Multi-locus genotypes of Enterocytozoon bieneusi in captive Asiatic black bears in southwestern China: High genetic diversity, broad host range, and zoonotic potential.

Lei Deng,Guangneng Peng,Xuefeng Cao,Yanchun Hu,Ya Wang,Zhijun Zhong,Xuehan Liu,Xiangming Huang,Kongju Wu,Wuyou Wang,Yuan Song,Hualin Fu,Chao Gong,Min He,Yue Zhang,Wei Li,Tzen-Yuh Chiang

doi:10.1371/journal.pone.0171772

Lei Deng, Guangneng Peng + Show 15 more

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https://doi.org/10.1371/journal.pone.0171772

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Abstract

Enterocytozoon bieneusi is an obligate eukaryotic intracellular parasite that infects a wide variety of vertebrate and invertebrate hosts. Although considerable research has been conducted on this organism, relatively little information is available on the occurrence of E. bieneusi in captive Asiatic black bears. The present study was performed to determine the prevalence, genetic diversity, and zoonotic potential of E. bieneusi in captive Asiatic black bears in zoos in southwestern China. Fecal specimens from Asiatic black bears in four zoos, located in four different cities, were collected and analyzed for the prevalence of E. bieneusi. The average prevalence of E. bieneusi was 27.4% (29/106), with the highest prevalence in Guiyang Zoo (36.4%, 16/44). Altogether, five genotypes of E. bieneusi were identified among the 29 E. bieneusi-positive samples, including three known genotypes (CHB1, SC02, and horse2) and two novel genotypes named ABB1 and ABB2. Multi-locus sequence typing using three microsatellites (MS1, MS3, and MS7) and one minisatellite (MS4) revealed V, III, V, and IV genotypes at these four loci, respectively. Phylogenetic analysis showed that the genotypes SC02 and ABB2 were clustered into group 1 of zoonotic potential, the genotypes CHB1 and ABB1 were clustered into a new group, and the genotype horse2 was clustered into group 6 of unclear zoonotic potential. In conclusion, this study identified two novel E. bieneusi genotypes in captive Asiatic black bears, and used microsatellite and minisatellite markers to reveal E. bieneusi genetic diversity. Moreover, our findings show that genotypes SC02 (identified in humans) and ABB2 belong to group 1 with zoonotic potential, suggesting the risk of transmission of E. bieneusi from Asiatic black bears to humans and other animals.

Highlights

Microsporidia, which are emerging obligate intracellular pathogens, have been classified as fungi
Five genotypes were identified by sequence analysis of the internal transcribed spacer (ITS) gene in 29 E. bieneusi-positive specimens (16 from Guizhou and 13 from Sichuan province), including three known genotypes (CHB1, SC02, and horse2) and two novel genotypes, which were named ABB1 and ABB2
Genotype CHB1, which was identified in the largest number of E. bieneusi-positive specimens (65.5%, 19/29), was the most prevalent genotype in Guiyang Zoo, Panzhihua Zoo, and Xichang Zoo, followed by genotype SC02 (20.7%, 6/29), which was only detected in Chengdu Zoo

Summary

Introduction

Microsporidia, which are emerging obligate intracellular pathogens, have been classified as fungi. These organisms have been shown to infect invertebrate and vertebrate hosts worldwide [1]. Individuals infected with E. bieneusi may shed spores into the environment via feces, resulting in an increased risk of transmission to other animals, including humans, through consumption of contaminated food and water [5]. Clinical manifestations of microsporidiosis caused by E. bieneusi include life-threatening diarrhea and weight loss in individuals with deficient immune systems, such as those with AIDs, transplant recipients, and patients with cancer. Following the first discovery of E. bieneusi infection in a Haitian patient with AIDS, several studies have been performed on the prevalence, genetic diversity, and route of transmission of this pathogen in various animals worldwide [2, 7]

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