Skip to main content
Download PDF

Host-adaptation of the rare Enterocytozoon bieneusi genotype CHN4 in Myocastor coypus (Rodentia: Echimyidae) in China

Parasites & Vectors volume 13, Article number: 578 (2020) Cite this article

Abstract

Background

Enterocytozoon bieneusi is a zoonotic gastrointestinal pathogen and can infect both humans and animals. The coypu (Myocastor coypus) is a semi-aquatic rodent, in which few E. bieneusi infections have been reported and the distribution of genotypes and zoonotic potential remains unknown.

Methods

A total of 308 fresh fecal samples were collected from seven coypu farms in China to determine the infection rate and the distribution of genotypes of E. bieneusi from coypus using nested-PCR amplification of the internal transcribed spacer (ITS) region of the ribosomal RNA (rRNA) gene.

Results

Enterocytozoon bieneusi was detected with an infection rate of 41.2% (n = 127). Four genotypes were identified, including three known genotypes (CHN4 (n = 111), EbpC (n = 8) and EbpA (n = 7)) and a novel genotype named CNCP1 (n = 1).

Conclusions

The rare genotype CHN4 was the most common genotype in the present study, and the transmission dynamics of E. bieneusi in coypus were different from other rodents. To the best of our knowledge, this is the first report of E. bieneusi infections in coypus in China. Our study reveals that E. bieneusi in coypus may be a potential infection source to humans.

Background

Enterocytozoon bieneusi is an obligate intracellular pathogen, which has been detected in a broad range of hosts, including humans, livestock, companion animals, birds and wildlife [1, 2]. Hosts can be infected by ingesting infective spores through food-borne and water-borne routes or direct contact with infected humans or animals [3]. To date, over 500 genotypes of E. bieneusi were identified in the world by molecular genotyping based on internal transcribed spacer (ITS) region of the ribosomal RNA (rRNA) gene [1, 4]. These genotypes were divided into 11 distinct groups (groups 1 to 11) in a phylogenetic analysis [5]. The majority of the zoonotic genotypes are clustered in Group 1 [5]. Meanwhile, more and more reports show that some genotypes (I, J, BEB4 and BEB6) in Group 2 can also infect humans, indicating a low host specificity and zoonotic inherence of this group [1, 6, 7]. Other groups mostly contain host-adapted genotypes [6].

Previous studies indicated that at least 63 E. bieneusi genotypes have been identified in more than 20 rodent species, including zoonotic ones (BEB6, C, D, EbpA, EbpC, H, Peru8, Peru11, Peru16, PigITS5, S6 and Type IV) [1, 8, 9]. In a previous study, the zoonotic transmission of E. bieneusi occurred between a child and guinea pigs in Peru [10]. About 40% to 50% of the mammalian species are rodents, which are distributed throughout the world except the Antarctic and a handful of islands [11]. Because of their abundant population and broad active range, rodents infected with E. bieneusi pose an unneglectable threat to public health. The coypu (Myocastor coypus) is a large rodent adapted to amphibious environments; nowadays coypus are being widely raised in farms as important fur-bearing animals. However, there is limited information about the infection rate and genetic characteristics of E. bieneusi in coypus worldwide. Therefore, this study aimed to determine the genotypes and infection rate and assess the zoonotic potential of E. bieneusi from coypus in China.

Methods

Sample collection

A total of 308 fresh fecal samples were collected from asymptomatic coypus from seven farms in Anyang and Kaifeng in Henan Province, Yongzhou in Hunan Province, Laibin in Guangxi Zhuang Autonomous Region, Baoding in Hebei Province, Chengdu in Sichuan Province and Ganzhou in Jiangxi Province in China (Table 1, Fig. 1). Each farm was sampled on one occasion from August 2018 to March 2019. In each farm, about 2–4 coypus were kept in one accommodation, which was surrounded by 80 cm-high walls to fence the animals off from each other. The ground of the accommodation was hardened with cement. An accommodation is typically composed of a piece of vacant land as the playground and a pool in which the coypus can swim. The samples were collected when the handlers finished the ground using a high-pressure water gun. All the fecal samples were collected immediately after they excreted using sterile polyethylene gloves and marked with animal information. To avoid duplicate sampling of animals, only one fecal sample was collected from one location of the ground in each accommodation, and all deposits from each accommodation pooled as a single sample. All the samples were transferred to the laboratory in a cooler with ice packs within 36 h and stored at 4 °C.

Table 1 Distribution of E. bieneusi genotypes in coypus from different farms in China
Full size table
Fig. 1
figure 1

adapted from Natural Earth (https://www.naturalearthdata.com)

Map of the Peopleʼs Republic of China showing the sampling locations. The figure was originally designed by the authors under the software ArcGIS 10.2. The original vector diagram imported in ArcGIS was

Full size image

DNA extraction and PCR amplification

Genomic DNA (gDNA) was directly extracted from 200 mg of each sample using E.Z.N.A. Stool DNA Kit (Omega Biotek Inc., Norcross, GA, USA) according to the manufacturer’s protocol with minor modification.

All samples were tested using a nested PCR that targets ITS region (~389-bp fragment) of the rRNA gene of E. bieneusi using primers described previously by Sulaiman et al. [12]. Double distilled water and known positive DNA derived from a golden snub-nosed monkey (genotype D, GenBank: KU604932) were used as negative and positive controls, respectively. The secondary PCR products were separated electrophoretically on 1% agarose (Life Technologies Corporation, CA, USA) gel stained with DNAGreen (Tiandz, Beijing, China) and visualized under UV light.

Sequencing and data analyses

Positive secondary PCR products were sequenced bidirectionally by Sangon Biotech Co. Ltd., Shanghai, China. The sequences obtained here were assembled and edited in the software Lasergene EditSeq version 7.1.0 (https://www.dnastar.com/) and multiple alignment with the reference sequences downloaded from GenBank was applied in Clustal X version 2.1 (https://www.clustal.org/).

All statistical analyses were performed with IBM SPSS Statistics version 19.0 (www.ibm.com/products/spssstatistics). Difference of prevalence of E. bieneusi among different age groups were compared using Fisher’s exact test, and the odds ratios (ORs) with the 95% confidence interval (CI) were also calculated. A two-sided P-value of 0.05 or less was set as significant.

To reveal the phylogenetic relationships and zoonotic risk of E. bieneusi isolates, a phylogenetic tree was constructed by the Neighbor-Joining (NJ) method using the Kimura-2-parameter algorithm in MEGA version 7.0.26 (https://www.megasoftware.net). The robustness of the nodes was tested by a bootstrap analysis of 1000 iterations.

Results

Infection rate of E. bieneusi in coypus

Enterocytozoon bieneusi was detected in 127 of 308 coypus with an infection rate of 41.2%. This parasite was found in every farm, and the highest infection rate of E. bieneusi in coypus was detected in Anyang (72.3%, 73/101), followed by Baoding (62.9%, 22/35), Kaifeng (30.8%, 16/52), Ganzhou (20.0%, 7/35), Chengdu (15.0%, 6/40), Laibin (9.1%, 2/22) and Yongzhou (4.3%, 1/23) (Table 1). The differences in infection rates of E. bieneusi in coypus among different farms were statistically significant (P < 0.0001).

The highest infection rate (76.9%, 50/65) was detected in the < 3-month-old group, followed by the 3–6 month-old group (51.1%, 24/47) and > 6 month-old group (28.5%, 53/186) (Table 2) (P < 0.0001). The correlations between age and the infection rates were evaluated by calculating the ORs and their 95% CIs, which are shown in Table 2. There was a significant negative correlation between the infection rate and age in this study, as an OR of 0.31 (95% CI: 0.14–0.70, P = 0.005) was associated with the 3–6-month-old group, and an OR of 0.12 (95% CI: 0.06–0.23, P < 0.0001) was associated with the > 6-month-old group.

Table 2 Occurrence of E. bieneusi in coypus by age
Full size table

Enterocytozoon bieneusi ITS genotypes

Four distinct E. bieneusi genotypes, including three previously reported genotypes [CHN4 (n = 111), EbpC (n = 8), EbpA (n = 7)], and one novel genotype (named CNCP1, n = 1) were observed. Genotype CHN4 was the most common genotype and detected in 6 farms except the farm in Yongzhou. Genotype EbpC was distributed in Yongzhou, Laibin and Kaifeng, while genotype EbpA and novel genotype CNCP1 were only detected in the specimens from Kaifeng.

CHN4 was the only genotype detected in the < 3-month-old group (n = 50). In the 3–6-month-old group, CHN4 was also the predominant genotype, which was detected in 16 samples, followed by EbpA (n = 4), EbpC (n = 3) and CNCP1 (n = 1). In the age group > 6 months, 3 genotypes (CHN4, EbpC and EbpA) were detected in 45, 5 and 3 samples, respectively.

Phylogenetic analysis of E. bieneusi

The phylogenetic relationships and zoonotic risk of E. bieneusi genotypes were analyzed by the NJ tree. Genotype CNCP1 had one single nucleotide polymorphism (SNP) at nucleotide position 274 (G to A) compared to genotype EbpA (GenBank: MK968834). All the genotypes identified in this study were clustered in Group 1 (Fig. 2).

Fig. 2
figure 2

Neighbor-joining tree of Enterocytozoon bieneusi ITS genotypes. Phylogenetic relationships of Enterocytozoon bieneusi genotypes of this study and other genotypes previously deposited in GenBank. Bootstrap values > 50% from 1000 are shown on nodes. Sample names include GenBank accession number followed by host and then genotype designation. Known and novel genotypes identified in this study are indicated by empty and filled triangles, respectively

Full size image

Discussion

The infection rate of E. bieneusi in rodent species varies from 2.5% to 100% worldwide [13, 14]. To the best of our knowledge, this is the first report of E. bieneusi infections in coypus in China. In the present study, the overall infection rate of E. bieneusi was 41.2% in coypus, which is higher than the infection rate of E. bieneusi reported in brown rats (7.9%) [8], bamboo rats (5.1%) [15], experimental brown rats (4.8%) [16], commensal rodents (mouse and brown rat) (4.0%) [14], pet chinchillas (3.6%) [17] and red squirrels (19.4%) [18] in China. In addition, lower infection rates were also reported in wild house mice (10.7%) from a hybrid zone across the Czech Republic-Germany border [19], and beavers (15.3%) and muskrats (8.4%) from the USA [20]. However, higher infection rates of E. bieneusi were reported in chipmunks (71.4%) and woodchucks (100%) from USA [13]. Similar infection rates of E. bieneusi have been reported in small rodents (mouse, bank vole, yellow-necked mouse and striped field mouse) (38.9%) from southwestern Poland [21], and a laboratory prairie dog colony (37.9%) in the USA [22]. The infection rates of E. bieneusi in rodents could be influenced by many factors, such as animal immune status, age distribution, sample size, detection method, feeding environment, management system and population density [16]. Because the high infection rate detected in coypus in our study, we can draw a preliminary inference that coypus are more susceptible to E. bieneusi than many other rodent species, which should be confirmed by more investigations in the future.

A variation of the positive rate of E. bieneusi in coypus was observed in the present study with the highest being detected in Anyang (72.3%, 73/101) and the lowest in Laibin (9.1%, 2/22). Geographical location-based variation in the prevalence of E. bieneusi in rodents has been reported such as in brown rats in different provinces in China, which was ranged between 2.9–14.7% [8, 14, 16, 23, 24]. This phenomenon has also been reported in other animals, for example, in alpacas (Vicugna pacos) in China (0–42.9%) [25] and in Asiatic black bear (Ursus thibetanus) in China (0–50%) [26]. The difference may be related to geographical environments and feeding density.

In the present study, the dominant genotype of E. bieneusi was CHN4, which was detected in six cities except Yongzhou, indicating that genotype CHN4 is commonly found in coypus in China. This genotype has been identified in three human and two cattle samples [27] and four pre-weaned calf samples [28] from China, and is found for the first time in coypus in the present study. These findings indicated that genotype CHN4 has a wide range of animal reservoirs and potential for zoonotic transmission. Genotype D was identified in squirrels from China [29] and USA [13], chipmunks [30], bamboo rats [15] and brown rats [8, 23] from China, house mice from Czech Republic-Germany border [19] and striped field mice from Poland [21], and genotype WL4 was observed in squirrels, chipmunks and muskrats from the USA [13, 20] (Table 3). EbpA, EbpC, PigEBITS7, S7, Peru16 and CHG14 have also been reported as the most common genotypes in experimental brown rat, beaver, giant rat, guinea pig, guinea pig and brown rat, respectively [10, 14, 16, 20, 23, 31]. Additionally, in a more recent study of E. bieneusi in Himalayan marmots (Marmota himalayana) and Alashan ground squirrels (Spermophilus alashanicus) revealed that genotype ZY37 was the most common one [9]. The rare genotype CHN4 was the dominant genotype, indicating that the transmission dynamic of E. bieneusi in coypus is different from other rodents. This may be explained by the unique life habits of coypus as aquatic rodents compared to other rodents involved in previous studies.

Table 3 Prevalence and genotype distribution of Enterocytozoon bieneusi in rodents worldwide (Li et al. [1])
Full size table

Genotype EbpA and EbpC have been detected in several rodent species (squirrel, house mouse, experimental brown rat, muskrat, bamboo rat and beaver) worldwide [15, 16, 19, 20, 29] (Table 3). They are two of the most common genotypes detected in both immunocompetent and immunocompromised people worldwide [1]. Meanwhile, genotype EbpA and EbpC have a vast host range, such as non-human primates (NHPs), livestock (cattle, buffalo, sheep and goat), pets (dog and horse), wild animals (deer, fox, raccoon, bear, panda and otter) and birds (pigeon, crane and parrot) [1]. These two genotypes also have been observed in lake water [32], river water [33] and wastewater treatment plants [34, 35]. According to these data, the interspecies transmission of genotype EbpA and EbpC pose a zoonotic risk to human or other animals, and coypus may serve as a reservoir of EbpA and EbpC in the E. bieneusi transmission.

In the phylogenetic analysis, an NJ tree was constructed and the novel genotype CNCP1 clustered with CHN4, EbpC and EbpA in group 1. The majority of the zoonotic genotypes belongs to the Group 1, and genotypes CHN4, EbpC and EbpA have been reported in humans [27, 36, 37], indicating that genotype CNCP1 maybe has zoonotic potential and the E. bieneusi isolates in coypus detected in this study can be transmissible from coypus to humans, especially the animal handlers, or vice versa.

Conclusions

Enterocytozoon bieneusi infection was highly observed in coypus from China, with the high prevalence of rare genotype CHN4. The presence of zoonotic genotypes EbpC and EbpA revealed the role of coypus as a reservoir of E. bieneusi and posed a threat to the public health. To further characterize the role of coypus in the transmission of microsporidiosis, more intensive research of E. bieneusi should be devised and employed.

Availability of data and materials

The nucleotide sequences from this study were deposited in the GenBank database under the accession numbers MT549052 and MT557703-MT557705.

Abbreviations

ITS:

Internal transcribed spacer

gDNA:

Genomic DNA

CI:

Confidence interval

OR:

Odds ratio

NJ:

Neighbor-joining

NHP:

Non-human primate

SNP:

Single-nucleotide polymorphism

rRNA:

Ribosomal RNA

References

  1. Li W, Feng Y, Santin M. Host specificity of Enterocytozoon bieneusi and public health implications. Trends Parasitol. 2019;35:436–51.

    Article  CAS  Google Scholar 

  2. Santín M, Fayer R. Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Res Vet Sci. 2011;90:363–71.

    Article  Google Scholar 

  3. Thellier M, Breton J. Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite. 2008;15:349–58.

    Article  CAS  Google Scholar 

  4. Li W, Xiao L. Multilocus sequence typing and population genetic analysis of Enterocytozoon bieneusi: host specificity and its impacts on public health. Front Genet. 2019;10:307.

    Article  CAS  Google Scholar 

  5. Li N, Ayinmode AB, Zhang H, Feng Y, Xiao L. Host-adapted Cryptosporidium and Enterocytozoon bieneusi genotypes in straw-colored fruit bats in Nigeria. Int J Parasitol Parasites Wildl. 2019;8:19–24.

    Article  CAS  Google Scholar 

  6. Karim MR, Rume FI, Rahman A, Zhang Z, Li J, Zhang L. Evidence for zoonotic potential of Enterocytozoon bieneusi in its first molecular characterization in captive mammals at Bangladesh national zoo. J Eukaryot Microbiol. 2020;67:427–35.

    Article  CAS  Google Scholar 

  7. Wang S, Wang R, Fan X, Liu T, Zhang L, Zhao G. Prevalence and genotypes of Enterocytozoon bieneusi in China. Acta Trop. 2018;183:142–52.

    Article  CAS  Google Scholar 

  8. Zhao W, Wang J, Ren G, Yang Z, Yang F, Zhang W et al. Molecular characterizations of Cryptosporidium spp. and Enterocytozoon bieneusi in brown rats (Rattus norvegicus) from Heilongjiang Province, China. Parasit Vectors. 2018;11:313.

  9. Xu J, Wang X, Jing H, Cao S, Zhang X, Jiang Y, et al. Identification and genotyping of Enterocytozoon bieneusi in wild Himalayan marmots (Marmota himalayana) and Alashan ground squirrels (Spermophilus alashanicus) in the Qinghai-Tibetan Plateau area (QTPA) of Gansu Province. China Parasit Vectors. 2020;13:367.

    Article  CAS  Google Scholar 

  10. Cama VA, Pearson J, Cabrera L, Pacheco L, Gilman R, Meyer S, et al. Transmission of Enterocytozoon bieneusi between a child and guinea pigs. J Clin Microbiol. 2007;45:2708–10.

    Article  CAS  Google Scholar 

  11. Wikipedia contributors. Rodent. In: Wikipedia, The Free Encyclopedia. https://en.wikipedia.org/w/index.php?title=Rodent&oldid=975023737. Accessed 08 Sep 2020.

  12. Sulaiman IM, Fayer R, Yang C, Santín M, Matos O, Xiao L. Molecular characterization of Enterocytozoon bieneusi in cattle indicates that only some isolates have zoonotic potential. Parasitol Res. 2004;92:328–34.

    Article  Google Scholar 

  13. Guo Y, Alderisio KA, Yang W, Cama V, Feng Y, Xiao L. Host specificity and source of Enterocytozoon bieneusi genotypes in a drinking source watershed. Appl Environ Microbiol. 2014;80:218–25.

    Article  CAS  Google Scholar 

  14. Yu F, Qi M, Zhao Z, Lv C, Wang Y, Wang R, et al. The potential role of synanthropic rodents and flies in the transmission of Enterocytozoon bieneusi on a dairy cattle farm in China. J Eukaryot Microbiol. 2019;66:435–41.

    Article  Google Scholar 

  15. Wang H, Liu Q, Jiang X, Zhang Y, Zhao A, Cui Z, et al. Dominance of zoonotic genotype D of Enterocytozoon bieneusi in bamboo rats (Rhizomys sinensis). Infect Genet Evol. 2019;73:113–8.

    Article  Google Scholar 

  16. Li J, Jiang Y, Wang W, Chao L, Jia Y, Yuan Y, et al. Molecular identification and genotyping of Enterocytozoon bieneusi in experimental rats in China. Exp Parasitol. 2020;210:107850.

    Article  CAS  Google Scholar 

  17. Qi M, Luo N, Wang H, Yu F, Wang R, Huang J et al. Zoonotic Cryptosporidium spp. and Enterocytozoon bieneusi in pet chinchillas (Chinchilla lanigera) in China. Parasitol Int. 2015;64:339–41.

  18. Deng L, Chai Y, Luo R, Yang L, Yao J, Zhong Z 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.

  19. Sak B, Kváč M, Květoňová D, Albrecht T, Piálek J. The first report on natural Enterocytozoon bieneusi and Encephalitozoon spp. infections in wild East-European house mice (Mus musculus musculus) and West-European house mice (M. m. domesticus) in a hybrid zone across the Czech Republic-Germany border. Vet Parasitol. 2011;178:246–50.

  20. Sulaiman IM, Fayer R, Lal AA, Trout JM, Schaefer FW 3rd, Xiao L. Molecular characterization of microsporidia indicates that wild mammals Harbor host-adapted Enterocytozoon spp. as well as human-pathogenic Enterocytozoon bieneusi. Appl Environ Microbiol. 2003;69:4495–501.

  21. Perec-Matysiak A, Buńkowska-Gawlik K, Kváč M, Sak B, Hildebrand J, Leśniańska K. Diversity of Enterocytozoon bieneusi genotypes among small rodents in southwestern Poland. Vet Parasitol. 2015;214:242–6.

    Article  Google Scholar 

  22. Roellig DM, Salzer JS, Carroll DS, Ritter JM, Drew C, Gallardo-Romero N, et al. Identification of Giardia duodenalis and Enterocytozoon bieneusi in an epizoological investigation of a laboratory colony of prairie dogs Cynomys ludovicianus. Vet Parasitol. 2015;210:91–7.

    Article  Google Scholar 

  23. Wang J, Lv C, Zhao D, Zhu R, Li C, Qian W. First detection and genotyping of Enterocytozoon bieneusi in pet fancy rats (Rattus norvegicus) and guinea pigs (Cavia porcellus) in China. Parasite. 2020;27:21.

    Article  CAS  Google Scholar 

  24. Zhao W, Zhou H, Yang L, Ma T, Zhou J, Liu H, et al. Prevalence, genetic diversity and implications for public health of Enterocytozoon bieneusi in various rodents from Hainan Province. China Parasit Vectors. 2020;13:438.

    Article  CAS  Google Scholar 

  25. Zhang Q, Wang H, Zhao A, Zhao W, Wei Z, Li Z, et al. Molecular detection of Enterocytozoon bieneusi in alpacas (Vicugna pacos) in Xinjiang. China Parasite. 2019;26:31.

    Article  Google Scholar 

  26. Wu J, Han J, Shi L, Zou Y, Li Z, Yang J, et al. Prevalence, genotypes, and risk factors of Enterocytozoon bieneusi in Asiatic black bear (Ursus thibetanus) in Yunnan Province. Southwestern China Parasitol Res. 2018;117:1139–45.

    Article  Google Scholar 

  27. Zhang X, Wang Z, Su Y, Liang X, Sun X, Peng S, et al. Identification and genotyping of Enterocytozoon bieneusi in China. J Clin Microbiol. 2011;49:2006–8.

    Article  CAS  Google Scholar 

  28. Tang C, Cai M, Wang L, Guo Y, Li N, Feng Y, et al. Genetic diversity within dominant Enterocytozoon bieneusi genotypes in pre-weaned calves. Parasit Vectors. 2018;11:170.

    Article  Google Scholar 

  29. Deng L, Li W, Yu X, Gong C, Liu X, Zhong Z, et al. First report of the human-pathogenic Enterocytozoon bieneusi from red-bellied tree squirrels (Callosciurus erythraeus) in Sichuan. China PLoS One. 2016;11:e0163605.

    Article  Google Scholar 

  30. Deng L, Li W, Zhong Z, Chai Y, Yang L, Zheng H, et al. Molecular characterization and new genotypes of Enterocytozoon bieneusi in pet chipmunks (Eutamias asiaticus) in Sichuan province. China BMC Microbiol. 2018;18:37.

    Article  Google Scholar 

  31. Gui B, Zou Y, Chen Y, Li F, Jin Y, Liu M, et al. Novel genotypes and multilocus genotypes of Enterocytozoon bieneusi in two wild rat species in China: potential for zoonotic transmission. Parasitol Res. 2020;119:283–90.

    Article  Google Scholar 

  32. Ye J, Xiao L, Ma J, Guo M, Liu L, Feng Y. Anthroponotic enteric parasites in monkeys in public park. China Emerg Infect Dis. 2012;18:1640–3.

    Article  Google Scholar 

  33. Hu Y, Feng Y, Huang C, Xiao L. Occurrence, source, and human infection potential of Cryptosporidium and Enterocytozoon bieneusi in drinking source water in Shanghai, China, during a pig carcass disposal incident. Environ Sci Technol. 2014;48:14219–27.

    Article  CAS  Google Scholar 

  34. Li N, Xiao L, Wang L, Zhao S, Zhao X, Duan L et al. Molecular surveillance of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi by genotyping and subtyping parasites in wastewater. PLoS Negl Trop Dis. 2012;6:e1809.

  35. Ye J, Ji Y, Xu J, Ma K, Yang X. Zoonotic Enterocytozoon bieneusi in raw wastewater in Zhengzhou, China. Folia Parasitol (Praha). 2017;2017(64):002.

    Google Scholar 

  36. Sak B, Brady D, Pelikánová M, Květoňová D, Rost M, Kostka M, et al. Unapparent microsporidial infection among immunocompetent humans in the Czech Republic. J Clin Microbiol. 2011;49:1064–70.

    Article  Google Scholar 

  37. Wang L, Zhang H, Zhao X, Zhang L, Zhang G, Guo M, et al. Zoonotic Cryptosporidium species and Enterocytozoon bieneusi genotypes in HIV-positive patients on antiretroviral therapy. J Clin Microbiol. 2013;51:557–63.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank animal farm staff for collecting samples.

Funding

This work was supported in part by the National Natural Science Foundation of China (31860699), and by the Program for Young and Middle-aged Leading Science, Technology, and Innovation of Xinjiang Production & Construction Group (2018CB034). The sponsors played no role in study design, in the collection, analysis, or interpretation of the data, in writing the report, or in the decision to submit the article for publication.

Author information

Authors and Affiliations

  1. College of Animal Science, Tarim University, No. 1188 Junken Avenue, Alar, 843300, Xinjiang, People’s Republic of China

    Fuchang Yu, Yangwenna Cao, Qiang Liu, Aiyun Zhao & Meng Qi

  2. College of Animal Science and Veterinary Medicine, Henan Agricultural University, No. 15 Longzihu University Area, Zhengzhou New District, Zhengzhou, 450046, Henan, People’s Republic of China

    Fuchang Yu, Meng Qi & Longxian Zhang

  3. Experimental and Research Center, Henan University of Animal Husbandry and Economy, Zhengzhou, 450046, Henan, People’s Republic of China

    Haiyan Wang

Authors
  1. Fuchang Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yangwenna Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haiyan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qiang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aiyun Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Meng Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Longxian Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YC, HW and QL collected samples, FY, YC, HW and QL performed the analysis and interpretation, FY, YC, HW, QL and AZ carried out the methodology, HW, AZ, MQ and LZ were involved in conceptualization, FY, MQ and LZ wrote the manuscript, AZ and LZ provided supervision of project and MQ obtained grant funding. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Meng Qi or Longxian Zhang.

Ethics declarations

Ethics approval and consent to participate

The present study was carried out in accordance with the Chinese Laboratory Animal Administration Act of adopted in 1988. The research protocol was reviewed and approved by the Institutional Review Board of Henan Agricultural University (Approval No. IRB-HENAU-20190424-01). Specimens were collected after acquiring the permission of animal owners and no animals were injured during this procedure.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yu, F., Cao, Y., Wang, H. et al. Host-adaptation of the rare Enterocytozoon bieneusi genotype CHN4 in Myocastor coypus (Rodentia: Echimyidae) in China. Parasites Vectors 13, 578 (2020). https://doi.org/10.1186/s13071-020-04436-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s13071-020-04436-0

Keywords

  • Microsporidia
  • Rodent
  • Species specificity
  • Transmission
  • Zoonotic

Parasites & Vectors

ISSN: 1756-3305

Contact us