Cryptosporidium sciurinum n. sp. (Apicomplexa: Cryptosporidiidae) in Eurasian Red Squirrels (Sciurus vulgaris)
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
21-23773S
Grantová Agentura České Republiky
028/2019/Z
Grant Agency of the University of South Bohemia
PubMed
34683369
PubMed Central
PMC8537388
DOI
10.3390/microorganisms9102050
PII: microorganisms9102050
Knihovny.cz E-zdroje
- Klíčová slova
- Cryptosporidium sp. ferret genotype, biology, course of infection, infectivity, occurrence, oocyst size, phylogeny,
- Publikační typ
- časopisecké články MeSH
Cryptosporidium spp. are common protozoan pathogens in mammals. The diversity and biology of Cryptosporidium in tree squirrels are not well studied. A total of 258 Eurasian red squirrels (Sciurus vulgaris) from 25 and 15 locations in the Czech Republic and Slovakia, respectively, were examined for Cryptosporidium spp. oocysts and specific DNA at the SSU, actin, HSP70, TRAP-C1, COWP, and gp60 loci. Out of 26 positive animals, only juveniles (9/12) were microscopically positive (18,000 to 72,000 OPG), and molecular analyses revealed the presence of Cryptosporidium sp. ferret genotype in all specimens. Oocysts obtained from naturally-infected squirrels measured 5.54-5.22 μm and were not infectious for laboratory mice (BALB/c and SCID), Mongolian gerbils, Guinea pigs, Southern multimammate mice, chickens, or budgerigars. None of naturally infected squirrels showed clinical signs of disease. The frequency of occurrence of the ferret genotype in squirrels did not vary statistically based on host age, gender or country of capture. Phylogenetic analysis of sequences from six loci revealed that Cryptosporidium sp. ferret genotype is genetically distinct from the currently accepted Cryptosporidium species. Morphological and biological data from this and previous studies support the establishment of Cryptosporidium sp. ferret genotype as a new species, Cryptosporidium sciurinum n. sp.
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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. Evolutionary genomics of anthroponosis in Cryptosporidium. Nat. Microbiol. 2019;4:826–836. doi: 10.1038/s41564-019-0377-x. PubMed DOI
Caccio S.M., Putignani L. Epidemiology of Human Cryptosporidiosis. In: Cacciò S.M., Widmer G., editors. Cryptosporidium: Parasite and Disease. 1st ed. Springer; Vienna, Austria: 2014. pp. 43–80.
Kváč M., McEvoy J., Stenger B., Clark M. Cryptosporidiosis in other vertebrates. In: Cacciò S.M., Widmer G., editors. Cryptosporidium: Parasite and Disease. 1st ed. Springer; Vienna, Austria: 2014. pp. 237–326.
Zahedi A., Bolland S.J., Oskam C.L., Ryan U. Cryptosporidium abrahamseni n. sp. (Apicomplexa: Cryptosporidiiae) from red-eye tetra (Moenkhausia sanctaefilomenae) Exp. Parasitol. 2021;223:108089. doi: 10.1016/j.exppara.2021.108089. PubMed DOI
Ryan U.M., Monis P., Enemark H.L., Sulaiman I., Samarasinghe B., Read C., Buddle R., Robertson I., Zhou L., Thompson R.C.A., et al. Cryptosporidium suis n. sp. (Apicomplexa: Cryptosporidiidae) in pigs (Sus scrofa) J. Parasitol. 2004;90:769–773. doi: 10.1645/GE-202R1. PubMed DOI
Bujila I., Troell K., Fischerstrom K., Nordahl M., Killander G., Hansen A., Soderlund R., Lebbad M., Beser J. Cryptosporidium chipmunk genotype I—An emerging cause of human cryptosporidiosis in Sweden. Infect. Genet. Evol. 2021;92:104895. doi: 10.1016/j.meegid.2021.104895. PubMed DOI
Sundberg J.P., Hill D., Ryan M.J. Cryptosporidiosis in a gray squirrel. J. Am. Vet. Med. Assoc. 1982;181:1420–1422. PubMed
Current W.L. Cryptosporidium spp. In: Walzer P.D., Genta R.M., editors. Parasitic Infections in the Compromised Host. Dekker; New York, NY, USA: 1990. pp. 281–341.
Stenger B.L., Clark M.E., Kváč M., Khan E., Giddings C.W., Prediger J., McEvoy J.M. North American tree squirrels and ground squirrels with overlapping ranges host different Cryptosporidium species and genotypes. Infect. Genet. Evol. 2015;36:287–293. doi: 10.1016/j.meegid.2015.10.002. PubMed DOI
Ziegler P.E., Wade S.E., Schaaf S.L., Chang Y.F., Mohammed H.O. Cryptosporidium spp. from small mammals in the New York City watershed. J. Wildl. Dis. 2007;43:586–596. doi: 10.7589/0090-3558-43.4.586. PubMed DOI
Ziegler P.E., Wade S.E., Schaaf S.L., Stern D.A., Nadareski C.A., Mohammed H.O. Prevalence of Cryptosporidium species in wildlife populations within a watershed landscape in southeastern New York State. Vet. Parasitol. 2007;147:176–184. doi: 10.1016/j.vetpar.2007.03.024. PubMed DOI
Feng Y., Alderisio K.A., Yang W., Blancero L.A., Kuhne W.G., Nadareski C.A., Reid M., Xiao L. Cryptosporidium genotypes in wildlife from a New York watershed. Appl. Environ. Microbiol. 2007;73:6475–6483. doi: 10.1128/AEM.01034-07. PubMed DOI PMC
Lv C., Zhang L., Wang R., Jian F., Zhang S., Ning C., Wang H., Feng C., Wang X., Ren X., et al. Cryptosporidium spp. in wild, laboratory, and pet rodents in china: Prevalence and molecular characterization. Appl. Environ. Microbiol. 2009;75:7692–7699. doi: 10.1128/AEM.01386-09. PubMed DOI PMC
Chai Y.J., Deng L., Liu H.F., Yao J.X., Zhong Z.J., Xiang L.Q., Fu H.L., Shen L.H., Zhou Z.Y., Deng J.L., et al. First detection of Cryptosporidium spp. in red-bellied tree squirrels (Callosciurus erythraeus) in China. Parasite. 2019;26:28. doi: 10.1051/parasite/2019029. PubMed DOI PMC
Deng L., Chai Y., Luo R., Yang L., Yao J., Zhong Z., Wang W., Xiang L., Fu H., Liu H., et al. Occurrence and genetic characteristics of Cryptosporidium spp. and Enterocytozoon bieneusi in pet red squirrels (Sciurus vulgaris) in China. Sci. Rep. 2020;10:1026. doi: 10.1038/s41598-020-57896-w. PubMed DOI PMC
Kváč M., Hofmannová L., Bertolino S., Wauters L., Tosi G., Modrý D. Natural infection with two genotypes of Cryptosporidium in red squirrels (Sciurus vulgaris) in Italy. Folia Parasitol. 2008;55:95–99. doi: 10.14411/fp.2008.012. PubMed DOI
Prediger J., Horčičková M., Hofmannová L., Sak B., Ferrari N., Mazzamuto M.V., Romeo C., Wauters L.A., McEvoy J., Kváč M. Native and introduced squirrels in Italy host different Cryptosporidium spp. Eur. J. Protistol. 2017;61:64–75. doi: 10.1016/j.ejop.2017.09.007. PubMed DOI
Wauters L., Dhondt A.A. Body-Weight, Longevity and Reproductive Success in Red Squirrels (Sciurus vulgaris) J. Anim. Ecol. 1989;58:637–651. doi: 10.2307/4853. DOI
Miláček P., Vítovec J. Differential staining of cryptosporidia by aniline-carbol-methyl violet and tartrazine in smears from feces and scrapings of intestinal mucosa. Folia Parasitol. 1985;32:50. PubMed
Kváč M., Ondráčková Z., Květoňová D., Sak B., Vítovec J. Infectivity and pathogenicity of Cryptosporidium andersoni to a novel host, southern multimammate mouse (Mastomys coucha) Vet. Parasitol. 2007;143:229–233. doi: 10.1016/j.vetpar.2006.08.031. PubMed DOI
Arrowood M.J., Donaldson K. Improved purification methods for calf-derived Cryptosporidium parvum oocysts using discontinuous sucrose and cesium chloride gradients. J. Eukaryot. Microbiol. 1996;43:89S. doi: 10.1111/j.1550-7408.1996.tb05015.x. PubMed DOI
Sauch J.F., Flanigan D., Galvin M.L., Berman D., Jakubowski W. Propidium iodide as an indicator of Giardia cyst viability. Appl. Environ. Microbiol. 1991;57:3243–3247. doi: 10.1128/aem.57.11.3243-3247.1991. PubMed DOI PMC
Xiao L., Escalante L., Yang C., Sulaiman I., Escalante A.A., Montali R.J., Fayer R., Lal A.A. Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Appl. Environ. Microbiol. 1999;65:1578–1583. doi: 10.1128/AEM.65.4.1578-1583.1999. PubMed DOI PMC
Sulaiman I.M., Morgan U.M., Thompson R.C., Lal A.A., Xiao L. Phylogenetic relationships of Cryptosporidium parasites based on the 70-kilodalton heat shock protein (HSP70) gene. Appl. Environ. Microbiol. 2000;66:2385–2391. doi: 10.1128/AEM.66.6.2385-2391.2000. PubMed DOI PMC
Sulaiman I.M., Lal A.A., Xiao L.H. Molecular phylogeny and evolutionary relationships of Cryptosporidium parasites at the actin locus. J. Parasitol. 2002;88:388–394. doi: 10.1645/0022-3395(2002)088[0388:MPAERO]2.0.CO;2. PubMed DOI
Spano F., Putignani L., Naitza S., Puri C., Wright S., Crisanti A. Molecular cloning and expression analysis of a Cryptosporidium parvum gene encoding a new member of the thrombospondin family. Mol. Biochem. Parasitol. 1998;92:147–162. doi: 10.1016/S0166-6851(97)00243-0. PubMed DOI
Jiang J., Alderisio K.A., Xiao L. Distribution of Cryptosporidium genotypes in storm event water samples from three watersheds in New York. Appl. Environ. Microbiol. 2005;71:4446–4454. doi: 10.1128/AEM.71.8.4446-4454.2005. PubMed DOI PMC
Spano F., Puri C., Ranucci L., Putignani L., Crisanti A. Cloning of the entire COWP gene of Cryptosporidium parvum and ultrastructural localization of the protein during sexual parasite development. Pt 5Parasitology. 1997;114:427–437. doi: 10.1017/S0031182096008761. PubMed DOI
Alves M., Xiao L.H., Sulaiman I., Lal A.A., Matos O., Antunes F. Subgenotype analysis of Cryptosporidium isolates from humans, cattle, and zoo ruminants in Portugal. J. Clin. Microbiol. 2003;41:2744–2747. doi: 10.1128/JCM.41.6.2744-2747.2003. PubMed DOI PMC
Hall T.A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids. Symp. Ser. 1999;41:95–98.
Henriksen S.A., Pohlenz J.F. Staining of cryptosporidia by a modified Ziehl-Neelsen technique. Acta Vet. Scand. 1981;22:594–596. doi: 10.1186/BF03548684. PubMed DOI PMC
Kváč M., Vítovec J. Prevalence and pathogenicity of Cryptosporidium andersoni in one herd of beef cattle. J. Vet. Med. B. 2003;50:451–457. doi: 10.1046/j.0931-1793.2003.00701.x. PubMed DOI
Holubová N., Zikmundová V., Limpouchová Z., Sak B., Konečný R., Hlásková L., Rajský D., Kopacz Z., McEvoy J., Kváč M. Cryptosporidium proventriculi sp. n. (Apicomplexa: Cryptosporidiidae) in Psittaciformes birds. Eur. J. Protistol. 2019;69:70–87. doi: 10.1016/j.ejop.2019.03.001. PubMed DOI
Team R.C. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; Vienna, Austria: 2019.
Xiao L., Morgan U.M., Limor J., Escalante A., Arrowood M., Shulaw W., Thompson R.C., Fayer R., Lal A.A. Genetic diversity within Cryptosporidium parvum and related Cryptosporidium species. Appl. Environ. Microbiol. 1999;65:3386–3391. doi: 10.1128/AEM.65.8.3386-3391.1999. PubMed DOI PMC
Li Q., Li L., Tao W., Jiang Y., Wan Q., Lin Y., Li W. Molecular investigation of Cryptosporidium in small caged pets in northeast China: Host specificity and zoonotic implications. Parasitol. Res. 2016;115:2905–2911. doi: 10.1007/s00436-016-5076-4. PubMed DOI
ICZN International Commission on Zoological Nomenclature: Amendment of articles 8, 9, 10, 21 and 78 of the international code of zoologicalnomenclature to expand and refine methods of publication. Bull. Zool. Nomencl. 2012;69:161–169. doi: 10.21805/bzn.v69i3.a8.161. PubMed DOI
Stenger B.L.S., Horčičková M., Clark M.E., Kváč M., Čondlová S., Khan E., Widmer G., Xiao L., Giddings C.W., Pennil C., et al. Cryptosporidium infecting wild cricetid rodents from the subfamilies Arvicolinae and Neotominae. Parasitology. 2017;145:326–334. doi: 10.1017/S0031182017001524. PubMed DOI PMC
Li F.L., Zhang Z.J., Hu S.H., Zhao W.T., Zhao J.G., Kváč M., Guo Y.Q., Li N., Feng Y.Y., Xiao L.H. Common occurrence of divergent Cryptosporidium species and Cryptosporidium parvum subtypes in farmed bamboo rats (Rhizomys sinensis) Parasites Vectors. 2020;13:149. doi: 10.1186/s13071-020-04021-5. PubMed DOI PMC
Ježková J., Prediger J., Holubová N., Sak B., Konečný R., Feng Y., Xiao L., Rost M., McEvoy J., Kváč M. Cryptosporidium ratti n. sp. (Apicomplexa: Cryptosporidiidae) and genetic diversity of Cryptosporidium spp. in brown rats (Rattus norvegicus) in the Czech Republic. Parasitology. 2021;148:84–97. doi: 10.1017/S0031182020001833. PubMed DOI PMC
Murakoshi F., Fukuda Y., Matsubara R., Kato Y., Sato R., Sasaki T., Tada C., Nakai Y. Detection and genotyping of Cryptosporidium spp. in large Japanese field mice, Apodemus speciosus. Vet. Parasitol. 2013;196:184–188. doi: 10.1016/j.vetpar.2013.02.011. PubMed DOI
Čondlová S., Horčičková M., Havrdová N., Sak B., Hlásková L., Perec-Matysiak A., Kicia M., McEvoy J., Kváč M. Diversity of Cryptosporidium spp. in Apodemus spp. in Europe. Eur. J. Protistol. 2019;69:1–13. doi: 10.1016/j.ejop.2019.02.005. PubMed DOI PMC
Čondlová S., Horčičková M., Sak B., Květoňová D., Hlásková L., Konečný R., Stanko M., McEvoy J., Kváč M. Cryptosporidiumapodemi sp. n. and Cryptosporidium ditrichi sp. n. (Apicomplexa: Cryptosporidiidae) in Apodemus spp. Eur. J. Protistol. 2018;63:1–12. doi: 10.1016/j.ejop.2017.12.006. PubMed DOI
Horčičková M., Čondlová S., Holubová N., Sak B., Květoňová D., Hlásková L., Konečný R., Sedláček F., Clark M., Giddings C., et al. Diversity of Cryptosporidium in common voles and description of Cryptosporidium alticolis sp. n. and Cryptosporidium microti sp. n. (Apicomplexa: Cryptosporidiidae) Parasitology. 2019;146:220–233. doi: 10.1017/S0031182018001142. PubMed DOI PMC
Holubová N., Sak B., Hlásková L., Květoňová D., Hanzal V., Rajský D., Rost M., McEvoy J., Kváč M. Host specificity and age-dependent resistance to Cryptosporidium avium infection in chickens, ducks and pheasants. Exp. Parasitol. 2018;191:62–65. doi: 10.1016/j.exppara.2018.06.007. PubMed DOI
Pavlásek I. Findings of cryptosporidia in the stomach of hens and of exotic and wild birds. Veterinářství (Czech) 2001;51:103–108.
Sreter T., Varga I., Bekesi L. Age-dependent resistance to Cryptosporidium baileyi infection in chickens. J. Parasitol. 1995;81:827–829. doi: 10.2307/3283992. PubMed DOI
Rhee J.K., So W.S., Kim H.C. Age-dependent resistance to Cryptosporidium muris (strain MCR) infection in golden hamsters and mice. Korean J. Parasitol. 1999;37:33–37. doi: 10.3347/kjp.1999.37.1.33. PubMed DOI PMC
Kváč M., Sak B., Květoňová D., Secor W.E. Infectivity of gastric and intestinal Cryptosporidium species in immunocompetent Mongolian gerbils (Meriones unguiculatus) Vet. Parasitol. 2009;163:33–38. doi: 10.1016/j.vetpar.2009.03.047. PubMed DOI
Kváč M., Kestřánová M., Květoňová D., Kotková M., Ortega Y., McEvoy J., Sak B. Cryptosporidium tyzzeri and Cryptosporidium muris originated from wild West-European house mice (Mus musculus domesticus) and East-European house mice (Mus musculus musculus) are non-infectious for pigs. Exp. Parasitol. 2012;131:107–110. doi: 10.1016/j.exppara.2012.03.016. PubMed DOI
Graczyk T.K., Cranfield M.R. Experimental transmission of Cryptosporidium oocyst isolates from mammals, birds and reptiles to captive snakes. Vet. Res. 1998;29:187–195. PubMed
Graczyk T.K., Cranfield M.R., Fayer R. Oocysts of Cryptosporidium from snakes are not infectious to ducklings but retain viability after intestinal passage through a refractory host. Vet. Parasitol. 1998;77:33–40. doi: 10.1016/S0304-4017(97)00137-4. PubMed DOI
Crawshaw G.J., Mehren K.G. Erkrankungen der Zootiere, Verhandlungsbericht des 29, Proceedings of the Internationalen Symposiums Uber die Erkrankungen der Zootiere, Cardiff, UK, 20–24 May 1987. Internationales Symposium uber die Erkrankungen der Zoo- und Wildtiere; Berlin, Germany: 1987. Cryptosporidiosis in Zoo and Wild Animals; pp. 353–362.
Stenger B.L., Clark M.E., Kváč M., Khan E., Giddings C.W., Dyer N.W., Schultz J.L., McEvoy J.M. Highly divergent 18S rRNA gene paralogs in a Cryptosporidium genotype from eastern chipmunks (Tamias striatus) Infect. Genet. Evol. 2015;32:113–123. doi: 10.1016/j.meegid.2015.03.003. PubMed DOI PMC
Le Blancq S.M., Khramtsov N.V., Zamani F., Upton S.J., Wu T.W. Ribosomal RNA gene organization in Cryptosporidium parvum. Mol. Biochem. Parasitol. 1997;90:463–478. doi: 10.1016/S0166-6851(97)00181-3. PubMed DOI
Ng-Hublin J.S., Singleton G.R., Ryan U. Molecular characterization of Cryptosporidium spp. from wild rats and mice from rural communities in the Philippines. Infect. Genet. Evol. 2013;16:5–12. doi: 10.1016/j.meegid.2013.01.011. PubMed DOI
Li N., Xiao L., Alderisio K., Elwin K., Cebelinski E., Chalmers R., Santin M., Fayer R., Kváč M., Ryan U., et al. Subtyping Cryptosporidium ubiquitum, a zoonotic pathogen emerging in humans. Emerg. Infect. Dis. 2014;20:217–224. doi: 10.3201/eid2002.121797. PubMed DOI PMC
Ježková J., Limpouchová Z., Prediger J., Holubová N., Sak B., Konečný R., Květoňová D., Hlásková L., Rost M., McEvoy J., et al. Cryptosporidium myocastoris n. sp. (Apicomplexa: Cryptosporidiidae), the Species Adapted to the Nutria (Myocastor coypus) Microorganisms. 2021;9:813. doi: 10.3390/microorganisms9040813. PubMed DOI PMC
Kváč M., McEvoy J., Loudová M., Stenger B., Sak B., Květoňová D., Ditrich O., Rašková V., Moriarty E., Rost M., et al. Coevolution of Cryptosporidium tyzzeri and the house mouse (Mus musculus) Int. J. Parasitol. 2013;43:805–817. doi: 10.1016/j.ijpara.2013.04.007. PubMed DOI PMC
Xiao L. Molecular epidemiology of cryptosporidiosis: An update. Exp. Parasitol. 2010;124:80–89. doi: 10.1016/j.exppara.2009.03.018. PubMed DOI
High Occurrence of Zoonotic Subtypes of Cryptosporidiumparvum in Cypriot Dairy Farms