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Multilocus Sequence Typing and Population Genetic Analysis of Enterocytozoon bieneusi: Host Specificity and Its Impacts on Public Health.

ABSTRACT: Microsporidia comprise a large class of unicellular eukaryotic pathogens that are medically and agriculturally important, but poorly understood. There have been nearly 1,500 microsporidian species described thus far, which are variable in biology, genetics, genomics, and host specificity. Among those, Enterocytozoon bieneusi is the well-known species responsible for the most recorded cases of human microsporidian affections. The pathogen can colonize a broad range of mammals and birds and most of the animals surveyed share some genotypes with humans, posing a threat to public health. Based on DNA sequence analysis of the ribosomal internal transcribed spacer (ITS) and phylogenetic analysis, several hundreds of E. bieneusi genotypes have been defined and clustered into different genetic groups with varied levels of host specificity. However, single locus-based typing using ITS might have insufficient resolution to discriminate among E. bieneusi isolates with complex genetic or hereditary characteristics and to assess the elusive reproduction or transmission modes of the organism, highlighting the need for exploration and application of multilocus sequence typing (MLST) and population genetic tools. The present review begins with a primer on microsporidia and major microsporidian species, briefly introduces the recent advances on E. bieneusi ITS genotyping and phylogeny, summarizes recent MLST and population genetic data, analyzes the inter- and intragroup host specificity at the MLST level, and interprets the public health implications of host specificity in zoonotic or cross-species transmission of this ubiquitous fungus.

SUBMITTER: Li W

PROVIDER: S-EPMC6454070 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Project description:Enterocytozoon bieneusi is one of the most common intestinal pathogens in humans and animals. E. bieneusi has been confirmed to be complex microsporidian species. Approximately 500 ITS genotypes of E. bieneusi have been defined. With the establishment and application of multilocus sequencing typing and population genetic tools in E. bieneusi, the studies on these aspects have been carried out worldwide, but little information is available. To understand genetic variation of mini-/micro-satellites and the population structure and substructure of E. bieneusi in northeastern China, 305 E. bieneusi DNA specimens composed of 28 ITS genotypes were from 13 mammal species and five bird species in the investigated areas. They were characterized by nested-PCR amplification and sequencing at four mini-/micro-satellite loci (MS1, MS3, MS4, and MS7). At the MS1, MS3, MS4, and MS7 loci, 153 (50.16%), 131 (42.95%), 133 (43.61%), and 128 (41.97%) DNA specimens were amplified and sequenced successfully with 44, 17, 26, and 24 genotypes being identified, respectively. Multilocus genotypes (MLGs) showed a higher genetic diversity than ITS genotypes. 48 MLGs were produced out of 90 ITS-positive DNA specimens based on concatenated sequences of all the five genetic loci including ITS. Linkage disequilibrium (LD) and limited genetic recombination were observed by measuring LD using both multilocus sequences and allelic profile data, indicating an overall clonal population structure of E. bieneusi in the investigated areas. These data will aid in the longitudinal tracking of the attribution of source of infection/contamination and in elucidating transmission dynamics, and will provide valuable information for making efficient control strategies to intervene with and prevent occurrence of microsporidiosis caused by E. bieneusi among animals and transmission of E. bieneusi from animals to humans in the investigated areas. Phylogenetic and network analyses identified three different subgroups, revealing the presence of host-shaped segregation and the absence of geographical segregation in E. bieneusi population. Meanwhile, the MLGs from zoonotic ITS genotypes were observed to be basically separated from the MLGs from host-adapted ones. Assessment of substructure will have a reference effect on understanding of zoonotic or interspecies transmission of E. bieneusi and evolution direction from zoonotic genotypes to host-adapted genotypes.

Project description:BackgroundEnterocytozoon bieneusi is a common opportunistic pathogen that is widely detected in humans, domestic animals and wildlife, and poses a challenge to public health. The present study was performed to evaluate the prevalence, genotypic diversity and zoonotic potential of E. bieneusi among wildlife at Chengdu and Bifengxia zoological gardens in Sichuan Province, China.ResultsOf the 272 fresh fecal samples harvested from 70 captive wildlife species at Chengdu Zoo (n = 198) and Bifengxia Zoo (n = 74), 21 (10.6 %) and 22 (29.7 %) tested positive for E. bieneusi by internal transcribed spacer (ITS) sequencing analysis, respectively. Specifically, genotypes D, Peru 6, CHB1, BEB6, CHS9, SC02 and SC03, and genotypes D, CHB1, SC01 and SC02 were detected in the Chengdu and Bifengxia Zoo samples, respectively. Five known genotypes (D, Peru 6, BEB6, CHS9 and CHB1) and three novel genotypes (SC01, SC02 and SC03) were clustered into the zoonotic group (group 1) and host-adapted group (group 2). Multilocus sequence typing (MLST) analysis targeting three microsatellites (MS1, MS3 and MS7) and one minisatellite (MS4) were successfully sequenced for 37, 33, 35 and 37 specimens, generating 8, 3, 11 and 15 distinct locus types, respectively. Altogether, we identified 27 multilocus genotypes (MLGs) among the E. bieneusi isolates by MLST. These data highlight the high genetic diversity of E. bieneusi among zoo wildlife.ConclusionsTo our knowledge, this is the first report on the prevalence and genotypic diversity of E. bieneusi infections among captive wildlife in zoos in southwest China. Notably, we identified three novel E. bieneusi genotypes, as well as six new mammalian hosts (Asian golden cats, Tibetian blue bears, blackbucks, hog deer, Malayan sun bears and brown bears) for this organism. Moreover, the occurrence of zoonotic genotypes suggests that wildlife may act as reservoirs of E. bieneusi that can serve as a source of human microsporidiosis. The findings presented here should contribute to the control of zoonotic disease in China.

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Multilocus Sequence Typing and Population Genetic Analysis of Enterocytozoon bieneusi: Host Specificity and Its Impacts on Public Health.

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