Sympatric recombination in zoonotic Cryptosporidium leads to emergence of populations with modified host preference

Authors: WANG, TIANPENG - China Agricultural University; GUO, YAQIONG - South China Agricultural University; ROELLING, DAWN - Centers For Disease Control And Prevention (CDC) - United States; LI, NA - South China Agricultural University; Santin-Duran, Monica; LOMBARD, JASON - Animal And Plant Health Inspection Service (APHIS); KVAC, MARTIN - Academy Of Sciences Of The Czech Republic (ASCR); NAGUIB, DOAA - Mansoura University; ZHANG, ZIDING - China Agricultural University; FENG, YAOYU - South China Agricultural University; XIAO, LIHUA - South China Agricultural University

Submitted to: Nature Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/29/2022
Publication Date: 7/1/2022
Citation: Wang, T., Guo, Y., Roelling, D.M., Li, N., Santin, M., Lombard, J., Kvac, M., Naguib, D., Zhang, Z., Feng, Y., Xiao, L. 2022. Sympatric recombination in zoonotic Cryptosporidium leads to emergence of populations with modified host preference. Nature Microbiology. 39(7). Article e150msac150. https://doi.org/10.1093/molbev/msac150.
DOI: https://doi.org/10.1093/molbev/msac150

Interpretive Summary: Genetic recombination plays a critical role in the emergence of novel virulent pathogens. In this study, we tested the hypothesis that recombination between sympatric ancestral populations leads to the emergence of divergent variants of the zoonotic parasite Cryptosporidium parvum with modified host ranges. Comparative genomic analyses of 101 isolates have identified seven subpopulations of C. parvum isolated by distance. They appear to be decedents of two ancestral populations, IIa in northwestern Europe and IId from southwestern Asia. Sympatric recombination is seen only in areas with both ancestral subtypes, leading to the emergence of new subpopulations with mosaic genomes and modified host preference. Subtelomeric genes appear to be involved in the adaptive selection of the subpopulations and copy number variations of genes encoding invasion-associated proteins are associated with modified host ranges. These observations reveal ancestral origins of zoonotic C. parvum and suggest that pathogen import through modern animal farming drives the emergence of divergent subpopulations of C. parvum with modified host preference.The full-length SSU rRNA reference sequences generated in this study provide essential new data to study and understand the relationships between the genetic complexity of Blastocystis and its host specificity, pathogenicity, and epidemiology. This information should be useful to other scientists and public health agencies working on Blastocystis.

Technical Abstract: Genetic recombination plays a critical role in the emergence of pathogens with phenotypes such as drug resistance, virulence, and host adaptation. Here, we tested the hypothesis that recombination between sympatric ancestral populations leads to the emergence of divergent variants of the zoonotic parasite Cryptosporidium parvum with modified host ranges. Comparative genomic analyses of 101 isolates have identified seven subpopulations isolated by distance. They appear to be descendants of two ancestral populations, IIa in northwestern Europe and IId from southwestern Asia. Sympatric recombination in areas with both ancestral subtypes and subsequent selective sweeps have led to the emergence of new subpopulations with mosaic genomes and modified host preference. Subtelomeric genes could be involved in the adaptive selection of subpopulations, while copy number variations of genes encoding invasion-associated proteins are potentially associated with modified host ranges. These observations reveal ancestral origins of zoonotic C. parvum and suggest that pathogen import through modern animal farming might promote the emergence of divergent subpopulations of C. parvum with modified host preference.