Hostname: page-component-77f85d65b8-g98kq Total loading time: 0 Render date: 2026-04-11T06:21:44.200Z Has data issue: false hasContentIssue false
  • English
  • Français

A new molecular nomenclature for Taenia hydatigena: mitochondrial DNA sequences reveal sufficient diversity suggesting the assignment of major haplotype divisions

Published online by Cambridge University Press:  23 October 2020

John Asekhaen Ohiolei Open the ORCID record for John Asekhaen Ohiolei [Opens in a new window] ,
Hong-Bin Yan ,
Li Li ,
Wen-Hui Li ,
Yao-Dong Wu ,
Mughees Aizaz Alvi ,
Nian-Zhang Zhang ,
Bao-Quan Fu ,
Xue-Lin Wang Open the ORCID record for Xue-Lin Wang [Opens in a new window]  and
Wan-Zhong Jia
John Asekhaen Ohiolei
Affiliation:
State Key Laboratory of Veterinary Etiological Biology/National Professional Laboratory for Animal Echinococcosis/Key Laboratory of Veterinary Parasitology of Gansu Province/Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou 730046, Gansu Province, P. R. China
Hong-Bin Yan
Affiliation:
State Key Laboratory of Veterinary Etiological Biology/National Professional Laboratory for Animal Echinococcosis/Key Laboratory of Veterinary Parasitology of Gansu Province/Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou 730046, Gansu Province, P. R. China
Li Li
Affiliation:
State Key Laboratory of Veterinary Etiological Biology/National Professional Laboratory for Animal Echinococcosis/Key Laboratory of Veterinary Parasitology of Gansu Province/Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou 730046, Gansu Province, P. R. China
Wen-Hui Li
Affiliation:
State Key Laboratory of Veterinary Etiological Biology/National Professional Laboratory for Animal Echinococcosis/Key Laboratory of Veterinary Parasitology of Gansu Province/Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou 730046, Gansu Province, P. R. China
Yao-Dong Wu
Affiliation:
State Key Laboratory of Veterinary Etiological Biology/National Professional Laboratory for Animal Echinococcosis/Key Laboratory of Veterinary Parasitology of Gansu Province/Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou 730046, Gansu Province, P. R. China
Mughees Aizaz Alvi
Affiliation:
State Key Laboratory of Veterinary Etiological Biology/National Professional Laboratory for Animal Echinococcosis/Key Laboratory of Veterinary Parasitology of Gansu Province/Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou 730046, Gansu Province, P. R. China
Nian-Zhang Zhang
Affiliation:
State Key Laboratory of Veterinary Etiological Biology/National Professional Laboratory for Animal Echinococcosis/Key Laboratory of Veterinary Parasitology of Gansu Province/Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou 730046, Gansu Province, P. R. China
Bao-Quan Fu
Affiliation:
State Key Laboratory of Veterinary Etiological Biology/National Professional Laboratory for Animal Echinococcosis/Key Laboratory of Veterinary Parasitology of Gansu Province/Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou 730046, Gansu Province, P. R. China
Xue-Lin Wang
Affiliation:
Key Laboratory for Zoonoses Research, Ministry of Education, Institute of Zoonoses, College of Veterinary Medicine, Jilin University, OIE Collaborating Center on Foodborne Parasites in Asian-Pacific Region, Changchun 130062, P. R. China
Wan-Zhong Jia*
Affiliation:
State Key Laboratory of Veterinary Etiological Biology/National Professional Laboratory for Animal Echinococcosis/Key Laboratory of Veterinary Parasitology of Gansu Province/Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou 730046, Gansu Province, P. R. China Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Disease, Yangzhou 225009, Jiangsu Province, P. R. China
*
Author for correspondence: Wan-Zhong Jia, E-mail: jiawanzhong@caas.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Cysticercosis caused by the metacestode larval stage of Taenia hydatigena formerly referred to as Cysticercus tenuicollis is a disease of veterinary importance that constitutes a significant threat to livestock production worldwide, especially in endemic regions due to condemnation of visceral organs and mortality rate of infected young animals. While the genetic diversity among parasites is found to be potentially useful in many areas of research including molecular diagnostics, epidemiology and control, that of T. hydatigena across the globe remains poorly understood. In this study, analysis of the mitochondrial DNA (mtDNA) of adult worms and larval stages of T. hydatigena isolated from dogs, sheep and a wild boar in China showed that the population structure consists of two major haplogroups with very high nucleotide substitutions involving synonymous and non-synonymous changes. Compared with other cestodes such as Echinococcus spp., the genetic variation observed between the haplogroups is sufficient for the assignment of major haplotype or genotype division as both groups showed a total of 166 point-mutation differences between the 12 mitochondrial protein-coding gene sequences. Preliminary analysis of a nuclear protein-coding gene (pepck) did not reveal any peculiar changes between both groups which suggests that these variants may only differ in their mitochondrial makeup.

Keywords

Chinagenetic diversityhaplogroupsphylogenyTaenia hydatigena

Information

Type
Research Article
Information
Parasitology , Volume 148 , Issue 3 , March 2021 , pp. 311 - 326
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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.)

Article purchase

Temporarily unavailable

References

Abidi, SMA, Nazami, WA, Khan, P, Ahmad, M and Irshadullah, M (1989) Biochemical characterization of Taenia hydatigena cysticerci from goats and pigs. Journal of Helminthology 63, 333–337.CrossRefGoogle ScholarPubMed
Alvi, MA, Ohiolei, JA, Saqib, M, Li, L, Muhammad, N, Tayyab, MH, Qamar, W, Alvi, AA, Wu, YD, Li, XR, Fu, BQ, Yan, HB and Jia, WZ (2020) Preliminary information on the prevalence and molecular description of Taenia hydatigena isolates in Pakistan based on mitochondrial cox1 gene. Infection, Genetics and Evolution 85, 104481.CrossRefGoogle ScholarPubMed
Boufana, B, Scala, A, Lahmar, S, Pointing, S, Craig, PS, Dessì, G, Zidda, A, Pipia, AP and Varcasia, A (2015) A preliminary investigation into the genetic variation and population structure of Taenia hydatigena from Sardinia, Italy. Veterinary Parasitology 214, 67–74.CrossRefGoogle ScholarPubMed
Bowles, J and McManus, DP (1993) NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. International Journal for Parasitology 23, 969–972.CrossRefGoogle ScholarPubMed
Bowles, J, Blair, D and McManus, D (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.CrossRefGoogle ScholarPubMed
Braae, UC, Kabululu, M, Nørmark, ME, Nejsum, P, Ngowi, HA and Johansen, MV (2015) Taenia hydatigena cysticercosis in slaughtered pigs, goats, and sheep in Tanzania. Tropical Animal Health and Production 47, 1523–1530. https://doi.org/10.1007/s11250-015-0892-6.CrossRefGoogle ScholarPubMed
Burland, TG (2000) DNASTAR's Lasergene sequence analysis software. In Misener, S and Krawetz, SA (eds), Bioinformatics Methods and Protocols. Methods in Molecular BiologyTM, Vol. 32. Totowa: Humana Press, pp. 71–91.Google Scholar
Cengiz, G, Yucel Tenekeci, G and Bilgen, N (2019) Molecular and morphological characterization of Cysticercus tenuicollis in red deer (Cervus elaphus) from Turkey. Acta Parasitologica 64, 652–657.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Excoffier, L, Laval, G and Schneider, S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.Google Scholar
Filip, KJ, Pyziel, AM, Jeżewski, W, Myczka, AW, Demiaszkiewicz, AW and Laskowski, Z (2019) First molecular identification of Taenia hydatigena in wild ungulates in Poland. Ecohealth 16, 161–170.CrossRefGoogle ScholarPubMed
Fu, YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.CrossRefGoogle ScholarPubMed
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Kilinc, SG, Kesik, HK and Simsek, S (2019) Molecular characterization and haplotypes of sheep and goat isolates of Cysticercus tenuicollis in Turkey. Parasitology 146, 1047–1054.CrossRefGoogle ScholarPubMed
Kinkar, L, Laurimäe, T, Simsek, S, Balkaya, I, Casulli, A, Manfredi, MT, Ponce-Gordo, F, Varcasia, A, Lavikainen, A, González, LM, Rehbein, S, Van der Giessen, J, Sprong, H and Saarma, U (2016) High-resolution phylogeography of zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1 with an emphasis on its distribution in Turkey, Italy and Spain. Parasitology 143, 1790–1801.CrossRefGoogle ScholarPubMed
Kinkar, L, Laurimäe, T, Acosta-Jamett, G, Andresiuk, V, Balkaya, I, Casulli, A, Gasser, RB, González, LM, Haag, KL, Zait, H, Irshadullah, M, Jabbar, A, Jenkins, DJ, Manfredi, MT, Mirhendi, H, M'rad, S, Rostami-Nejad, M, Oudni-M'rad, M, Pierangeli, NB, Ponce-Gordo, F, Rehbein, S, Sharbatkhori, M, Kia, EB, Simsek, S, Soriano, SV, Sprong, H, Šnábel, V, Umhang, G, Varcasia, A and Saarma, U (2018) Distinguishing Echinococcus granulosus sensu stricto genotypes G1 and G3 with confidence: a practical guide. Infection, Genetics and Evolution 64, 178–184.CrossRefGoogle Scholar
Knapp, J, Nakao, M, Yanagida, T, Okamoto, M, Saarma, U, Lavikainen, A and Ito, A (2011) Phylogenetic relationships within Echinococcus and Taenia tapeworms (Cestoda: Taeniidae): an inference from nuclear protein-coding genes. Molecular Phylogenetics and Evolution 61, 628–638.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Laurimäe, T, Kinkar, L, Moks, E, Romig, T, Omer, RA, Casulli, A, Umhang, G, Bagrade, G, Irshadullah, M, Sharbatkhori, M, Mirhendi, H, Ponce-Gordo, F, Soriano, SV, Varcasia, A, Rostami-Nejad, M, Andresiuk, V and Saarma, U (2018a) Molecular phylogeny based on six nuclear genes suggests that Echinococcus granulosus sensu lato genotypes G6/G7 and G8/G10 can be regarded as two distinct species. Parasitology 145, 1929–1937.CrossRefGoogle Scholar
Laurimäe, T, Kinkar, L, Romig, T, Omer, RA, Casulli, A, Umhang, G, Gasser, RB, Jabbar, A, Sharbatkhori, M, Mirhendi, H, Ponce-Gordo, F, Lazzarini, LE, Soriano, SV, Varcasia, A, Rostami Nejad, M, Andresiuk, V, Maravilla, P, González, LM, Dybicz, M, Gawor, J, Šarkūnas, M, Šnábel, V, Kuzmina, T and Saarma, U (2018b) The benefits of analysing complete mitochondrial genomes: deep insights into the phylogeny and population structure of Echinococcus granulosus sensu lato genotypes G6 and G7. Infection, Genetics and Evolution 64, 85–94.CrossRefGoogle Scholar
Morais, DF, Vilela, VLR, Feitosa, TF, Santos, VMD, Gouveia, VR, Athayde, ACR and Azevêdo, SS (2017) Prevalence and risk factors for Cysticercus tenuicollis in goats and sheep in Paraíba, northeastern Brazil. Revista Brasileira de Parasitologia Veterinaria 26, 235–238.CrossRefGoogle ScholarPubMed
Muku, RJ, Yan, HB, Ohiolei, JA, Saaid, AA, Ahmed, S, Jia, WZ and Fu, BQ (2020) Molecular identification of Taenia hydatigena from sheep in Khartoum, Sudan. Korean Journal of Parasitology 58, 93–97.CrossRefGoogle ScholarPubMed
Nakao, M, Sako, Y, Yokoyama, N, Fukunaga, M and Ito, A (2000) Mitochondrial genetic code in cestodes. Molecular and Biochemical Parasitology 111, 415–424.CrossRefGoogle ScholarPubMed
Nguyen, MT, Gabriël, S, Abatih, EN and Dorny, P (2016) A systematic review on the global occurrence of Taenia hydatigena in pigs and cattle. Veterinary Parasitology 226, 97–103.CrossRefGoogle ScholarPubMed
Ohiolei, JA, Luka, J, Zhu, GQ, Yan, HB, Li, L, Magaji, AA, Alvi, MA, Wu, YT, Li, JQ, Fu, BQ and Jia, WJ (2019) First molecular description, phylogeny, and genetic variation of Taenia hydatigena from Nigerian sheep and goats based on three mitochondrial genes. Parasites and Vectors 12, 520.CrossRefGoogle ScholarPubMed
Ohiolei, JA, Li, L, Yan, HB, Fu, BQ and Jia, WZ (2020) Complete mitochondrial genome analysis confirms the presence of Echinococcus granulosus sensu lato genotype G6 in Nigeria. Infection, Genetics and Evolution 84, 104377.CrossRefGoogle ScholarPubMed
Okonechnikov, K, Golosova, O, Fursov, M and the UGENE team (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics (Oxford, England) 28, 1166–1167.CrossRefGoogle ScholarPubMed
Oryan, A, Goorgipour, S, Moazeni, M and Shirian, S (2012) Abattoir prevalence, organ distribution, public health and economic importance of major metacestodes in sheep goats and cattle in Fars, southern Iran. Tropical Biomedicine 29, 349–359.Google ScholarPubMed
Perna, NT and Kocher, TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal of Molecular Evolution 41, 353–358.CrossRefGoogle ScholarPubMed
Rozas, J, Ferrer-Mata, A, Sanchez-DelBarrio, JC, Guirao Librado, P, Ramos-Onsins, SE and Sanchez-Gracia, A (2017) DnaSP v6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution 34, 3299–3302.CrossRefGoogle Scholar
Sarvi, S, Ebrahimi Behrestaghi, L, Alizadeh, A, Abdollah Hosseini, S, Gohardieh, S, Bastani, R, Yazdani Charati, J, Daryani, A, Amouei, A, Spotin, A and Gholami, S (2020) Morphometric, genetic diversity and phylogenetic analysis of Taenia hydatigena (Pallas, 1766) larval stage in Iranian livestock. Parasitology 147, 231–239.CrossRefGoogle ScholarPubMed
Scala, A, Pipia, AP, Dore, F, Sanna, G, Tamponi, C, Marrosu, R, Bandino, E, Carmona, C, Boufana, B and Varcasia, A (2015) Epidemiological updates and economic losses due to Taenia hydatigena in sheep from Sardinia, Italy. Parasitology Research 114, 3137–3143.CrossRefGoogle ScholarPubMed
Scala, A, Urrai, G, Varcasia, A, Nicolussi, P, Mulas, M, Goddi, L, Pipia, AP, Sanna, G, Genchi, M and Bandino, E (2016) Acute visceral cysticercosis by Taenia hydatigena in lambs and treatment with praziquantel. Journal of Helminthology 90, 113–116.CrossRefGoogle ScholarPubMed
Sgroi, G, Varcasia, A, D'Alessio, N, Varuzza, P, Buono, F, Amoroso, MG, Boufana, B, Otranto, D, Fioretti, A and Veneziano, V (2020) Taenia hydatigena cysticercosis in wild boar (Sus scrofa) from southern Italy: an epidemiological and molecular survey. Parasitology, 1–7. https://doi.org/10.1017/S0031182020001559.Google ScholarPubMed
Tajima, F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.CrossRefGoogle ScholarPubMed
Tamura, K and Nei, M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.Google ScholarPubMed
Varma, TK and Ahluwalia, SS (1986) Some observations on the prevalence and variations in the morphology and biology of Cysticercus tenuicollis of sheep, goat, pig and buffalo origin. Indian Journal of Animal Sciences 56, 1135–1140.Google Scholar
Varma, TK and Ahluwalia, SS (1987) Some observations on the development of Taenia hydatigena in pups and laboratory animals. Indian Journal of Animal Sciences 57, 804–811.Google Scholar
Varma, TK and Rao, BV (1973) Certain epidemiological studies on larval and strobilar phases of the common dog tapeworm Taenia hydatigena. Indian Journal of Animal Sciences 43, 534–539.Google Scholar
Wondimu, A, Abera, D and Hailu, Y (2011) A study on the prevalence, distribution and economic importance of Cysticercus tenuicollis in visceral organs of small ruminants slaughtered at an abattoir in Ethiopia. Journal of Veterinary Medicine and Animal Health 3, 67–74.Google Scholar
Supplementary material: File

Ohiolei et al. supplementary material

Ohiolei et al. supplementary material 1

Download Ohiolei et al. supplementary material(File)
File 2.1 MB
Supplementary material: File

Ohiolei et al. supplementary material

Ohiolei et al. supplementary material 2

Download Ohiolei et al. supplementary material(File)
File 19.1 KB