Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T08:20:58.077Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  17 July 2018

Michaela Horčičková ,
Šárka Čondlová ,
Nikola Holubová ,
Bohumil Sak ,
Dana Květoňová ,
Lenka Hlásková ,
Roman Konečný ,
František Sedláček ,
Mark Clark  and
Catherine Giddings
...Show all authors
Michaela Horčičková
Affiliation:
Faculty of Agriculture, University of South Bohemia in České Budějovice, Czech Republic Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, České Budějovice, Czech Republic
Šárka Čondlová
Affiliation:
Faculty of Agriculture, University of South Bohemia in České Budějovice, Czech Republic Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, České Budějovice, Czech Republic
Nikola Holubová
Affiliation:
Faculty of Agriculture, University of South Bohemia in České Budějovice, Czech Republic Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, České Budějovice, Czech Republic
Bohumil Sak
Affiliation:
Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, České Budějovice, Czech Republic
Dana Květoňová
Affiliation:
Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, České Budějovice, Czech Republic
Lenka Hlásková
Affiliation:
Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, České Budějovice, Czech Republic
Roman Konečný
Affiliation:
Faculty of Agriculture, University of South Bohemia in České Budějovice, Czech Republic
František Sedláček
Affiliation:
Faculty of Science, University of South Bohemia in České Budějovice, Czech Republic
Mark Clark
Affiliation:
Biological Sciences Department, North Dakota State University, Fargo, USA
Catherine Giddings
Affiliation:
Microbiological Sciences Department, North Dakota State University, Fargo, USA
John McEvoy
Affiliation:
Microbiological Sciences Department, North Dakota State University, Fargo, USA
Martin Kváč*
Affiliation:
Faculty of Agriculture, University of South Bohemia in České Budějovice, Czech Republic Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, České Budějovice, Czech Republic
*
Author for correspondence: M. Kváč, E-mail: kvac@paru.cas.cz
Get access Rights & Permissions [Opens in a new window]

Abstract

Fecal samples from wild-caught common voles (n = 328) from 16 locations in the Czech Republic were screened for Cryptosporidium by microscopy and PCR/sequencing at loci coding small-subunit rRNA, Cryptosporidium oocyst wall protein, actin and 70 kDa heat shock protein. Cryptosporidium infections were detected in 74 voles (22.6%). Rates of infection did not differ between males and females nor between juveniles and adults. Phylogenetic analysis revealed the presence of eight Cryptosporidium species/genotypes including two new species, C. alticolis and C. microti. These species from wild-caught common voles were able to infect common and meadow voles under experimental conditions, with a prepatent period of 3–5 days post-infection (DPI), but they were not infectious for various other rodents or chickens. Meadow voles lost infection earlier than common voles (11–14 vs 13–16 DPI) and had significantly lower infection intensity. Cryptosporidium alticolis infects the anterior small intestine and has larger oocysts (5.4 × 4.9 µm), whereas C. microti infects the large intestine and has smaller oocysts (4.3 × 4.1 µm). None of the rodents developed clinical signs of infection. Genetic and biological data support the establishment of C. alticolis and C. microti as separate species of the genus Cryptosporidium.

Keywords

Experimental infectionmolecular analysesoocyst sizephylogenyRodentiavoles
Type
Research Article
Information
Parasitology , Volume 146 , Issue 2 , February 2019 , pp. 220 - 233
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

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.)

References

Arrowood, MJ and Donaldson, K (1996) Improved purification methods for calf-derived Cryptosporidium parvum oocysts using discontinuous sucrose and caesium chloride gradients. Journal of Eukaryotic Microbiology 43, 89S.Google Scholar
Bajer, A (2008) Cryptosporidium and Giardia spp. infections in humans, animals and the environment in Poland. Parasitology Research 104, 1–17.Google Scholar
Bajer, A, Bednarska, M, Pawelczyk, A, Behnke, JM, Gilbert, FS and Sinski, E (2002) Prevalence and abundance of Cryptosporidium parvum and Giardia spp. in wild rural rodents from the Mazury Lake District region of Poland. Parasitology 125, 21–34.Google Scholar
Bajer, A, Caccio, S, Bednarska, M, Behnke, JM, Pieniazek, NJ and Sinski, E (2003) Preliminary molecular characterization of Cryptosporidium parvum isolates of wildlife rodents from Poland. Journal of Parasitology 89, 1053–1055.Google Scholar
Baneth, G, Thamsborg, SM, Otranto, D, Guillot, J, Blaga, R, Deplazes, P and Solano-Gallego, L (2016) Major parasitic zoonoses associated with dogs and cats in Europe. Journal of Comparative Pathology 155, S54–S74.Google Scholar
Bednarska, M, Bajer, A, Sinski, E, Girouard, AS, Tamang, L and Graczyk, TK (2007) Fluorescent in situ hybridization as a tool to retrospectively identify Cryptosporidium parvum and Giardia lamblia in samples from terrestrial mammalian wildlife. Parasitology Research 100, 455–460.Google Scholar
Bull, SA, Chalmers, RM, Sturdee, AP and Healing, TD (1998) A survey of Cryptosporidium species in Skomer bank voles (Clethrionomys glareolus skomerensis). Journal of Zoology 244, 119–122.Google Scholar
Castro-Hermida, JA, García-Presedo, I, González-Warleta, M and Mezo, M (2011) Prevalence of Cryptosporidium and Giardia in roe deer (Capreolus capreolus) and wild boars (Sus scrofa) in Galicia (NW, Spain). Veterinary Parasitology 179, 216–219.Google Scholar
Chalmers, RM, Sturdee, AP, Bull, SA, Miller, A and Wright, SE (1997) The prevalence of Cryptosporidium parvum and C. muris in Mus domesticus, Apodemus sylvaticus and Clethrionomys glareolus in an agricultural system. Parasitology Research 83, 478–482.Google Scholar
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. The Lancet Infectious Diseases 15, 85–94.Google Scholar
Čondlová, S, Horčičková, M, Sak, B, Květoňová, D, Hlásková, L, Konečný, R, Stanko, M, McEvoy, J and Kváč, M (2018) Cryptosporidium apodemi sp. n. and Cryptosporidium ditrichi sp. n. (Apicomplexa: Cryptosporidiidae) in Apodemus spp. European Journal of Protistology 63, 1–12.Google Scholar
Danišová, O, Valenčáková, A, Stanko, M, Luptaková, L, Hatalová, E and Canady, A (2017) Rodents as a reservoir of infection caused by multiple zoonotic species/genotypes of C. parvum, C. hominis, C. suis, C. scrofarum, and the first evidence of C. muskrat genotypes I and II of rodents in Europe. Acta Tropica 172, 29–35.Google Scholar
Fayer, R (2010) Taxonomy and species delimitation in Cryptosporidium. Experimental Parasitology 124, 90–97.Google Scholar
Feng, Y (2010) Cryptosporidium in wild placental mammals. Experimental Parasitology 124, 128–137.Google Scholar
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.Google Scholar
Foo, C, Farrell, J, Boxell, A, Robertson, I and Ryan, UM (2007) Novel Cryptosporidium genotype in wild Australian mice (Mus domesticus). Applied and Environmental Microbiology 73, 7693–7696.Google Scholar
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.Google Scholar
Hajdušek, O, Ditrich, O and Šlapeta, J (2004) Molecular identification of Cryptosporidium spp. in animal and human hosts from the Czech Republic. Veterinary Parasitology 122, 183–192.Google Scholar
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
Hikosaka, K and Nakai, Y (2005) A novel genotype of Cryptosporidium muris from large Japanese field mice, Apodemus speciosus. Parasitology Research 97, 373–379.Google Scholar
Jeníková, M, Němejc, K, Sak, B, Květoňová, D and Kváč, M (2011) New view on the age-specificity of pig Cryptosporidium by species-specific primers for distinguishing Cryptosporidium suis and Cryptosporidium pig genotype II. Veterinary Parasitology 176, 120–125.Google Scholar
Jiang, J, Alderisio, KA and Xiao, L (2005) Distribution of Cryptosporidium genotypes in storm event water samples from three watersheds in New York. Applied and Environmental Microbiology 71, 4446–4454.Google Scholar
Jirků, M, Valigurová, A, Koudela, B, Křížek, J, Modrý, D and Šlapeta, J (2008) New species of Cryptosporidium tyzzer, 1907 (Apicomplexa) from amphibian host: morphology, biology and phylogeny. Folia Parasitologica (Praha) 55, 81–94.Google Scholar
Kváč, M, Ondráčková, Z, Květoňová, D, Sak, B and Vítovec, J (2007) Infectivity and pathogenicity of Cryptosporidium andersoni to a novel host, southern multimammate mouse (Mastomys coucha). Veterinary Parasitology 143, 229–233.Google Scholar
Kváč, M, Hofmannová, L, Bertolino, S, Wauters, L, Tosi, G and Modrý, D (2008) Natural infection with two genotypes of Cryptosporidium in red squirrels (Sciurus vulgaris) in Italy. Folia Parasitologica 55, 95–99.Google Scholar
Kváč, M, McEvoy, J, Loudová, M, Stenger, B, Sak, B, Květoňová, 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.Google Scholar
Kváč, M, McEvoy, J, Stenger, B and Clark, M (2014) Cryptosporidiosis in other vertebrates. In Cacciò, SM and Widmer, G (eds), Cryptosporidium: Parasite and Disease. Wien: Springer, pp. 237–326.Google Scholar
Kváč, M, Vlnatá, G, Ježková, J, Horčičková, M, Konečný, R, Hlásková, L, McEvoy, J and Sak, B (2018) Cryptosporidium occultus sp. n. (Apicomplexa: Cryptosporidiidae) in rats. European Journal of Protistology 63, 96–104.Google Scholar
Laakkonen, J, Soveri, T and Henttonen, H (1994) Prevalence of Cryptosporidium sp. in peak density Microtus agrestis, Microtus oeconomus and Clethrionomys glareolus populations. Journal of Wildlife Diseases 30, 110–111.Google Scholar
Li, N, Xiao, L, Alderisio, K, Elwin, K, Cebelinski, E, Chalmers, R, Santin, 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.Google Scholar
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 Environmental Microbiology 75, 7692–7699.Google Scholar
Ma, JB, Cai, JZ, Ma, JW, Feng, YY and Xiao, LH (2014) Occurrence and molecular characterization of Cryptosporidium spp. in yaks (Bos grunniens) in China. Veterinary Parasitology 202, 113–118.Google Scholar
Miláček, P and Vítovec, J (1985) Differential staining of cryptosporidia by aniline-carbol-methyl violet and tartrazine in smears from feces and scrapings of intestinal mucosa. Folia Parasitologica 32, 50.Google Scholar
Modrý, D, Hofmannová, L, Antalová, Z, Sak, B and Kváč, M (2012) Variability in susceptibility of voles (Arvicolinae) to experimental infection with Cryptosporidium muris and Cryptosporidium andersoni. Parasitology Research 111, 471–473.Google Scholar
Němejc, K, Sak, B, Květoňová, D, Hanzal, V, Jeníková, M and Kváč, M (2012) The first report on Cryptosporidium suis and Cryptosporidium pig genotype II in Eurasian wild boars (Sus scrofa) (Czech Republic). Veterinary Parasitology 184, 122–125.Google Scholar
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.Google Scholar
Nichols, GL, Chalmers, RM and Hadfield, SJ (2014) Molecular epidemiology of human cryptosporidiosis. In Cacciò, SM and Widmer, G (eds), Cryptosporidium: Parasite and Disease. Wien: Springer, pp. 237–326.Google Scholar
Perec-Matysiak, A, Bunkowska-Gawlik, K, Zalesny, G and Hildebrand, J (2015) Small rodents as reservoirs of Cryptosporidium spp. and Giardia spp. in south-western Poland. Annals of Agricultural and Environmental Medicine 22, 1–5.Google Scholar
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.Google Scholar
Qi, M, Wang, H, Jing, B, Wang, D, Wang, R and Zhang, L (2015) Occurrence and molecular identification of Cryptosporidium spp. in dairy calves in Xinjiang, Northwestern China. Veterinary Parasitology 212, 404–407.Google Scholar
Rašková, V, Květoňová, D, Sak, B, McEvoy, J, Edwinson, A, Stenger, B and Kváč, M (2013) Human cryptosporidiosis caused by Cryptosporidium tyzzeri and C. parvum isolates presumably transmitted from wild mice. Journal of Clinical Microbiology 51, 360–362.Google Scholar
Ryan, U and Xiao, L (2014). Taxonomy and molecular taxonomy. In Cacciò, SM and Widmer, G (eds), Cryptosporidium: Parasite and Disease. Wien: Springer, pp. 3–42.Google Scholar
Ryan, UM, Monis, P, Enemark, HL, Sulaiman, I, Samarasinghe, B, Read, C, Buddle, R, Robertson, I, Zhou, L, Thompson, RCA and Xiao, L (2004) Cryptosporidium suis n. sp (Apicomplexa: Cryptosporidiidae) in pigs (Sus scrofa). Journal of Parasitology 90, 769–773.Google Scholar
Santín, M and Zarlenga, DS (2009) A multiplex polymerase chain reaction assay to simultaneously distinguish Cryptosporidium species of veterinary and public health concern in cattle. Veterinary Parasitology 166, 32–37.Google Scholar
Sinski, E, Hlebowicz, E and Bednarska, M (1993) Occurrence of Cryptosporidium parvum infection in wild small mammals in District of Mazury Lake (Poland). Acta Parasitologica 38, 59–61.Google Scholar
Sinski, E, Bednarska, M and Bajer, A (1998) The role of wild rodents in ecology of cryptosporidiosis in Poland. Folia Parasitologica 45, 173–174.Google Scholar
Spano, F, Putignani, L, McLauchlin, J, Casemore, DP and Crisanti, A (1997) PCR-RFLP analysis of the Cryptosporidium oocyst wall protein (COWP) gene discriminates between C. wrairi and C. parvum, and between C. parvum isolates of human and animal origin. FEMS Microbiology Letters 150, 209–217.Google Scholar
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.Google Scholar
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.Google Scholar
Stenger, BLS, Horčičková, M, Clark, ME, Kváč, M, Čondlová, S, Khan, E, Widmer, G, Xiao, L, Giddings, CW, Pennil, C, Stanko, M, Sak, B and McEvoy, JM (2018) Cryptosporidium infecting wild cricetid rodents from the subfamilies Arvicolinae and Neotominae. Parasitology 145, 326–334.Google Scholar
Sturdee, AP, Chalmers, RM and Bull, SA (1999) Detection of Cryptosporidium oocysts in wild mammals of mainland Britain. Veterinary Parasitology 80, 273–280.Google Scholar
Sulaiman, IM, Morgan, UM, Thompson, RC, Lal, AA and Xiao, L (2000) Phylogenetic relationships of Cryptosporidium parasites based on the 70-kilodalton heat shock protein (HSP70) gene. Applied and Environmental Microbiology 66, 2385–2391.Google Scholar
Sulaiman, IM, Lal, AA and Xiao, LH (2002) Molecular phylogeny and evolutionary relationships of Cryptosporidium parasites at the actin locus. Journal of Parasitology 88, 388–394.Google Scholar
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.Google Scholar
Torres, J, Gracenea, M, Gomez, MS, Arrizabalaga, A and Gonzalez-Moreno, O (2000) The occurrence of Cryptosporidium parvum and C. muris in wild rodents and insectivores in Spain. Veterinary Parasitology 92, 253–260.Google Scholar
Vítovec, J, Hamadejová, K, Landová, L, Kváč, M, Květoňová, D and Sak, B (2006) Prevalence and pathogenicity of Cryptosporidium suis in pre- and post-weaned pigs. Journal of Veterinary Medicine B 53, 239–243.Google Scholar
Xiao, L, Escalante, L, Yang, C, Sulaiman, I, Escalante, AA, Montali, RJ, Fayer, R and Lal, AA (1999) Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Applied and Environmental Microbiology 65, 1578–1583.Google Scholar
Xiao, L, Fayer, R, Ryan, U and Upton, SJ (2004) Cryptosporidium taxonomy: recent advances and implications for public health. Clinical Microbiology Reviews 17, 72–97.Google Scholar
Zhou, L, Fayer, R, Trout, JM, Ryan, UM, Schaefer, FW 3rd 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.Google Scholar
Ziegler, PE, Wade, SE, Schaaf, SL, Chang, YF and Mohammed, HO (2007 a) Cryptosporidium spp. from small mammals in the New York City watershed. Journal of Wildlife Diseases 43, 586–596.Google Scholar
Ziegler, PE, Wade, SE, Schaaf, SL, Stern, DA, Nadareski, CA and Mohammed, HO (2007 b) Prevalence of Cryptosporidium species in wildlife populations within a watershed landscape in southeastern New York State. Veterinary Parasitology, 147, 176–184.Google Scholar
Supplementary material: PDF

Horčičková et al. supplementary material

Table S1

Download Horčičková et al. supplementary material(PDF)
PDF 199.1 KB
Supplementary material: PDF

Horčičková et al. supplementary material

Figure S1

Download Horčičková et al. supplementary material(PDF)
PDF 1.4 MB
Supplementary material: PDF

Horčičková et al. supplementary material

Figure S2

Download Horčičková et al. supplementary material(PDF)
PDF 1.4 MB
Supplementary material: PDF

Horčičková et al. supplementary material

Figure S3

Download Horčičková et al. supplementary material(PDF)
PDF 1.4 MB
Supplementary material: PDF

Horčičková et al. supplementary material

Figure S4

Download Horčičková et al. supplementary material(PDF)
PDF 1.4 MB