Folia Parasitologica 70:016 (2023) | DOI: 10.14411/fp.2023.016

European ground squirrels Spermophilus citellus (Linnaeus) do not share identical Cryptosporidium spp. with North American ground squirrels

Jana Ježková1, 2, Nikola Holubová1, Jana Kvičerová3, Jan Matějů4, Bohumil Sak1, Martin Kváč1, 2, *
1 Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech Republic;
2 Faculty of Agriculture and Technology, University of South Bohemia in České Budějovice, Czech Republic;
3 Department of Parasitology, Faculty of Science, University of South Bohemia in České Budějovice, Czech Republic;
4 Museum Karlovy Vary, Karlovy Vary, Czech Republic *Address for correspondence: Martin Kváč, Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05 České Budějovice, Czech Republic, E-mail: kvac@paru.cas.cz

Cryptosporidium Tyzzer, 1910 is one of the most common protistan parasites of vertebrates. The results of this study provide the first data on Cryptosporidium diversity in the European ground squirrel Spermophilus citellus (Linnaeus). A total of 128 faecal samples of European ground squirrels from 39 localities in the Czech Republic were analysed for the presence of Cryptosporidium spp. by microscopy and PCR/sequence analysis of small subunit ribosomal RNA (SSU) and the actin gene. While the microscopical examination did not reveal the presence of any Cryptosporidium oocysts, eight samples from six localities were PCR-positive. Phylogenetic analyses revealed the presence of five different Cryptosporidium spp. isolates. Four isolates, designated as Cryptosporidium sp. isolate Sc01-04, detected in wild populations and never recorded before, clustered closely to Cryptosporidium genotypes that have previously been found in North American ground squirrels' species. Cryptosporidium sciurinum Prediger, Ježková, Holubová, Sak, Konečný, Rost, McEvoy, Rajský et Kváč, 2021 was found in an animal sanctuary. Because C. sciurinum had previously been detected in Eurasian red squirrels Sciurus vulgaris Linnaeus at the same facility, it can be concluded that this Cryptosporidium was transmitted from tree squirrels to ground squirrels within the animal sanctuary. The results indicate that populations of European and North American ground squirrels are parasitised by different Cryptosporidium spp. At the same time, this is the first description of the occurrence of C. sciurinum in ground squirrels.

Keywords: genotyping, PCR, SSU, actin, Sciuridae, rodents

Received: March 21, 2023; Revised: June 20, 2023; Accepted: June 24, 2023; Published online: July 31, 2023  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Ježková, J., Holubová, N., Kvičerová, J., Matějů, J., Sak, B., & Kváč, M. (2023). European ground squirrels Spermophilus citellus (Linnaeus) do not share identical Cryptosporidium spp. with North American ground squirrels. Folia Parasitologica70, Article 2023.016. https://doi.org/10.14411/fp.2023.016
Download citation

References

  1. Atwill E.R., Camargo S.M., Phillips R., Alonso L.H., Tate K.W., Jensen W.A., Bennet J., Little S., Salmon T.P. 2001: Quantitative shedding of two genotypes of Cryptosporidium parvum in California ground squirrels (Spermophilus beecheyi). Appl. Environ. Microbiol. 67: 2840-2843. Go to original source...
  2. Atwill E.R., Phillips R., Pereira M.D., Li X., McCowan B. 2004: Seasonal shedding of multiple Cryptosporidium genotypes in California ground squirrels (Spermophilus beecheyi). Appl. Environ. Microbiol. 70: 6748-6752. Go to original source...
  3. Checkley W., White A.C. Jr., Jaganath D., Arrowood M.J., Chalmers R.M., Chen X.M., Fayer R., Griffiths J.K., Guerrant R.L., Hedstrom L., Huston C.D., Kotloff K.L., Kang G., Mead J.R., Miller M., Petri W.A. Jr., Priest J.W., Roos D.S., Striepen B., Thompson R.C., Ward H.D., Van Voorhis W.A., Xiao L., Zhu G., Houpt E.R. 2015: A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for Cryptosporidium. Lancet Infect. Dis. 15: 85-94. Go to original source...
  4. Feng Y., Ryan U.M., Xiao L. 2018: Genetic diversity and population structure of Cryptosporidium. Trends Parasitol. 34: 997-1011. Go to original source... Go to PubMed...
  5. Guindon S., Gascuel O. 2003: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704. Go to original source...
  6. Hall T.A. 1999: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids. Symp. Ser. 41: 95-98.
  7. Helgen K., Cole F., Helgen L., Wilson D. 2009: Generic revision in the Holarctic ground squirrel genus Spermophilus. J. Mammal. 90: 270-305. Go to original source...
  8. Horčičková M., Čondlová S., Holubová N., Sak B., Květoňová D., Hlasková L., Konečný R., Sedláček F., Clark M., Giddings C., McEvoy J., Kváč M. 2019: Diversity of Cryptosporidium in common voles and description of Cryptosporidium alticolis sp. n. and Cryptosporidium microti sp. n. (Apicomplexa: Cryptosporidiidae). Parasitology 146: 220-233. Go to original source... Go to PubMed...
  9. Huang J., Chen M., He Y., Chen H., Huang M., Li N., Ryan U., Kváč M., Feng Y., Xiao L., Guo Y. 2023: Cryptosporidium equi n. sp. (Apicomplexa: Cryptosporidiidae): biological and genetic characterisations. Int. J. Parasitol.: (in press). Go to original source...
  10. Huelsenbeck J.P., Ronquist F. 2001: MrBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755. Go to original source... Go to PubMed...
  11. Ježková J., Prediger J., Holubová N., Sak B., Konečný R., Feng Y., Xiao L., Rost M., McEvoy J., Kváč M. 2021: Cryptosporidium ratti n. sp. (Apicomplexa: Cryptosporidiidae) and genetic diversity of Cryptosporidium spp. in brown rats (Rattus norvegicus) in the Czech Republic. Parasitology 148: 84-97. Go to original source... Go to PubMed...
  12. Kloch A., Bajer A. 2012: Natural infections with Cryptosporidium in the endangered spotted souslik (Spermophilus suslicus). Acta Parasitol. 57: 13-19. Go to original source... Go to PubMed...
  13. Kváč M., Hofmannová L., Bertolino S., Wauters L., Tosi G., Modrý D. 2008: Natural infection with two genotypes of Cryptosporidium in red squirrels (Sciurus vulgaris) in Italy. Folia Parasitol. 55: 95-99. Go to original source...
  14. Kváč M., McEvoy J., Loudová M., Stenger B., Sak B., Květoňová D., Ditrich O., Rašková V., Moriarty E., Rost M., Macholán M., Piálek J. 2013: Coevolution of Cryptosporidium tyzzeri and the house mouse (Mus musculus). Int. J. Parasitol. 43: 805-817. Go to original source...
  15. Li W., Xiao L.H. 2019: Multilocus sequence typing and population genetic analysis of Enterocytozoon bieneusi: host specificity and its impacts on public health. Front. Genet. 10: 307. Go to original source... Go to PubMed...
  16. Li X., Pereira M., Larsen R., Xiao C., Phillips R., Striby K., McCowan B., Atwill E.R. 2015: Cryptosporidium rubeyi n. sp. (Apicomplexa: Cryptosporidiidae) in multiple Spermophilus ground squirrel species. Int. J. Parasitol. Parasites Wildl. 4: 343-350. Go to original source...
  17. Miláček P., Vítovec J. 1985: Differential staining of cryptosporidia by aniline-carbol-methyl violet and tartrazine in smears from feces and scrapings of intestinal mucosa. Folia Parasitol. 32: 50.
  18. Nader J.L., Mathers T.C., Ward B.J., Pachebat J.A., Swain M.T., Robinson G., Chalmers R.M., Hunter P.R., van Oosterhout C., Tyler K.M. 2019: Evolutionary genomics of anthroponosis in Cryptosporidium. Nat. Microbiol. 4: 826-836. Go to original source... Go to PubMed...
  19. Nakamura A.A., Meireles M.V. 2015: Cryptosporidium infections in birds - a review. Rev. Bras. Parasitol. Vet. 24: 253-267. Go to original source... Go to PubMed...
  20. Page R.D. 1996: TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12: 357-358. Go to original source... Go to PubMed...
  21. Pereira M., Li X., McCowan B., Phillips R.L., Atwill E.R. 2010: Multiple unique Cryptosporidium isolates from three species of ground squirrels (Spermophilus beecheyi, S. beldingi, and S. lateralis) in California. Appl. Environ. Microbiol. 76: 8269-8276. Go to original source...
  22. Prediger J., Horčičková M., Hofmannová L., Sak B., Ferrari N., Mazzamuto M.V., Romeo C., Wauters L.A., McEvoy J., Kváč M. 2017: Native and introduced squirrels in Italy host different Cryptosporidium spp. Eur. J. Protistol. 61: 64-75. Go to original source... Go to PubMed...
  23. Prediger J., Ježková J., Holubová N., Sak B., Konečný R., Rost M., McEvoy J., Rajský D., Kváč M. 2021: Cryptosporidium sciurinum n. sp. (Apicomplexa: Cryptosporidiidae) in Eurasian red squirrels (Sciurus vulgaris). Microorganisms 9: 2050. Go to original source... Go to PubMed...
  24. Ryan U.M., Feng Y., Fayer R., Xiao L. 2021: Taxonomy and molecular epidemiology of Cryptosporidium and Giardia - a 50 year perspective (1971-2021). Int. J. Parasitol. 51: 1099-1119. Go to original source...
  25. Santín M., Trout J.M., Fayer R. 2008: A longitudinal study of cryptosporidiosis in dairy cattle from birth to 2 years of age. Vet. Parasitol. 155: 15-23. Go to original source... Go to PubMed...
  26. Stenger B.L., Clark M.E., Kváč M., Khan E., Giddings C.W., Prediger J., McEvoy J.M. 2015: North American tree squirrels and ground squirrels with overlapping ranges host different Cryptosporidium species and genotypes. Infect. Genet. Evol. 36: 287-293. Go to original source... Go to PubMed...
  27. Stenger B.L.S., Horčičková M., Clark M.E., Kváč M., Čondlová S., Khan E., Widmer G., Xiao L., Giddings C.W., Pennil C., Stanko M., Sak B., McEvoy J.M. 2017: Cryptosporidium infecting wild cricetid rodents from the subfamilies Arvicolinae and Neotominae. Parasitology 145: 326-334. Go to original source... Go to PubMed...
  28. Sulaiman I.M., Lal A.A., Xiao L. 2002: Molecular phylogeny and evolutionary relationships of Cryptosporidium parasites at the actin locus. J. Parasitol. 88: 388-394. Go to original source... Go to PubMed...
  29. Tůmová L., Ježková J., Prediger J., Holubová N., Sak B., Konečný R., Květoňová D., Hlásková L., Rost M., McEvoy J., Xiao L., Santín M., Kváč M. 2023: Cryptosporidium mortiferum n. sp. (Apicomplexa: Cryptosporidiidae), the species causing lethal cryptosporidiosis in Eurasian red squirrels (Sciurus vulgaris). Parasit. Vectors. 16: 235 Go to original source... Go to PubMed...
  30. Xiao L., Escalante L., Yang C., Sulaiman I., Escalante A.A., Montali R.J., Fayer R., Lal A.A. 1999: Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Appl. Environ. Microbiol. 65: 1578-1583. Go to original source...
  31. Xu J., Liu H., Jiang Y., Jing H., Cao J., Yin J., Li T., Sun Y., Shen Y., Wang X. 2022: Genotyping and subtyping of Cryptosporidium spp. and Giardia duodenalis isolates from two wild rodent species in Gansu Province, China. Sci. Rep. 12: 12178. Go to original source... Go to PubMed...