Skip to main content
SpringerLink
Log in

Molecular identification of the rodent-borne pathogen Rodentolepis nana using the genetic markers of ITS-1, 18 S, and 28 S rDNA

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Background

Rodentolepis nana (syn. Hymenolepis nana), the most common cyclophyllid tapeworm infecting rodents, is a well-studied gastrointestinal parasite in mice and belongs to the family Hymenolepididae.

Methods

The present study focuses on the molecular analysis for the nuclear genes (ITS-1, 18 S, and 28 S rDNA) used for the accurate recognition of the recovered Rodentolepis species.

Results

The annotated partial ITS-1, 18 S, and 28 S rDNA gene regions were deposited in GenBank (gbǀ MW310394.1, gbǀ MW327585.1, and gbǀ MW324479.1, respectively) and further used in the maximum likelihood method (ML) to clarify their genetic relationships at the species level. The interrogation sequence of R. nana was aligned and belonged to the family Hymenolepididae, in the same group as all Hymenolepis species, which were distinct from Cyclophyllidea cestodes, especially species belonging to Anoplocephalidae and Taeniidae. Sequence data support the paraphyly of Hymenolepis species.

Conclusions

The phylogeny supports the availability of the ITS-1, 18 S, and 28 S rDNA genes as reliable genetic markers for evolutionary relationships.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

All data generated or analyzed as part of this study are included in this published article.

References

  1. Georgiev BB (2003) Cestoda (Tapeworms). In: (In: Thoney DA (ed) Schlager) Lower Metazoans and Lesser Deuterostomes. Grzimek's Animal Life Encyclopedia, vol 1, 2nd edn. Gale, Detroit

    Google Scholar 

  2. Ariola V (1899) II gen. Scyphocephalus Rigg. E proposta di una nuova classificazione dei cestodi. Atti Soc Ligust Sci Nat Geogr 10:160–167

    Google Scholar 

  3. Mariaux J, Tkach VV, Vasileva GP, Waeschenbach A, Beveridge I, Dimitrova YD, Haukisalmi V, Greiman SE, Littlewood DTJ, Makarikov AA, Phillips AJ, Razafiarisolo T, Widmer V, Georgiev BB (2017) Cyclophyllidea van Beneden in Braun, 1900. In: In: Caira JN, Jensen K (eds) Planetary Biodiversity Inventory (2008–2017): Tapeworms from Vertebrate Bowels of the Earth. University of Kansas, Natural History Museum, Lawrence

    Google Scholar 

  4. Weinland DF (1858) Human cestoides. An essay on the tapeworms of man. Metcalf & Co, Cambridge, p 93

    Google Scholar 

  5. Sulima A, Savijoki K, Bien J, Näreaho A, Salamatin R, Conn DB, Mlocicki D (2018) Comparative proteomic analysis of Hymenolepis diminuta cysticercoid and adult stages. Front Microbiol 8:2672

    Article  Google Scholar 

  6. Willcocks B, McAuliffe GN, Baird RW (2015) Dwarf tapeworm (Hymenolepis nana): characteristics in the Northern Territory 2002-2013. Aust Paediatric J 51:982–987

    Google Scholar 

  7. Jarošová J, Šnábel V, Cavallero S, Chovancová Z, Antolová D (2020) The mouse bile duct tapeworm, Hymenolepis living small mammals in Slovakia: Occurrence and genetic analysis. Helminthologia 57:120–128

    Article  Google Scholar 

  8. Thompson RC (2015) Neglected zoonotic helminthes Hymenolepis nana, Echinococcus canadensis and Ancylostoma ceylanicum. Clin Microbiol Infect 21:426–432

    Article  CAS  Google Scholar 

  9. Gliga DS, Pisanu B, Walzer C, Desvars-Larrive A (2020) Helminths of urban rats in developed countries: a systematic review to identify research gaps. Helminthology 119:2383–2397

    Google Scholar 

  10. Foronda P, López-González M, Ferrer MH, Makarikov V, Feliu C (2011) Distribution and genetic variation of hymenolepidid cestodes in murid rodents on the Canary Islands (Spain). Parasit Vectors 4:185

    Article  Google Scholar 

  11. Shahnazi M, Mehrizi MZ, Alizadeh SA, Heydarian P, Saraei M, Alipour M, Hajialilo E (2019) Molecular characterization of Hymenolepis nana based on nuclear rDNA ITS2 gene marker. Afr Health Sci 19:1–7

    Article  Google Scholar 

  12. Gibson DI (1998) Nature and classification of parasitic helminths. In Topley and Wilsons: Microbiology and Microbial Infections, pp. 453-477. Edited by F. E. G. Cox, J. P. Kreier and D. Wakelin. London: Arnold. https://doi.org/10.1002/9780470688618.taw0192

  13. Haukisalmi V, Hardman LM, Foronda P, Feliu C, Laakkonen J, Niemimaa J, Lehtonen JT, Henttonen H (2010) Systematic relationships of hymenolepidid cestodes of rodents and shrews inferred from sequences of 28S ribosomal RNA. Zool Scripta 39:631–641

    Article  Google Scholar 

  14. Tijjani M, Majid RA, Abdullahi SA, Unyah NZ (2020) Detection of rodent-borne parasitic pathogens of wild rats in Serdang, Slangor, Malaysia: A potential threat to human health. Int J Parasitol Parasites Wildl 11:174–182

    Article  Google Scholar 

  15. Coleman AW (2003) ITS-2 is a double-edged tool for eukaryotic evolutionary comparisons. Trends Genet 19:370–375

    Article  CAS  Google Scholar 

  16. Waeschenbach A, Webster BL, Bray RA, Littlewood DTJ (2007) Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Mol Phylogenet Evol 45:311–325

    Article  CAS  Google Scholar 

  17. Al-Olayan E, Elamin M, Alshehri E, Aloufi A, Alanazi Z, Almayouf M, Bakr L, Abdel-Gaber R (2020) Morphological, molecular, and pathological appraisal of Hymenolepis nana (Hymenolepididae) infecting Laboratory mice (Mus musculus). Microsc Microanal 26:348–362

    Article  CAS  Google Scholar 

  18. Baehellerie J-P, Qu L-H (1993) Ribosomal RNA probes for detection and identification of species. In: In: Hyde JE (ed) Protocols in molecular parasitology. Humana Press, New Jersey

    Google Scholar 

  19. Littlewood DTJ, Olson PD (2001) Small subunit rDNA and the phylum Platyhelminthes: signal, noise, conflict and compromise. In: In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London

    Google Scholar 

  20. Littlewood DTJ, Waeschenbach A, Nikolov PN (2008) In search of mitochondrial marker for resolving the phylogeny of cyclophyllidean tapeworms (Platyhelminths, Cestode) – a test study with Davaineidae. Acta Parasitol 53:133–144

    Article  CAS  Google Scholar 

  21. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  22. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  23. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0. Mol Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  24. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  25. Rokni M (2008) The present status of human helminthic diseases in Iran. Ann Trop Med Parasitol 102:283–295

    Article  CAS  Google Scholar 

  26. Král’ová I, Špakulová M (1996) Interspecific variability of Proteocephalidae exiguus La Rue, 1911 (Cestoda: Proteocephalidae) as studied by the random amplified polymorphic DNA method (RAPD). Parasitol Res 82:542–545

    Article  Google Scholar 

  27. Zhu XQ, Amelio SD, Gasser RB, Yang TB, Paggi L, He F, Lin RQ, Song HQ, Ai L, Li AX (2007) Practical PCR tools for the delineation of Contracaecum rudolphii A and Contracaecum rudolphii B (Ascaridoidea: Anisakidae) using genetic markers in nuclear ribosomal DNA. Mol Cell Probes 21:97–102

    Article  CAS  Google Scholar 

  28. Macnish MG, Morgan-Ryan UM, Monis PT, Behnke JM, Thompson RCA (2002) A molecular phylogeny of nuclear and mitochondrial sequences in Hymenolepis nana (Cestoda) supports the existence of a cryptic species. Parasitology 125:567–575

    Article  CAS  Google Scholar 

  29. Mariaux J (1998) A molecular phylogeny of the Eucestoda. J Parasitol 84:114–124

    Article  CAS  Google Scholar 

  30. Hoberg EP, Mariaux J, Brooks DR (2001) Phylogeny among orders of the Eucestoda (Cercomeromorphae): Integrating morphology, molecules and total evidence. In: In: Littlewood DJT, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp 112–126

    Google Scholar 

  31. Al-Quraishy S, Abdel-Gaber R, Alajmi R, Dkhil MA, Al-Jawher M, Morsy K (2019) Morphological and molecular appraisal of cyclophyllidean cestoda parasite Raillietina saudiae sp. nov. infecting the domestic pigeon Columba livia domestica and its role as a bio-indicator for environmental quality. Parasitol Inter 71:59–72

    Article  Google Scholar 

  32. Nickisch-Rosenegk M, Lucius R, Loosfrank B (1999) Contribution to the Phylogeny of the Cyclophyllidea (Cestoda) inferred from mitochondrial 12S rDNA. J Mol Evol 48:586–596

    Article  Google Scholar 

  33. Sharma S, Lyngdoh D, Roy B, Tandon V (2016) Differential diagnosis and molecular characterization of Hymenolepis nana and Hymenolepis diminuta (Cestoda: Cyclophyllidea: Hymenolepididae) based on nuclear rDNA ITS2 gene marker. Parasitol Res 115:4293–4298

    Article  Google Scholar 

  34. Jarošová J, Antolová D, Šnábel V, Miklisová D, Cavallero S (2020) The dwarf tapeworm Hymenolepis nana in pet rodents in Slovakia – epidemiological survey and genetic analysis. Parasitol Res 119:519–527

    Article  Google Scholar 

  35. Ito A, Onitake K, Andreassen J (1988) Lumen phase-specific cross-immunity between Hymenolepis microstoma and H. nana in mice. Inter J Parasitol 18:1019–1027

    Article  CAS  Google Scholar 

  36. Nkouawa A, Haukisalmi V, Li T, Nakao M, Lavikainen A, Chen X, Henttonen H, Ito A (2016) Cryptic diversity in hymenolepidid tapeworms infecting humans. Parasitol Inter 65:83–86

    Article  Google Scholar 

  37. Mirjalali H, Kia EB, Kamranrashani B, Hajjaran H, Sharifdini M (2015) Molecular analysis of isolates of the cestoda Rodentolepis nana from the great gerbil, Rhombomys opimus. J Helminthol 90:1–4

    Google Scholar 

Download references

Acknowledgements

This study was supported by the Researchers Supporting Project Number (RSP-2021/25), King Saud University, Riyadh, Saudi Arabia.

Author information

Authors and Affiliations

  1. Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia

    Ohoud Al-Amri, Saleh Al-Quraishy, Esam M. Al-Shaebi, Hossam M. A. Aljawdah & Rewaida Abdel-Gaber

Authors
  1. Ohoud Al-Amri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saleh Al-Quraishy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Esam M. Al-Shaebi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hossam M. A. Aljawdah
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rewaida Abdel-Gaber
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rewaida Abdel-Gaber.

Ethics declarations

Conflict of interest

The authors have no conflict of interest related to the content of this article.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Al-Amri, O., Al-Quraishy, S., Al-Shaebi, E.M. et al. Molecular identification of the rodent-borne pathogen Rodentolepis nana using the genetic markers of ITS-1, 18 S, and 28 S rDNA. Mol Biol Rep 49, 1361–1367 (2022). https://doi.org/10.1007/s11033-021-06966-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-021-06966-x

Keywords

Search

Navigation