Population genetic analysis suggests genetic recombination is responsible for increased zoonotic potential of Enterocytozoon bieneusi from ruminants in China

One Health - Tập 11 - Trang 100184 - 2020
Zhenjie Zhang1,2, Jingbo Ma3, Xitong Huang1, Xi Wen1, Wen Jiang4, Li Chen4, Na Li1, Yaqiong Guo1, Longxian Zhang5, Lihua Xiao1,2, Yaoyu Feng1,2
1Center for Emerging and Zoonotic Diseases, College of Veterinary Medicine, South China Agricultural University, Guangzhou, Guangdong 510642, China
2Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, Guangdong, 510642, China
3Department of Parasitology, School of Basic Medical Sciences, Xinxiang Medical University, Xinxiang, Henan 453003, China
4School of Resource and Environmental Engineering, East China University of Science and Technology, Shanghai, 200237, China
5College of Veterinary Medicine, Henan Agricultural University, Zhengzhou, 450002, China

Tài liệu tham khảo

Stentiford, 2019, Ultimate opportunists—the emergent Enterocytozoon group microsporidia, PLoS Pathog., 15, 10.1371/journal.ppat.1007668 Li, 2019, Potential impacts of host specificity on zoonotic or interspecies transmission of Enterocytozoon bieneusi, Infect. Genet. Evol., 75, 104033, 10.1016/j.meegid.2019.104033 Stentiford, 2016, Microsporidia – emergent pathogens in the global food chain, Trends Parasitol., 32, 336, 10.1016/j.pt.2015.12.004 Matos, 2012, Epidemiology of Enterocytozoon bieneusi infection in humans, J. Parasitol. Res., 2012, 981424, 10.1155/2012/981424 Muadica, 2020, First identification of genotypes of Enterocytozoon bieneusi (microsporidia) among symptomatic and asymptomatic children in mozambique, PLoS Negl. Trop. Dis., 14, 10.1371/journal.pntd.0008419 Yu, 2019, Molecular characterization of three intestinal protozoans in hospitalized children with different disease backgrounds in Zhengzhou, central China, Parasit. Vectors, 12, 543, 10.1186/s13071-019-3800-5 Kicia, 2018, Respiratory microsporidiosis caused by Enterocytozoon bieneusi in an HIV-negative hematopoietic stem cell transplant recipient, Int. J. Infect. Dis., 77, 26, 10.1016/j.ijid.2018.07.021 Mirjalali, 2015, Genotyping and molecular analysis of Enterocytozoon bieneusi isolated from immunocompromised patients in Iran, Infect. Genet. Evol., 36, 244, 10.1016/j.meegid.2015.09.022 Velasquez, 2019, Multimethodological approach to gastrointestinal microsporidiosis in HIV-infected patients, Acta Parasitol., 64, 658, 10.2478/s11686-019-00095-z Agholi, 2013, HIV/AIDS-associated opportunistic protozoal diarrhea, AIDS Res. Hum. Retrovir., 29, 35, 10.1089/aid.2012.0119 Lobo, 2012, Microsporidia as emerging pathogens and the implication for public health: a 10-year study on HIV-positive and -negative patients, Int. J. Parasitol., 42, 197, 10.1016/j.ijpara.2011.12.002 Botterel, 2002, Pulmonary localization of Enterocytozoon bieneusi in an AIDS patient: case report and review, J. Clin. Microbiol., 40, 4800, 10.1128/JCM.40.12.4800-4801.2002 Didier, 2011, Microsporidiosis: not just in AIDS patients, Curr. Opin. Infect. Dis., 24, 490, 10.1097/QCO.0b013e32834aa152 Cotte, 1999, Waterborne outbreak of intestinal microsporidiosis in persons with and without human immunodeficiency virus infection, J. Infect. Dis., 180, 2003, 10.1086/315112 Decraene, 2012, First reported foodborne outbreak associated with microsporidia, Sweden, october 2009, Epidemiol. Infect., 140, 519, 10.1017/S095026881100077X Desoubeaux, 2019, Genotyping approach for potential common source of Enterocytozoon bieneusi infection in hematology unit, Emerg. Infect. Dis., 25, 1625, 10.3201/eid2509.190311 Wang, 2013, Concurrent infections of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile in children during a cryptosporidiosis outbreak in a pediatric hospital in China, PLoS Negl. Trop. Dis., 7, 10.1371/journal.pntd.0002437 Santin, 2011, Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals, Res. Vet. Sci., 90, 363, 10.1016/j.rvsc.2010.07.014 Han, 2018, Therapeutic targets for the treatment of microsporidiosis in humans, Expert Opin. Ther. Targets, 22, 903, 10.1080/14728222.2018.1538360 Anane, 2010, Microsporidiosis: epidemiology, clinical data and therapy, Gastroenterol. Clin. Biol., 34, 450, 10.1016/j.gcb.2010.07.003 Li, 2019, Host specificity of Enterocytozoon bieneusi and public health implications, Trends Parasitol., 35, 436, 10.1016/j.pt.2019.04.004 Sulaiman, 2004, Molecular characterization of Enterocytozoon bieneusi in cattle indicates that only some isolates have zoonotic potential, Parasitol. Res., 92, 328, 10.1007/s00436-003-1049-5 Zhang, 2011, Identification and genotyping of Enterocytozoon bieneusi in China, J. Clin. Microbiol., 49, 2006, 10.1128/JCM.00372-11 Du, 2015, Cryptosporidium spp., Giardia intestinalis, and Enterocytozoon bieneusi in captive non-human primates in Qinling Mountains, Korean J. Parasitol., 53, 395, 10.3347/kjp.2015.53.4.395 Karim, 2015, Predomination and new genotypes of Enterocytozoon bieneusi in captive nonhuman primates in zoos in China: high genetic diversity and zoonotic significance, PLoS One, 10, 10.1371/journal.pone.0117991 Karim, 2014, Genetic polymorphism and zoonotic potential of Enterocytozoon bieneusi from nonhuman primates in China, Appl. Environ. Microbiol., 80, 1893, 10.1128/AEM.03845-13 Li, 2016, Multilocus genotypes and broad host-range of Enterocytozoon bieneusi in captive wildlife at zoological gardens in China, Parasit. Vectors, 9, 395, 10.1186/s13071-016-1668-1 Yu, 2017, High prevalence of Enterocytozoon bieneusi zoonotic genotyped in captive golden snub-nosed monkey (rhinopithecus roxellanae) in zoos in China, BMC Vet. Res., 13, 158, 10.1186/s12917-017-1084-6 Sak, 2011, Unapparent microsporidial infection among immunocompetent humans in the Czech Republic, J. Clin. Microbiol., 49, 1064, 10.1128/JCM.01147-10 Feng, 2011, Development of a multilocus sequence typing tool for high-resolution genotyping of Enterocytozoon bieneusi, Appl. Environ. Microbiol., 77, 4822, 10.1128/AEM.02803-10 Li, 2019, Multilocus typing of Enterocytozoon bieneusi in pig reveals the high prevalence, zoonotic potential, host adaptation and geographical segregation in China, J. Eukaryot. Microbiol., 10.1111/jeu.12715 Li, 2013, Multilocus sequence typing of Enterocytozoon bieneusi: lack of geographic segregation and existence of genetically isolated sub-populations, Infect. Genet. Evol., 14, 111, 10.1016/j.meegid.2012.11.021 Li, 2012, Population genetic analysis of Enterocytozoon bieneusi in humans, Int. J. Parasitol., 42, 287, 10.1016/j.ijpara.2012.01.003 Li, 2016, 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, 10.1007/s00436-016-5069-3 Wan, 2016, Clonal evolution of Enterocytozoon bieneusi populations in swine and genetic differentiation in subpopulations between isolates from swine and humans, PLoS Negl. Trop. Dis., 10, 10.1371/journal.pntd.0004966 Wang, 2019, Prevalence and population genetics analysis of Enterocytozoon bieneusi in dairy cattle in China, Front. Microbiol., 10, 1399, 10.3389/fmicb.2019.01399 Wang, 2016, Multilocus genotyping of Giardia duodenalis and Enterocytozoon bieneusi in dairy and native beef (Qinchuan) calves in Shaanxi province, Northwestern China, Parasitol. Res., 115, 1355, 10.1007/s00436-016-4908-6 Li, 2019, Multilocus sequence typing and population genetic analysis of Enterocytozoon bieneusi: host specificity and its impacts on public health, Front. Genet., 10, 307, 10.3389/fgene.2019.00307 Ma, 2015, Enterocytozoon bieneusi genotypes in yaks (Bos grunniens) and their public health potential, J. Eukaryot. Microbiol., 62, 21, 10.1111/jeu.12141 Tang, 2018, Genetic diversity within dominant Enterocytozoon bieneusi genotypes in pre-weaned calves, Parasit. Vectors, 11, 170, 10.1186/s13071-018-2768-x Wang, 2019, Infection patterns, clinical significance, and genetic characteristics of Enterocytozoon bieneusi and Giardia duodenalis in dairy cattle in Jiangsu, China, Parasitol. Res., 118, 3053, 10.1007/s00436-019-06426-3 Wu, 2018, Occurrence and molecular characterization of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi from Tibetan sheep in Gansu, China, Infect. Genet. Evol., 64, 46, 10.1016/j.meegid.2018.06.012 Zhang, 2018, Enterocytozoon bieneusi genotypes in Tibetan sheep and yaks, Parasitol. Res., 117, 721, 10.1007/s00436-017-5742-1 Zhao, 2015, First report of zoonotic Cryptosporidium spp., Giardia intestinalis and Enterocytozoon bieneusi in golden takins (Budorcas taxicolor bedfordi), Infect. Genet. Evol., 34, 394, 10.1016/j.meegid.2015.07.016 Rozas, 2017, Dnasp 6: DNA sequence polymorphism analysis of large data sets, Mol. Biol. Evol., 34, 3299, 10.1093/molbev/msx248 Haubold, 2000, Lian 3.0: detecting linkage disequilibrium in multilocus data. Linkage analysis, Bioinformatics, 16, 847, 10.1093/bioinformatics/16.9.847 Kumar, 2016, Mega7: molecular evolutionary genetics analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 33, 1870, 10.1093/molbev/msw054 Peakall, 2012, Genalex 6.5: genetic analysis in excel. Population genetic software for teaching and research--an update, Bioinformatics, 28, 2537, 10.1093/bioinformatics/bts460 Bandelt, 1999, Median-joining networks for inferring intraspecific phylogenies, Mol. Biol. Evol., 16, 37, 10.1093/oxfordjournals.molbev.a026036 van Baarlen, 2007, Molecular mechanisms of pathogenicity: how do pathogenic microorganisms develop cross-kingdom host jumps?, FEMS Microbiol. Rev., 31, 239, 10.1111/j.1574-6976.2007.00065.x Wang, 2018, Prevalence and genotypes of Enterocytozoon bieneusi in China, Acta Trop., 183, 142, 10.1016/j.actatropica.2018.04.017 Li, 2014, Genotypes of Enterocytozoon bieneusi in livestock in China: high prevalence and zoonotic potential, PLoS One, 9 Liu, 2017, Infection by and genotype characteristics of Enterocytozoon bieneusi in HIV/AIDS patients from Guangxi Zhuang autonomous region, China, BMC Infect. Dis., 17, 684, 10.1186/s12879-017-2787-9 Wan, 2016, High prevalence and widespread distribution of zoonotic Enterocytozoon bieneusi genotypes in swine in Northeast China: implications for public health, J. Eukaryot. Microbiol., 63, 162, 10.1111/jeu.12264 Yang, 2017, Molecular characterization of Enterocytozoon bieneusi isolates in laboratory macaques in North China: zoonotic concerns, Parasitol. Res., 116, 2877, 10.1007/s00436-017-5603-y Jiang, 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, 3326, 10.1128/AEM.00328-15 Feng, 2019, Prevalence and genotypic identification of Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in pre-weaned dairy calves in Guangdong, China, Parasit. Vectors, 12, 41, 10.1186/s13071-019-3310-5 Li, 2020, Zoonotic potential of Enterocytozoon bieneusi and Giardia duodenalis in horses and donkeys in northern China, Parasitol. Res., 119, 1101, 10.1007/s00436-020-06612-8 Deng, 2016, Molecular characterization and multilocus genotypes of Enterocytozoon bieneusi among horses in Southwestern China, Parasit. Vectors, 9, 561, 10.1186/s13071-016-1844-3 Zhao, 2019, Molecular detection and genotyping of Enterocytozoon bieneusi in racehorses in China, Front. Microbiol., 10, 1920, 10.3389/fmicb.2019.01920 Yu, 2020, Molecular characterization and zoonotic potential of Enterocytozoon bieneusi, Giardia duodenalis and Cryptosporidium sp. In farmed masked palm civets (Paguma larvata) in Southern China, Parasit. Vectors, 13, 403, 10.1186/s13071-020-04274-0 Ma, 2020, Prevalence and genotype distribution of Enterocytozoon bieneusi in farmed raccoon dogs (Nyctereutes procyonoides) in Shandong province, eastern China, Parasitol. Res., 119, 1873, 10.1007/s00436-020-06693-5 Li, 2020, Molecular identification and genotyping of Enterocytozoon bieneusi in experimental rats in China, Exp. Parasitol., 210, 107850, 10.1016/j.exppara.2020.107850 Wang, 2019, Dominance of zoonotic genotype d of Enterocytozoon bieneusi in bamboo rats (Rhizomys sinensis), Infect. Genet. Evol., 73, 113, 10.1016/j.meegid.2019.04.025 Li, 2018, Genotypes of Enterocytozoon bieneusi in dogs and cats in eastern China, Iran. J. Parasitol., 13, 457 Li, 2015, Molecular characterization of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi in captive wildlife at Zhengzhou zoo, China, J. Eukaryot. Microbiol., 62, 833, 10.1111/jeu.12269 Karim, 2014, Genetic diversity in Enterocytozoon bieneusi isolates from dogs and cats in China: host specificity and public health implications, J. Clin. Microbiol., 52, 3297, 10.1128/JCM.01352-14 Ye, 2014, Occurrence of human-pathogenic Enterocytozoon bieneusi, Giardia duodenalis and Cryptosporidium genotypes in laboratory macaques in Guangxi, China, Parasitol. Int., 63, 132, 10.1016/j.parint.2013.10.007 Smith, 2004, Outbreaks of enteric infections caused by multiple pathogens associated with calves at a farm day camp, Pediatr. Infect. Dis. J., 23, 1098, 10.1097/01.inf.0000145409.74116.e5 Conrad, 2017, Farm fairs and petting zoos: a review of animal contact as a source of zoonotic enteric disease, Foodborne Pathog. Dis., 14, 59, 10.1089/fpd.2016.2185 Robinson, 2014, Raw milk consumption among patients with non-outbreak-related enteric infections, Minnesota, USA, 2001–2010, Emerg. Infect. Dis., 20, 38, 10.3201/eid2001.120920 Karmali, 2018, Factors in the emergence of serious human infections associated with highly pathogenic strains of Shiga toxin-producing Escherichia coli, Int. J. Med. Microbiol., 308, 1067, 10.1016/j.ijmm.2018.08.005