Cyclospora cayetanensis comprises at least 3 species that cause human cyclosporiasis

• Type of Material: Article
• Authors: Joel Leonard Nicholas Barratt, Centers for Disease Control and Prevention, Atlanta; John Shen, Centers for Disease Control and Prevention, Atlanta; Katelyn Houghton, Centers for Disease Control and Prevention, Atlanta; Travis Richins, Centers for Disease Control and Prevention, Atlanta; Sarah GH Sapp, Centers for Disease Control and Prevention, Atlanta; Vitaliano Cama, Centers for Disease Control and Prevention, Atlanta; Micheal J Arrowood, Centers for Disease Control and Prevention, Atlanta; Anne Straily, Centers for Disease Control and Prevention, Atlanta; Yvonne Qvarnstrom, Centers for Disease Control and Prevention, Atlanta
• Language: English
• Date: 2023-03-01
• Publisher: Cambridge University Press (CUP)
• Publication Version: Final Published Version
• Copyright Statement: © The Author(s) 2022
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1017/S003118202200172X
• Title of Journal or Parent Work: PARASITOLOGY
• Volume: 150
• Issue: 3
• Start Page: 269
• End Page: 285
• Grant/Funding Information: The authors acknowledge the CDC's Office of Advanced Molecular Detection for their financial support of this work.
• Keywords: Cyclospora ashfordi; Cyclospora henanensis; Cyclospora cayetanensis; genotyping; epidemiology; speciation
• Research Categories: Health Sciences, Public Health

Abstract

The apicomplexan parasite Cyclospora cayetanensis causes seasonal foodborne outbreaks of the gastrointestinal illness cyclosporiasis. Prior to the coronavirus disease-2019 pandemic, annually reported cases were increasing in the USA, leading the US Centers for Disease Control and Prevention to develop a genotyping tool to complement cyclosporiasis outbreak investigations. Thousands of US isolates and 1 from China (strain CHN_HEN01) were genotyped by Illumina amplicon sequencing, revealing 2 lineages (A and B). The allelic composition of isolates was examined at each locus. Two nuclear loci (CDS3 and 360i2) distinguished lineages A and B. CDS3 had 2 major alleles: 1 almost exclusive to lineage A and the other to lineage B. Six 360i2 alleles were observed – 2 exclusive to lineage A (alleles A1 and A2), 2 to lineage B (B1 and B2) and 1 (B4) was exclusive to CHN_HEN01 which shared allele B3 with lineage B. Examination of heterozygous genotypes revealed that mixtures of A- and B-type 360i2 alleles occurred rarely, suggesting a lack of gene flow between lineages. Phylogenetic analysis of loci from whole-genome shotgun sequences, mitochondrial and apicoplast genomes, revealed that CHN_HEN01 represents a distinct lineage (C). Retrospective examination of epidemiologic data revealed associations between lineage and the geographical distribution of US infections plus strong temporal associations. Given the multiple lines of evidence for speciation within human-infecting Cyclospora, we provide an updated taxonomic description of C. cayetanensis, and describe 2 novel species as aetiological agents of human cyclosporiasis: Cyclospora ashfordi sp. nov. and Cyclospora henanensis sp. nov. (Apicomplexa: Eimeriidae).