Abstract
Enterocytozoon bieneusi is an obligate intracellular protozoan parasite that infects a wide range of mammal hosts and birds. Previous genotypic surveys were limited to measure the polymorphisms at the ribosomal internal transcribed spacer (ITS) that evolved slowly. Data on population structure are available only on E. bieneusi isolates from primates. This study explored the genotypic and phylogenetic characteristics of four mini- and microsatellites and performed a population genetic analysis in 39 E. bieneusi isolates of potentially zoonotic ITS genotype D from farmed foxes and raccoon dogs in China. Sequence polymorphisms facilitated determination of six, two, four, and five genotypes at markers MS1, MS3, MS4, and MS7, respectively. Patterns of phylogeny revealed different levels of diversity within and among the genetic markers. Clear genotypic and phylogenetic divergences between E. bieneusi isolates of ITS genotype D from fur animals and humans were observed at individual markers. Complete linkage disequilibrium and very limited recombination in subsequent population genetic analysis supported a clonal structure for E. bieneusi population from fur animals (FID). Phylogenetic analysis, genetic network, and measures of F ST and gene flow demonstrated population differentiation of FID from two known human E. bieneusi populations HID (with a clonal structure) and HIA (with an epidemic structure). The data indicated an ideal resolving power of MLST compared to the previously widely used ITS genotyping and confirmed the clonal nature and population differentiation of E. bieneusi in various hosts.
References
Fayer R, Santin M, Macarisin D (2012) Detection of concurrent infection of dairy cattle with Blastocystis, Cryptosporidium, Giardia, and Enterocytozoon by molecular and microscopic methods. Parasitol Res 111(3):1349–1355
Feng Y et al (2011) Development of a multilocus sequence typing tool for high-resolution genotyping of Enterocytozoon bieneusi. Appl Environ Microbiol 77(14):4822–4828
Fiuza VR, Oliveira FC, Fayer R, Santin M (2015) First report of Enterocytozoon bieneusi in pigs in Brazil. Parasitol Int 64(4):18–23
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147(2):915–925
Guo Y, Alderisio KA, Yang W, Cama V, Feng Y, Xiao L (2014) Host specificity and source of Enterocytozoon bieneusi genotypes in a drinking source watershed. Appl Environ Microbiol 80(1):218–225
Heitman J (2006) Sexual reproduction and the evolution of microbial pathogens. Curr Biol 16(17):R711–725
Jeong DK et al (2007) Occurrence and genotypic characteristics of Enterocytozoon bieneusi in pigs with diarrhea. Parasitol Res 102(1):123–128
Jiang Y et al (2015) Zoonotic and potentially host-adapted Enterocytozoon bieneusi genotypes in sheep and cattle in northeast China and an increasing concern about the zoonotic importance of previously considered ruminant-adapted genotypes. Appl Environ Microbiol 81(10):3326–3335
Karim MR et al (2014) Multilocus sequence typing of Enterocytozoon bieneusi in nonhuman primates in China. Vet Parasitol 200(1–2):13–23
Keeling P (2009) Five questions about microsporidia. PLoS Pathog 5(9):e1000489
Li W et al (2013) Multilocus sequence typing of Enterocytozoon bieneusi: lack of geographic segregation and existence of genetically isolated sub-populations. Infect Genet Evol 14:111–119
Li W et al (2012) Population genetic analysis of Enterocytozoon bieneusi in humans. Int J Parasitol 42(3):287–293
Li W et al (2015) Prevalence and genetic characteristics of Cryptosporidium, Enterocytozoon bieneusi and Giardia duodenalis in cats and dogs in Heilongjiang province, China. Vet Parasitol 208(3–4):125–134
Matos O, Lobo ML, Xiao L (2012) Epidemiology of Enterocytozoon bieneusi infection in humans. J Parasitol Res 2012:981424
Santin M, Fayer R (2011) Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Res Vet Sci 90(3):363–371
Slodkowicz-Kowalska A, Graczyk TK, Tamang L, Girouard AS, Majewska AC (2007) Asymptomatic Enterocytozoon bieneusi microsporidiosis in captive mammals. Parasitol Res 100(3):505–509
Thellier M, Breton J (2008) Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite 15(3):349–358
Valencakova A et al (2012) Molecular identification and genotyping of Microsporidia in selected hosts. Parasitol Res 110(2):689–693
Widmer G, Akiyoshi DE (2010) Host-specific segregation of ribosomal nucleotide sequence diversity in the microsporidian Enterocytozoon bieneusi. Infect Genet Evol 10(1):122–128
Yang Y et al (2015) Widespread presence of human-pathogenic Enterocytozoon bieneusi genotype D in farmed foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in China: first identification and zoonotic concern. Parasitol Res 114(11):4341–4348
Acknowledgements
This study was supported by the Young Talents’ Project of Northeast Agricultural University (no. 14QC19) and the University Nursing Program for Young Scholars with Creative Talents in Heilongjiang Province (no. UNPYSCT-2015008).
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Li, W., Wan, Q., Yu, Q. et al. Genetic variation of mini- and microsatellites and a clonal structure in Enterocytozoon bieneusi population in foxes and raccoon dogs and population differentiation of the parasite between fur animals and humans. Parasitol Res 115, 2899–2904 (2016). https://doi.org/10.1007/s00436-016-5069-3
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DOI: https://doi.org/10.1007/s00436-016-5069-3