Abstract
BackgroundEnterocytozoon bieneusi is one of common intestinal pathogens in humans and animals including non-human primates (NHPs). Many zoonotic pathogens including E. bieneusi have been found in these animals. However, there are few studies on the population structure of E. bieneusi in NHPs. To infer the gene diversity and population genetics of E. bieneusi, we selected 88 E. bieneusi-positive samples from crab-eating macaques for multilocus characterizations in this study.MethodsThe E. bieneusi isolates examined belonged to three common genotypes with different host ranges by sequence analysis of the ribosomal internal transcribed spacer (ITS): Type IV (n = 44), Macaque3 (n = 24) and Peru8 (n = 20). They were further characterized by sequence analysis at four microsatellite and minisatellite loci (MS1, MS3, MS4 and MS7). DnaSP, Arlequin and LIAN were used to analyze the sequence data together with those from the ITS locus to infer the population genetics. Subpopulation structure was inferred using phylogenetic and STRUCTURE analyses.ResultsSeventy-two (81.8%), 71 (80.7%), 76 (86.4%) and 79 (89.8%) samples were amplified and sequenced successfully at the MS1, MS3, MS4 and MS7 loci, respectively, with 53 having sequence data at all five MLST loci including ITS. Altogether, 33 multilocus genotypes (MLGs) were produced based on concatenated sequences from the 53 samples. In phylogenetic analyses of sequences and allelic data, four major subpopulations (SPs) were observed with different ITS genotypes in each of them: Type IV and Peru8 in SP1 and SP2; Type IV, Macaque3 and Peru8 in SP3; and Type IV and Macaque3 in SP4. SP3 and SP4 were phylogenetically related and might be NHP-specific based on the fact that Macaque3 is mostly found in NHPs. A strong linkage disequilibrium (LD) was observed among the multilocus sequences and allelic data.ConclusionsThe significant LD in the multilocus sequence analysis indicated the presence of an overall clonal population structure of E. bieneusi in crab-eating macaques. The inconsistent segregation of MLGs among ITS genotypes suggested some occurrence of genetic recombination. These observations should improve our understanding of the population genetics of E. bieneusi in NHPs.
Highlights
Enterocytozoon bieneusi is one of common intestinal pathogens in humans and animals including nonhuman primates (NHPs)
These observations should improve our understanding of the population genetics of E. bieneusi in NHPs
The clustering of the host-adapted internal transcribed spacer (ITS) genotype Macaque3 in SP3 and SP4 suggests the NHP-specific nature of these two subpopulations. Both potentially zoonotic and host-adapted subpopulations have been identified in Group 1 in previous studies. The former included multilocus genotype (MLG) of ITS genotypes Type IV, D, Peru8, WL11, and Peru11 in humans, NHPs, pigs and Conclusions A much higher genetic diversity was revealed in E. bieneusi isolates from crab-eating macaques by multilocus sequence typing (33 MLGs) than by ITS genotyping
Summary
Enterocytozoon bieneusi is one of common intestinal pathogens in humans and animals including nonhuman primates (NHPs). Since the detection of E. bieneusi in AIDS patients in 1985 for the first time, this pathogen has been found in other immunocompromised/immunodeficient individuals, such as organ transplant recipients, children, and lifethreatening and persistent diarrhea often occur in these populations [2,3,4,5,6,7] It has been recently identified in several species of non-human primates (NHPs) in China and elsewhere [8,9,10,11,12,13,14]. 500 E. bieneusi genotypes have been identified based on sequence analysis of the internal transcribed spacer (ITS) region of the rRNA gene [15, 16] Macaque has been mostly found in monkeys and occasionally in dogs in China [1, 21, 23,24,25,26]
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