Widespread distribution of human-infective Enterocytozoon bieneusi genotypes in small rodents in northeast China and phylogeny and zoonotic implications revisited

Authors: JIANG, SHUNING - Northeast Agricultural University, China; YU, SHUI - Northeast Agricultural University, China; FENG, YAOYU - South China Agricultural University; ZHNAG, LONGXIAN - Henan Agricultural University; Santin-Duran, Monica; XIAO, LIHUA - South China Agricultural University; LI, WEI - Northeast Agricultural University, China

Submitted to: ACTA TROPICA
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/23/2024
Publication Date: 2/24/2024
Citation: Jiang, S., Yu, S., Feng, Y., Zhnag, L., Santin, M., Xiao, L., Li, W. 2024. Widespread distribution of human-infective Enterocytozoon bieneusi genotypes in small rodents in northeast China and phylogeny and zoonotic implications revisited. ACTA TROPICA. 253: Article e107160. https://doi.org/10.1016/j.actatropica.2024.107160.
DOI: https://doi.org/10.1016/j.actatropica.2024.107160

Interpretive Summary: Microsporidia consists of a diverse group of obligate intracellular spore-forming parasites that infect a wide range of animals. Among them, Enterocytozoon bieneusi is the most frequently reported Microsporidia species in humans and animals representing a global public and veterinary health concern. Enterocytozoon bieneusi has been recognized to contain a great deal of diversity at the sequence level with over 500 genotypes in 11 phylogenetic groups. Rodents can also act as the carriers of E. bieneusi and can be a source of infection to humans. However, the role of rodents in transmission of El bieneusi is still unclear. To fill that gap, fecal samples from rodents were collected and screened for the presence of E. bieneusi. The parasite was present in 15 %, 60%, and 7% of the gray squirrels, guinea pigs, and rats examined. Six known genotypes (EbpB, SCC-1, SCC-2, D, S7, and HLJ-CP1) and two novel genotypes (NESQ1 and NEGP1) were identified. Widespread distribution of human infective S7 and D genotypes indicates that rodents are a zoonotic reservoir of microsporidiosis. This information is useful to other scientists, veterinarians, and public health agencies to understand the potential role of rodents in transmission of this parasite to humans.

Technical Abstract: Enterocytozoon bieneusi features high genetic diversity among host species and environmental sources and over 500 genotypes in 11 phylogenetic groups have been defined. Here we investigated 291 small rodents in Heilongjiang province, northeast China, for the presence of E. bieneusi by PCR of the ribosomal internal transcribed spacer (ITS). Nine of 60 (15.0%) gray squirrels from a park in Harbin, 120 of 201 (59.7%) guinea pigs from a pet shop in Harbin, and two of 30 (6.7%) peridomestic rats from a pasture in Qiqihar were positive for the parasite. Six known genotypes (EbpB, SCC-1, SCC-2, D, S7 and HLJ-CP1) and two novel genotypes (NESQ1 and NEGP1) were identified by sequence analysis of the ITS, with EbpB, SCC-1, SCC-2 and NESQ1 found in squirrels, D, S7 and NEGP1 in guinea pigs, and EbpB and HLJ-CP1 in rats. Widespread distribution of human-infective Group 10 genotype S7 and Group 1 genotype D in guinea pigs raised our concerns about the importance of pet animals as zoonotic reservoirs of microsporidiosis. Co-occurrence of Group 1 genotypes D and HLJ-CP1 in cancer patients and rodents in Heilongjiang indicated a possibility of zoonotic transmission. The host range of Group 1 genotype EbpB previously considered pig-adapted was extended. A potential variant of genotype S7, namely NESQ1, went into the existing Group 10 in phylogenetic analysis. The other new genotype, NEGP1, was clustered in an undefined clade we proposed as Group 15. With the emerging epidemiologic evidence, the host specificity of existing E. bieneusi genotypes is now being challenged.