]
  21. Dumbovic G, Forcales SV, Perucho M (2017) Emerging roles of macrosatellite repeats in genome organization and disease development. Epigenetics 12(7):515–526. https://doi.org/10.1080/15592294.2017.1318235 [DOI: 10.1080/15592294.2017.1318235]
  22. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–21. https://doi.org/10.1093/sysbio/syq010.2010
  23. Habe S, Agatsuma T, Hirai H (1985) Evidence for metacercarial polymorphism in lung flukes, Paragonimus ohirai and Paragonimus iloktsuenensis. J Parasitol 71:820–827 (PMID: 4093814) [DOI: 10.2307/3281721]
  24. Ivashko YI, Semenchenko AA, Solodovnik DA, Atopkin DM (2022) Characterization of complete mitochondrial genome and ribosomal operon for Carassotrema koreanum Park, 1938 (Digenea: Haploporidae) by means of next-generation sequencing data. J Helminthol 96:e54. https://doi.org/10.1017/S0022149X22000438 [DOI: 10.1017/S0022149X22000438]
  25. Iwagami M, Rajapakse RP, Paranagama W, Agatsuma T (2003) Identities of two Paragonimus species from Sri Lanka inferred from molecular sequences. J Helminthol 77(3):239–245. https://doi.org/10.1079/JOH2003180 [DOI: 10.1079/JOH2003180]
  26. 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(1):25–33. https://doi.org/10.1016/j.actatropica.2006.01.008 [DOI: 10.1016/j.actatropica.2006.01.008]
  27. Le TH, Pham KLT, Doan HTT, Le TKX, Nguyen KT, Lawton SP (2020) Description and phylogenetic analyses of ribosomal transcription units from species of Fasciolidae (Platyhelminthes: Digenea). J Helminthol 94:e136. https://doi.org/10.1017/S0022149X20000164 [DOI: 10.1017/S0022149X20000164]
  28. Le TH, Nguyen KT, Pham LTK, Doan HTT, Agatsuma T, Blair D (2022) The complete mitogenome of the Asian lung fluke Paragonimus skrjabini miyazakii and its implications for the family Paragonimidae (Trematoda: Platyhelminthes). Parasitology 149(13):1709–1719. https://doi.org/10.1017/S0031182022001184 [DOI: 10.1017/S0031182022001184]
  29. Le TH, Pham LTK, Van Quyen D, Nguyen KT, Doan HTT, Saijuntha W, Blair D (2024) The ribosomal transcription units of five echinostomes and their taxonomic implications for the suborder Echinostomata (Trematoda: Platyhelminthes). Parasitol Res 123(1):103. https://doi.org/10.1007/s00436-023-08110-z [DOI: 10.1007/s00436-023-08110-z]
  30. Le TH, Nguyen KT, Nguyen NT, Doan HT, Dung DT, Blair D (2017) The ribosomal transcription units of Haplorchis pumilio and H. taichui and the use of 28S sequences for phylogenetic identification of common heterophyids in Vietnam. Parasit Vectors 10:17. https://doi.org/10.1186/s13071-017-1968-0
  31. Le TH, Nguyen KT, Nguyen NTB, Doan HTT, Agatsuma T, Blair D (2019) The complete mitochondrial genome of Paragonimus ohirai (Paragonimidae: Trematoda: Platyhelminthes) and its comparison with P. westermani congeners and other trematodes. PeerJ 7:e7031. https://doi.org/10.7717/peerj.7031
  32. Le TH, Nguyen KT, Pham LTK, Doan HTT, Roan DT, Le XTK, Agatsuma T, Blair D (2023) Mitogenomic and nuclear ribosomal transcription unit datasets support the synonymy of Paragonimus iloktsuenensis and P. ohirai (Paragonimidae: Platyhelminthes). Parasitol Res 122(7):1531–1544. https://doi.org/10.1007/s00436-023-07854-y
  33. Lee OR, Chung PR (2001) Immunoelectron microscopic localization of partially purified antigens in adult Paragonimus iloktsuenesis. Korean J Parasitol 39(2):119–132. https://doi.org/10.3347/kjp.2001.39.2.119 [DOI: 10.3347/kjp.2001.39.2.119]
  34. Littlewood DTJ, Bray RA, Waeschenbach A (2015) Phylogenetic patterns of diversity in cestodes and trematodes. In: Morand S, Krasnov BR, Littlewood DTJ (eds) Book: diversity and diversification, Cambridge University Press, pp 304–319. https://doi.org/10.1017/CBO9781139794749.018
  35. Lockyer AE, Olson PD, Littlewood DTJ (2003a) 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. Biol J Linn Soc Lond 78(2):155–171. https://doi.org/10.1046/j.1095-8312.2003.00141.x [DOI: 10.1046/j.1095-8312.2003.00141.x]
  36. Lockyer AE, Olson PD, Ostergaard P, Rollinson D, Johnston DA, Attwood SW, Southgate VR, Horak P, Snyder SD, Le TH, Agatsuma T, McManus DP, Carmichael AC, Naem S, Littlewood DT (2003b) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126(3):203–224. https://doi.org/10.1017/s0031182002002792 [DOI: 10.1017/s0031182002002792]
  37. Martin SB (2024) Chapter 46: Opecoelidae Ozaki, 1925 (Family): the richest trematode family. In: Gardner SL, Gardner SA (eds) Book: Concepts in Animal Parasitology, Zea Books, Lincoln, Nebraska, United States, pp 480–489. https://doi.org/10.32873/unl.dc.ciap046
  38. Olson PD (2000) New insights into platyhelminth systematics and evolution. Parasitol Today 16(1):3–5. https://doi.org/10.1016/s0169-4758(99)01555-0 [DOI: 10.1016/s0169-4758(99)01555-0]
  39. Olson PD, Tkach V (2005) Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Adv Parasitol 60:165–243. https://doi.org/10.1016/S0065-308X(05)60003-6 [DOI: 10.1016/S0065-308X(05)60003-6]
  40. Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DT (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33(7):733–755. https://doi.org/10.1016/s0020-7519(03)00049-3 [DOI: 10.1016/s0020-7519(03)00049-3]
  41. Pérez-Ponce de León G, Hernández-Mena DI (2019) Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the ‘next-generation’ Tree of Life. J Helminthol 93(3):260–276. https://doi.org/10.1017/S0022149X19000191 [DOI: 10.1017/S0022149X19000191]
  42. Perna NT, Kocher TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol 41:353–358. https://doi.org/10.1007/BF00186547 [DOI: 10.1007/BF00186547]
  43. Potapova TA, Gerton JL (2019) Ribosomal DNA and the nucleolus in the context of genome organization. Chromosome Res 27(1–2):109–127. https://doi.org/10.1007/s10577-018-9600-5 [DOI: 10.1007/s10577-018-9600-5]
  44. Qiu YY, Gao Y, Li Y, Ma XX, Lv QB, Hu Y, Qiu HY, Chang QC, Wang CR (2020) Comparative analyses of complete ribosomal DNA sequences of Clonorchis sinensis and Metorchis orientalis: IGS sequences may provide a novel genetic marker for intraspecific variation. Infect Genet Evol 78:104125. https://doi.org/10.1016/j.meegid.2019.104125 [DOI: 10.1016/j.meegid.2019.104125]
  45. Rambaut A (2018) FigTree, version 1.4.4. http://tree.bio.ed.ac.uk/software/figtree/
  46. Ryu JS, Hwang UW, Min DY, Shin KS, Nam SJ, Lee OR (2000) Molecular identification of Paragonimus ohirai and P. westermani from Anhui province, China. Parasite 7(4):305–309. https://doi.org/10.1051/parasite/2000074305
  47. Sanpool O, Intapan PM (2013) Thanchomnang T, Janwan P, Nawa Y, Blair D, Maleewong W. Molecular variation in the Paragonimus heterotremus complex in Thailand and Myanmar. Korean J Parasitol 51(6):677–681. https://doi.org/10.3347/kjp.2013.51.6.677
  48. Sato H, Suzuki K (2006) Gastrointestinal helminths of feral raccoons (Procyon lotor) in Wakayama Prefecture. Japan J Vet Med Sci 68(4):311–318. https://doi.org/10.1292/jvms.68.311 [DOI: 10.1292/jvms.68.311]
  49. Singh TS, Sugiyama H, Umehara A, Hiese S, Khalo K (2009) Paragonimus heterotremus infection in Nagaland: a new focus of Paragonimiasis in India. Indian J Med Microbiol 27(2):123–127. https://doi.org/10.4103/0255-0857.49424 [DOI: 10.4103/0255-0857.49424]
  50. Sokolov SG, Shchenkov SV, Frolov EV, Gordeev II (2022) A phylogenetic re-evaluation of the Stenakrine Opecoelids (Trematoda, Digenea: Opecoeloidea) with some taxonomic novelties. Diversity 14:949. https://doi.org/10.3390/d14110949 [DOI: 10.3390/d14110949]
  51. Sokolov SG, Lebedeva DI, Gordeev II, Khasanov FK (2019). Zdzitowieckitrema incognitum gen. et sp. nov. (Trematoda, Xiphidiata) from the antarctic fish Muraenolepis marmorata Günther, 1880 (Gadiformes: Muraenolepidae): ordinary morphology but unclear family affiliation. Mar Biodivers 49(1):451–462. https://doi.org/10.1007/s12526-017-0830-0
  52. Su X, Zhang Y, Zheng X, Wang XX, Li Y, Li Q, Wang CR (2018) Characterization of the complete nuclear ribosomal DNA sequences of Eurytrema pancreaticum. J Helminthol 92(4):484–490. https://doi.org/10.1017/S0022149X17000554 [DOI: 10.1017/S0022149X17000554]
  53. Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120 [DOI: 10.1093/molbev/msab120]
  54. Tatonova YV, Chelomina GN, Besprosvannykh VV (2012) Genetic diversity of nuclear ITS1-5.8S-ITS2 rDNA sequence in Clonorchis sinensis Cobbold, 1875 (Trematoda: Opisthorchidae) from the Russian Far East. Parasitol Int 61:664–674. https://doi.org/10.1016/j.parint.2012.07.005 [DOI: 10.1016/j.parint.2012.07.005]
  55. Thaenkham U, Nawa Y, Blair D, Pakdee W (2011) Confirmation of the paraphyletic relationship between families Opisthorchiidae and Heterophyidae using small and large subunit ribosomal DNA sequences. Parasitol Int 60(4):521–523. https://doi.org/10.1016/j.parint.2011.07.015 [DOI: 10.1016/j.parint.2011.07.015]
  56. Tkach V, Pawlowski J, Mariaux J (2000a) Phylogenetic analysis of the suborder Plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. Int J Parasitol 30(1):83–93. https://doi.org/10.1016/s0020-7519(99)00163-0 [DOI: 10.1016/s0020-7519(99)00163-0]
  57. Tkach VV, Littlewood DT, Olson PD, Kinsella JM, Swiderski Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Syst Parasitol 56(1):1–15. https://doi.org/10.1023/a:1025546001611 [DOI: 10.1023/a]
  58. Tkach VV, Kudlai O, Kostadinova A (2016) Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea). Int J Parasitol 46(3):171–185. https://doi.org/10.1016/j.ijpara.2015.11.001 [DOI: 10.1016/j.ijpara.2015.11.001]
  59. Tkach V, Pawlowski J, Mariaux J, Swiderski Z (2000b) Chapter 17. Molecular phylogeny of the suborder Plagiorchiata and its position in the system of digenea. In book: interrelationships of platyhelminthes (Eds: Littlewood DTJ and Bray RA), 186–193. Taylor & Francis, London
  60. Vainutis KS, Voronova AN, Duscher GG, Shchelkanov EM, Shchelkanov MY (2022) Origins, phylogenetic relationships and host-parasite interactions of Troglotrematoidea since the cretaceous. Infect Genet Evol 101:105274. https://doi.org/10.1016/j.meegid.2022.105274 [DOI: 10.1016/j.meegid.2022.105274]
  61. van Herwerden L, Blair D, Agatsuma T (1999) Intra- and interindividual variation in ITS1 of Paragonimus westermani (Trematoda: Digenea) and related species: implications for phylogenetic studies. Mol Phylogenet Evol 12:67–73. https://doi.org/10.1006/mpev.1998.0572 [DOI: 10.1006/mpev.1998.0572]
  62. Vilas R, Criscione CD, Blouin MS (2005) A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 131(6):839–846. https://doi.org/10.1017/S0031182005008437 [DOI: 10.1017/S0031182005008437]
  63. Voronova AN, Besprozvannykh VV, Ngo HD, Plekhova NG, Hung NM, Tatonova YV (2020) Paragonimus heterotremus Chen et Hsia, 1964 (Digenea: Paragonimidae): species identification based on the biological and genetic criteria, and pathology of infection. Parasitol Res 119(12):4073–4088. https://doi.org/10.1007/s00436-020-06929-4 [DOI: 10.1007/s00436-020-06929-4]
  64. Voronova AN, Vainutis KS, Tabakaeva TV, Sapotsky MV, Karaeka NN, Volkov YG, Galkina IV, Shchelkanov MY (2022) Molecular identification of the trematode P. ichunensis stat. n. from lungs of siberian tigers justified reappraisal of Paragonimus westermani species complex. J Parasit Dis. https://doi.org/10.1007/s12639-022-01481-7
  65. Waeschenbach A, Webster BL, Littlewood DTJ (2012) Adding resolution to ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with large fragments of mtDNA. Mol Phylogenet Evol 63:834–847. https://doi.org/10.1016/j.ympev.2012.02.020 [DOI: 10.1016/j.ympev.2012.02.020]
  66. Waeschenbach A, Littlewood DTJ (2017) A molecular framework for the cestoda. In: Caira JN and Jensen K (eds.). Planetary biodiversity inventory (2008–2017): tapeworms from vertebrate bowels of the earth. University of Kansas, Natural History Museum, Special Publication No. 25, Lawrence, KS, USA, pp 431–451
  67. Weider LJ, Elser JJ, Crease TJ, Mateos M, Cotner JB, Markow TA (2005) The functional significance of ribosomal rDNA variation: impacts on the evolutionary ecology of organisms. Annu Rev Ecol Evol Syst 36:219–242. https://doi.org/10.1146/annurev.ecolsys.36.102003.152620 [DOI: 10.1146/annurev.ecolsys.36.102003.152620]
  68. Yoshida A, Doanh PN, Maruyama H (2019) Paragonimus and paragonimiasis in Asia: an update. Acta Trop 199:105074. https://doi.org/10.1016/j.actatropica [DOI: 10.1016/j.actatropica]
  69. Zhao GH, Blair D, Li XY, Li J, Lin RQ, Zou FC, Sugiyama H, Mo XH, Yuan ZG, Song HQ, Zhu XQ (2011) The ribosomal intergenic spacer (IGS) region in Schistosoma japonicum: structure and comparisons with related species. Infect Genet Evol 11(3):610–617. https://doi.org/10.1016/j.meegid.2011.01.015 [DOI: 10.1016/j.meegid.2011.01.015]
  70. Zheng X, Chang QC, Zhang Y, Tian SQ, Lou Y, Duan H, Guo DH, Wang CR, Zhu XQ (2014) Characterization of the complete nuclear ribosomal DNA sequences of Paramphistomum cervi. Scientific World J 2014:751907. https://doi.org/10.1155/2014/751907 [DOI: 10.1155/2014/751907]
  71. Zhou XJ, Yang Q, Tan QH, Zhang LY, Shi LB, Zou JX (2021) Paragonimus and its hosts in China: An update. Acta Trop 223:106094. https://doi.org/10.1016/j.actatropica.2021.106094 [DOI: 10.1016/j.actatropica.2021.106094]

Grants

  1. VINIF.2023.STS.85./the Vingroup Innovation Foundation in Vietnam (VINIF)

MeSH Term

Animals
Phylogeny
Paragonimus
Polymorphism, Genetic
RNA, Ribosomal, 18S
DNA, Helminth
RNA, Ribosomal, 28S
Asia
DNA, Ribosomal
Sequence Analysis, DNA
Paragonimiasis

Chemicals

RNA, Ribosomal, 18S
DNA, Helminth
RNA, Ribosomal, 28S
DNA, Ribosomal
Journal Article

Word Cloud

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