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

Enterocytozoon bieneusi is a zoonotic pathogen with worldwide distribution. Among the 11 established groups of E. bieneusi genotypes based on phylogenetic analysis of the ribosomal internal transcribed spacer (ITS), the human-infective potential and population genetics of the Group 1 genotypes from diverse hosts are well characterized. In contrast, Group 2 genotypes from ruminants have unclear population genetics, leading to poor understanding of their host range and zoonotic potential. In this study, we sequence-characterized 121 Group 2 isolates from dairy cattle, beef cattle, yaks, Tibetan sheep, golden takins, and deer from China at five genetic loci (ITS, MS1, MS3, MS4 and MS7), comparing with data from 113 Group 1 isolates from nonhuman primates. Except for MS7, most of the genetic loci produced efficient PCR amplification and high nucleotide identity between Groups 1 and 2 of E. bieneusi genotypes. In population genetic analyses of the sequence data, a strong linkage disequilibrium was observed among these genetic loci in the overall Group 2 population. The individual ITS genotypes (I, J and BEB4) within Group 2, however, had reduced linkage disequilibrium and increased genetic exchanges among isolates. There was only partial genetic differentiation between Group 1 and Group 2 genotypes, with some occurrence of genetic recombination between them. Genetic recombination was especially common between genotypes I and J within Group 2. The data presented indicate a high genetic identity between Group 1 and Group 2 genotypes of E. bieneusi, which could be responsible for the broad host range and high zoonotic potential of Group 2 genotypes in China. As there is no effective treatment against E. bieneusi, the One Health approach should be used in the control and prevention of zoonotic transmission of the pathogen.