We undertook a study on Cryptosporidium spp. in wild cricetid rodents. Fecal samples were collected from meadow voles (Microtus pennsylvanicus), southern red-backed voles (Myodes gapperi), woodland voles (Microtus pinetorum), muskrats (Ondatra zibethicus) and Peromyscus spp. mice in North America, and from bank voles (Myodes glareolus) and common voles (Microtus arvalis) in Europe. Isolates were characterized by sequence and phylogenetic analyses of the small subunit ribosomal RNA (SSU) and actin genes. Overall, 33·2% (362/1089) of cricetids tested positive for Cryptosporidium, with a greater prevalence in cricetids from North America (50·7%; 302/596) than Europe (12·1%; 60/493). Principal Coordinate analysis separated SSU sequences into three major groups (G1-G3), each represented by sequences from North American and European cricetids. A maximum likelihood tree of SSU sequences had low bootstrap support and showed G1 to be more heterogeneous than G2 or G3. Actin and concatenated actin-SSU trees, which were better resolved and had higher bootstrap support than the SSU phylogeny, showed that closely related cricetid hosts in Europe and North America are infected with closely related Cryptosporidium genotypes. Cricetids were not major reservoirs of human pathogenic Cryptosporidium spp.

Centers for Disease Control and Prevention Atlanta GA USA

Department of Biological Sciences North Dakota State University Fargo ND USA

Department of Infectious Disease and Global Health Tufts University Cummings School of Veterinary Medicine North Grafton MA USA

Department of Microbiological Sciences North Dakota State University Fargo ND USA

Environmental and Conservation Sciences Program North Dakota State University Fargo ND USA

Institute of Parasitology Biology Centre of Czech Academy of Sciences České Budějovice Czech Republic

Slovak Academy of Sciences Košice Slovakia

Zobrazit více v PubMed

Bonhomme F and Searle JB (2012). House mouse phylogeography In Evolution of the House Mouse (ed. Macholán M, Baird SJE, Munclinger P. and Piálek J.), pp. 278–296. Cambridge University Press, Cambridge.

Bowker LS and Pearson PG (1975). Habitat orientation and interspecific interaction of Microtus pennsylvanicus and Peromyscus leucopus. American Midland Naturalist 94, 491–496.

Brunner JL, Duerr S, Keesing F, Killilea M, Vuong H. and Ostfeld RS (2013). An experimental test of competition among mice, chipmunks, and squirrels in deciduous forest fragments. PLoS ONE 8, 9. PubMed PMC

Chalmers RM, Smith R, Elwin K, Clifton-Hadley FA and Giles M. (2011). Epidemiology of anthroponotic and zoonotic human cryptosporidiosis in England and Wales, 2004–2006. Epidemiology and Infection 139, 700–712. PubMed

Checkley W, White AC Jr, Jaganath D, Arrowood MJ,Chalmers RM, Chen XM, Fayer R, Griffiths JK, Guerrant RL, Hedstrom L, Huston CD, Kotloff KL, Kang G, Mead JR, Miller M, Petri WA Jr, Priest JW, Roos DS, Striepen B, Thompson RC, Ward HD, Van Voorhis WA, Xiao L, Zhu G. and Houpt ER (2015). A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for Cryptosporidium. Lancet Infectious Diseases 15, 85–94. PubMed PMC

Cieloszyk J, Goñi P, García A, Remacha MA, Sánchez E. and Clavel A. (2012). Two cases of zoonotic cryptosporidiosis in Spain by the unusual species Cryptosporidium ubiquitum and Cryptosporidium felis. Enfermedades Infecciosas y Microbiología Clínica 30, 549–551. PubMed

Clarke KR (1993). Nonparametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117–143.

Conroy CJ and Cook JA (1999). MtDNA evidence for repeated pulses of speciation within arvicoline and murid rodents. Journal of Mammalian Evolution 6, 221–245.

Cook JA, Runck AM and Conroy CJ (2004). Historical biogeography at the crossroads of the northern continents: molecular phylogenetics of red-backed voles (Rodentia: Arvicolinae). Molecular Phylogenetics and Evolution 30, 767–777. PubMed

Fayer R. (2010). Taxonomy and species delimitation in Cryptosporidium. Experimental Parasitology 124, 90–97. PubMed

Feltus DC, Giddings CW, Schneck BL, Monson T, Warshauer D. and McEvoy JM (2006). Evidence supporting zoonotic transmission of Cryptosporidium spp. in Wisconsin. Journal of Clinical Microbiology 44, 4303–4308. PubMed PMC

Feng Y, Alderisio KA, Yang W, Blancero LA, Kuhne WG, Nadareski CA, Reid M. and Xiao L. (2007). Cryptosporidium genotypes in wildlife from a New York watershed. Applied and Environmental Microbiology 73, 6475–6483. PubMed PMC

Hasegawa M, Kishino H. and Yano TA (1985). Dating of the human ape splitting by a molecular clock of mitochondrial-DNA. Journal of Molecular Evolution 22, 160–174. PubMed

Holubová N, Sak B, Horčičková M, Hlásková L, Květoñová D, Menchaca S, McEvoy J. and Kváč M. (2016). Cryptosporidium avium n. sp. (Apicomplexa: Cryptosporidiidae) in birds. Parasitology Research 115, 2243–2251. PubMed PMC

Ikarashi M, Fukuda Y, Honma H, Kasai K, Kaneta Y. and Nakai Y. (2013). First description of heterogeneity in 18S rRNA genes in the haploid genome of Cryptosporidium andersoni Kawatabi type. Veterinary Parasitology 196, 220–224. PubMed

Ježková J, Horčičková M, Hlásková L, Sak B, Květoňová D, Novák J, Hofmannová L, McEvoy J. and Kváč M. (2016). Cryptosporidium testudinis sp. n., Cryptosporidium ducismarci Traversa, 2010 and Cryptosporidium tortoise genotype III (Apicomplexa: Cryptosporidiidae) in tortoises. Folia Parasitologica 63, 035. doi: 10.14411/fp.2016.035. PubMed DOI

Katoh K. and Standley DM (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780. PubMed PMC

Kimura A, Edagawa A, Okada K, Takimoto A, Yonesho S. and Karanis P. (2007). Detection and genotyping of Cryptosporidium from brown rats (Rattus norvegicus) captured in an urban area of Japan. Parasitology Research 100, 1417–1420. PubMed

Kváč M, McEvoy J, Loudová M, Stenger B, Sak B, Kvétoňová D, Ditrich O, Rašková V, Moriarty E, Rost M, Macholán M. and Piálek J. (2013). Coevolution of Cryptosporidium tyzzeri and the house mouse (Mus musculus). International Journal for Parasitology 43, 805–817. PubMed PMC

Kváč M, McEvoy J, Stenger B. and Clark M. (2014). Cryptosporidiosis in other vertebrates In Cryptosporidium: Parasite and Disease (ed. Cacciò SM and Widmer G.), pp. 237–323. Springer; Vienna, Vienna, Austria.

Kváč M, Havrdová N, Hlásková L, Daňková T, Kanděra J, Ježková J, Vítovec J, Sak B, Ortega Y, Xiao L, Modrý D, Chelladurai JR, Prantlová V. and McEvoy J. (2016). Cryptosporidium proliferans n. sp. (Apicomplexa: Cryptosporidiidae): molecular and biological evidence of cryptic species within gastric Cryptosporidium of mammals. PloS ONE 11, e0147090. PubMed PMC

Le Blancq SM, Khramtsov NV, Zamani F, Upton SJ and Wu TW (1997). Ribosomal RNA gene organization in Cryptosporidium parvum. Molecular and Biochemical Parasitology 90, 463–478. PubMed

Li N, Xiao L, Alderisio K, Elwin K, Cebelinski E, Chalmers R, Santín M, Fayer R, Kváč M, Ryan U, Sak B, Stanko M, Guo Y, Wang L, Zhang L, Cai J, Roellig D. and Feng Y. (2014). Subtyping Cryptosporidium ubiquitum, a zoonotic pathogen emerging in humans. Emerging Infectious Diseases 20, 217–224. PubMed PMC

Lv C, Zhang L, Wang R, Jian F, Zhang S, Ning C, Wang H, Feng C, Wang X, Ren X, Qi M. and Xiao L. (2009). Cryptosporidium spp. in wild, laboratory, and pet rodents in China: prevalence and molecular characterization. Applied and Environment Microbiology 75, 7692–7699. PubMed PMC

Martin RA (2003). Biochronology of latest Miocene through Pleistocene arvicolid rodents from the Central Great Plains of North America. Coloquios de Paleontologia 1, 373–383.

McLauchlin J, Casemore DP, Moran S. and Patel S. (1998). The epidemiology of cryptosporidiosis: application of experimental subtyping and antibody detection systems to the investigation of water-borne outbreaks. Folia Parasitologica 45, 83–92. PubMed

Morgan UM, Monis PT, Xiao L, Limor J, Sulaiman I, Raidal S, O’Donoghue P, Gasser R, Murray A, Fayer R, Blagburn BL, Lal AA and Thompson RC (2001). Molecular and phylogenetic characterisation of Cryptosporidium from birds. International Journal for Parasitology 31, 289–296. PubMed

Ng-Hublin JS, Singleton GR and Ryan U. (2013). Molecular characterization of Cryptosporidium spp. from wild rats and mice from rural communities in the Philippines. Infection, Genetics and Evolution 16, 5–12. PubMed

Nichols GL, McLauchlin J. and Samuel D. (1991). A technique for typing Cryptosporidium isolates. Journal of Protozoology 38, 237S–240S. PubMed

Nina JM, McDonald V, Deer RM, Wright SE, Dyson DA, Chiodini PL and McAdam KP (1992). Comparative study of the antigenic composition of oocyst isolates of Cryptosporidium parvum from different hosts. Parasite Immunology 14, 227–232. PubMed

Ogunkolade BW, Robinson HA, McDonald V, Webster K. and Evans DA (1993). Isoenzyme variation within the genus Cryptosporidium. Parasitology Research 79, 385–388. PubMed

Paparini A, Jackson B, Ward S, Young S. and Ryan UM (2012). Multiple Cryptosporidium genotypes detected in wild black rats (Rattus rattus) from northern Australia. Experimental Parasitology 131, 404–412. PubMed

Peakall R. and Smouse PE (2012). Genalex 6·5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28, 2537–2539. PubMed PMC

Peng MM, Wilson ML, Holland RE, Meshnick SR, Lal AA and Xiao L. (2003). Genetic diversity of Cryptosporidium spp. in cattle in Michigan: implications for understanding the transmission dynamics. Parasitology Research 90, 175–180. PubMed

Perz JF and Le Blancq SM (2001). Cryptosporidium parvum infection involving novel genotypes in wildlife from lower New York State. Applied and Environmental Microbiology 67, 1154–1162. PubMed PMC

R Core Team (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

Robinson G, Chalmers RM, Stapleton C, Palmer SR, Watkins J, Francis C. and Kay D. (2011). A whole water catchment approach to investigating the origin and distribution of Cryptosporidium species. Journal of Applied Microbiology 111, 717–730. PubMed

Robinson M, Catzeflis F, Briolay J. and Mouchiroud D. (1997). Molecular phylogeny of rodents, with special emphasis on murids: evidence from nuclear gene LCAT. Molecular Phylogenetics and Evolution 8, 423–434. PubMed

Ruecker NJ, Braithwaite SL, Topp E, Edge T, Lapen DR, Wilkes G, Robertson W, Medeiros D, Sensen CW and Neumann NF (2007). Tracking host sources of Cryptosporidium spp. in raw water for improved health risk assessment. Applied and Environment Microbiology 73, 3945–3957. PubMed PMC

Ruecker NJ, Matsune JC, Wilkes G, Lapen DR, Topp E, Edge TA, Sensen CW, Xiao L. and Neumann NF (2012). Molecular and phylogenetic approaches for assessing sources of Cryptosporidium contamination in water. Water Research 46, 5135–5150. PubMed

Ryan U. (2010). Cryptosporidium in birds, fish and amphibians. Experimental Parasitology 124, 113–120. PubMed

Ryan U, Fayer R. and Xiao L. (2014). Cryptosporidium species in humans and animals: current understanding and research needs. Parasitology 141, 1667–1685. PubMed

Saitou N. and Nei M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425. PubMed

Santín M. and Fayer R. (2007). Intragenotypic variations in the Cryptosporidium sp. cervine genotype from sheep with implications for public health. Journal of Parasitology 93, 668–672. PubMed

Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ and Weber CF (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environment Microbiology 75, 7537–7541. PubMed PMC

Sevá Ada P, Funada MR, Richtzenhain L, Guimarães MB, Souza S. e. O., Allegretti L, Sinhorini JA, Duarte VV and Soares RM (2011). Genotyping of Cryptosporidium spp. from free-living wild birds from Brazil. Veterinary Parasitology 175, 27–32. PubMed

Stenger BL, Clark ME, Kváč M, Khan E, Giddings CW, Dyer NW, Schultz JL and McEvoy JM (2015a). Highly divergent 18S rRNA gene paralogs in a Cryptosporidium genotype from eastern chipmunks (Tamias striatus). Infection, Genetics and Evolution 32, 113–123. PubMed PMC

Stenger BL, Clark ME, Kváč M, Khan E, Giddings CW, Prediger J. and McEvoy JM (2015b). North American tree squirrels and ground squirrels with overlapping ranges host different Cryptosporidium species and genotypes. Infection, Genetics and Evolution 36, 287–293. PubMed

Steppan S, Adkins R. and Anderson J. (2004). Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Systematic Biology 53, 533–553. PubMed

Sulaiman IM, Lal AA and Xiao L. (2002). Molecular phylogeny and evolutionary relationships of Cryptosporidium parasites at the actin locus. Journal of Parasitology 88, 388–394. PubMed

Tamura K, Stecher G, Peterson D, Filipski A. and Kumar S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729. PubMed PMC

Tavaré S. (1986). Some probabilistic and statistical problems in the analysis of DNA sequences In Some Mathematical Questions in Biology: DNA Sequence Analysis (Lectures on Mathematics in the Life Sciences) (ed. Miura RM), pp. 57–86. American Mathematical Society, New York.

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

Wilson DE and Reeder DM (2005). Mammal Species of the World A Taxonomic and Geographic Reference. p. 2142 Johns Hopkins University Press, Baltimore, Maryland.

Xiao L, Limor JR, Li L, Morgan U, Thompson RC and Lal AA (1999). Presence of heterogeneous copies of the small subunit rRNA gene in Cryptosporidium parvum human and marsupial genotypes and Cryptosporidium felis. Journal of Eukaryotic Microbiology 46, 44S–45S. PubMed

Xiao L, Singh A, Limor J, Graczyk TK, Gradus S. and Lal A. (2001). Molecular characterization of Cryptosporidium oocysts in samples of raw surface water and wastewater. Applied and Environmental Microbiology 67, 1097–1101. PubMed PMC

Xiao L, Sulaiman IM, Ryan UM, Zhou L, Atwill ER, Tischler ML, Zhang X, Fayer R. and Lal AA (2002). Host adaptation and host-parasite co-evolution in Cryptosporidium: implications for taxonomy and public health. International Journal for Parasitology 32, 1773–1785. PubMed

Zhao Z, Wang R, Zhao W, Qi M, Zhao J, Zhang L, Li J. and Liu A. (2015). Genotyping and subtyping of Giardia and Cryptosporidium isolates from commensal rodents in China. Parasitology 142, 800–806. PubMed

Zhou L, Fayer R, Trout JM, Ryan UM, Schaefer FW III and Xiao L. (2004). Genotypes of Cryptosporidium species infecting fur-bearing mammals differ from those of species infecting humans. Applied and Environmental Microbiology 70, 7574–7577. PubMed PMC

Ziegler PE, Wade SE, Schaaf SL, Chang YF and Mohammed HO (2007). Cryptosporidium spp. from small mammals in the New York City watershed. Journal of Wildlife Diseases 43, 586–596. PubMed

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

Cryptosporidium sciurinum n. sp. (Apicomplexa: Cryptosporidiidae) in Eurasian Red Squirrels (Sciurus vulgaris)

Cryptosporidium myocastoris n. sp. (Apicomplexa: Cryptosporidiidae), the Species Adapted to the Nutria (Myocastor coypus)

Cryptosporidium ratti n. sp. (Apicomplexa: Cryptosporidiidae) and genetic diversity of Cryptosporidium spp. in brown rats (Rattus norvegicus) in the Czech Republic

Diversity of Cryptosporidium in common voles and description of Cryptosporidium alticolis sp. n. and Cryptosporidium microti sp. n. (Apicomplexa: Cryptosporidiidae)