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PreprintCited by 23Parasitic Infections and DiagnosticsViral gastroenteritis research and epidemiologyGenetic diversity and population structure

Global population genomics of two subspecies of Cryptosporidium hominis during 500 years of evolution

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Tichkule, Swapnil, Cacciò, Simone M., Robinson, Guy, Chalmers, Rachel M., Mueller, Ivo, Emery-Corbin, Samantha J., Eibach, Daniel, Tyler, Kevin M., van Oosterhout, Cock, Jex, Aaron R.·2021·Molecular Biology and Evolution
DOI 10.1101/2021.09.09.459610PMC PMC9004413

Preprint — published as 10.1093/molbev/msac056 · Paper page

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Abstract

Cryptosporidiosis is a major global health problem and a primary cause of diarrhoea, particularly in young children in low- and middle-income countries (LMICs). The zoonotic Cryptosporidium parvum and anthroponotic C. hominis cause most human infections. Here, we present a comprehensive whole-genome study of C. hominis , comprising 114 isolates from 16 countries within five continents. We detect two lineages with distinct biology and demography, which diverged circa 500 years ago. We consider these lineages two subspecies and propose the names C. hominis hominis and C. hominis aquapotentis ( gp60 subtype IbA10G2). In our study, C. h. hominis is almost exclusively represented by isolates from LMICs in Africa and Asia and appears to have undergone recent population contraction. In contrast, C. h. aquapotentis was found in high-income countries, mainly in Europe, North America and Oceania, and appears to be expanding. Notably, C. h. aquapotentis is associated with high rates of direct human-to-human transmission, which may explain its success in countries with well-developed environmental sanitation infrastructure. Intriguingly, we detected genomic regions of introgression following secondary contact between the subspecies. This resulted in high diversity and divergence in genomic islands of putative virulence genes (GIPVs), including muc5 (CHUDEA2_430) and a hypothetical protein (CHUDEA6_5270). This diversity is maintained by balancing selection, suggesting a coevolutionary arms race with the host. Lastly, we find that recent gene flow from C. h. aquapotentis to C. h. hominis , likely associated with increased human migration, may be driving evolution of more virulent C. hominis variants.

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Authors
Tichkule, S., Cacciò, S. M., Robinson, G., Chalmers, R. M., Mueller, I., Emery-Corbin, S. J., Eibach, D., Tyler, K. M., van Oosterhout, C., & Jex, A. R.
Affiliations
  • The University of Melbourne (AU)
  • Istituto Superiore di Sanità (IT)
  • Singleton Hospital (GB)
  • German Center for Infection Research (DE)
  • University of East Anglia (GB)
Corresponding author
  • Tichkule, Swapnil
  • Cacciò, Simone M.
  • van Oosterhout, Cock
  • Jex, Aaron R.
ORCID
Venue
Molecular Biology and Evolution
Publisher
openRxiv
Published
2021-09-09
Volume
39
Issue
4
ISSN
0737-4038 (ISSN-L)
DOI
10.1101/2021.09.09.459610
PMC
PMC9004413
OpenAlex
W4220870828
Cited by
23
References
1
Citations by year
2026: 3 · 2025: 5 · 2024: 3 · 2023: 6 · 2022: 6
FWCI
3.98
Type
journal article
Language
en
Open access
Licence
cc-by-nc
Locations
  • Molecular Biology and Evolution (publishedVersion, cc-by-nc)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • UEA Digital Repository (University of East Anglia) (acceptedVersion)
  • Minerva Access (University of Melbourne) (submittedVersion, cc-by-nc)
Funders
  • Australian Government
  • European Commission (2014‐2020, 643476, HORIZON2020)
  • Australian Society for Parasitology
  • Monash University
  • Earth and Life Systems Alliance
  • Medical Research Council
  • National Health and Medical Research Council (1194330)
  • European Regional Development Fund (2014-2020’, Interreg 2 Seas programme 2014-2020, 2S05-043)
  • Interreg (2S05-043 H4DC, 2014-2020)
Topics
  • Life Sciences › Immunology and Microbiology › Parasitology › Parasitic Infections and Diagnostics
  • Health Sciences › Medicine › Infectious Diseases › Viral gastroenteritis research and epidemiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
Keywords
Cryptosporidium hominis, cryptosporidiosis, subspecies differentiation, population genomics, population contraction, human-to-human transmission, introgression, virulence genes, balancing selection, host-pathogen coevolution, gene flow, low- and middle-income countries
MeSH terms
Child, Child, Preschool, Cryptosporidiosis, Cryptosporidium, Genotype, Humans, DNA, Protozoan, Genome, Metagenomics

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