Comparative genomics of Cryptosporidium parvum reveals the emergence of an outbreak-associated population in Europe and its spread to the United States

The zoonotic parasite Cryptosporidium parvum is a global cause of gastrointestinal disease in humans and ruminants. Sequence analysis of the highly polymorphic gp60 gene enabled the classification of C. parvum isolates into multiple groups (e.g., IIa, IIc, Id) and a large number of subtypes. In Euro...

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Published inGenome research Vol. 34; no. 6; pp. 877 - 887
Main Authors Bellinzona, Greta, Nardi, Tiago, Castelli, Michele, Batisti Biffignandi, Gherard, Adjou, Karim, Betson, Martha, Blanchard, Yannick, Bujila, Ioana, Chalmers, Rachel, Davidson, Rebecca, D'Avino, Nicoletta, Enbom, Tuulia, Gomes, Jacinto, Karadjian, Gregory, Klotz, Christian, Östlund, Emma, Plutzer, Judith, Rimhanen-Finne, Ruska, Robinson, Guy, Sannella, Anna Rosa, Sroka, Jacek, Stensvold, Christen Rune, Troell, Karin, Vatta, Paolo, Zalewska, Barbora, Bandi, Claudio, Sassera, Davide, Cacciò, Simone M.
Format Journal Article
LanguageEnglish
Published United States Cold Spring Harbor Laboratory Press 01.06.2024
Subjects
Online AccessGet full text
ISSN1088-9051
1549-5469
1549-5469
DOI10.1101/gr.278830.123

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Abstract The zoonotic parasite Cryptosporidium parvum is a global cause of gastrointestinal disease in humans and ruminants. Sequence analysis of the highly polymorphic gp60 gene enabled the classification of C. parvum isolates into multiple groups (e.g., IIa, IIc, Id) and a large number of subtypes. In Europe, subtype IIaA15G2R1 is largely predominant and has been associated with many water- and food-borne outbreaks. In this study, we generated new whole-genome sequence (WGS) data from 123 human- and ruminant-derived isolates collected in 13 European countries and included other available WGS data from Europe, Egypt, China, and the United States (n = 72) in the largest comparative genomics study to date. We applied rigorous filters to exclude mixed infections and analyzed a data set from 141 isolates from the zoonotic groups IIa (n = 119) and IId (n = 22). Based on 28,047 high-quality, biallelic genomic SNPs, we identified three distinct and strongly supported populations: Isolates from China (IId) and Egypt (IIa and IId) formed population 1; a minority of European isolates (IIa and IId) formed population 2; and the majority of European (IIa, including all IIaA15G2R1 isolates) and all isolates from the United States (IIa) clustered in population 3. Based on analyses of the population structure, population genetics, and recombination, we show that population 3 has recently emerged and expanded throughout Europe to then, possibly from the United Kingdom, reach the United States, where it also expanded. The reason(s) for the successful spread of population 3 remain elusive, although genes under selective pressure uniquely in this population were identified.
AbstractList The zoonotic parasite is a global cause of gastrointestinal disease in humans and ruminants. Sequence analysis of the highly polymorphic gene enabled the classification of isolates into multiple groups (e.g., IIa, IIc, Id) and a large number of subtypes. In Europe, subtype IIaA15G2R1 is largely predominant and has been associated with many water- and food-borne outbreaks. In this study, we generated new whole-genome sequence (WGS) data from 123 human- and ruminant-derived isolates collected in 13 European countries and included other available WGS data from Europe, Egypt, China, and the United States (n = 72) in the largest comparative genomics study to date. We applied rigorous filters to exclude mixed infections and analyzed a data set from 141 isolates from the zoonotic groups IIa (n = 119) and IId (n = 22). Based on 28,047 high-quality, biallelic genomic SNPs, we identified three distinct and strongly supported populations: Isolates from China (IId) and Egypt (IIa and IId) formed population 1; a minority of European isolates (IIa and IId) formed population 2; and the majority of European (IIa, including all IIaA15G2R1 isolates) and all isolates from the United States (IIa) clustered in population 3. Based on analyses of the population structure, population genetics, and recombination, we show that population 3 has recently emerged and expanded throughout Europe to then, possibly from the United Kingdom, reach the United States, where it also expanded. The reason(s) for the successful spread of population 3 remain elusive, although genes under selective pressure uniquely in this population were identified.
The zoonotic parasite Cryptosporidium parvum is a global cause of gastrointestinal disease in humans and ruminants. Sequence analysis of the highly polymorphic gp60 gene enabled the classification of C. parvum isolates into multiple groups (e.g., IIa, IIc, Id) and a large number of subtypes. In Europe, subtype IIaA15G2R1 is largely predominant and has been associated with many water- and food-borne outbreaks. In this study, we generated new whole-genome sequence (WGS) data from 123 human- and ruminant-derived isolates collected in 13 European countries and included other available WGS data from Europe, Egypt, China, and the United States (n = 72) in the largest comparative genomics study to date. We applied rigorous filters to exclude mixed infections and analyzed a data set from 141 isolates from the zoonotic groups IIa (n = 119) and IId (n = 22). Based on 28,047 high-quality, biallelic genomic SNPs, we identified three distinct and strongly supported populations: Isolates from China (IId) and Egypt (IIa and IId) formed population 1; a minority of European isolates (IIa and IId) formed population 2; and the majority of European (IIa, including all IIaA15G2R1 isolates) and all isolates from the United States (IIa) clustered in population 3. Based on analyses of the population structure, population genetics, and recombination, we show that population 3 has recently emerged and expanded throughout Europe to then, possibly from the United Kingdom, reach the United States, where it also expanded. The reason(s) for the successful spread of population 3 remain elusive, although genes under selective pressure uniquely in this population were identified.
The zoonotic parasite Cryptosporidium parvum is a global cause of gastrointestinal disease in humans and ruminants. Sequence analysis of the highly polymorphic gp60 gene enabled the classification of C. parvum isolates into multiple groups (e.g., IIa, IIc, Id) and a large number of subtypes. In Europe, subtype IIaA15G2R1 is largely predominant and has been associated with many water- and food-borne outbreaks. In this study, we generated new whole-genome sequence (WGS) data from 123 human- and ruminant-derived isolates collected in 13 European countries and included other available WGS data from Europe, Egypt, China, and the United States (n = 72) in the largest comparative genomics study to date. We applied rigorous filters to exclude mixed infections and analyzed a data set from 141 isolates from the zoonotic groups IIa (n = 119) and IId (n = 22). Based on 28,047 high-quality, biallelic genomic SNPs, we identified three distinct and strongly supported populations: Isolates from China (IId) and Egypt (IIa and IId) formed population 1; a minority of European isolates (IIa and IId) formed population 2; and the majority of European (IIa, including all IIaA15G2R1 isolates) and all isolates from the United States (IIa) clustered in population 3. Based on analyses of the population structure, population genetics, and recombination, we show that population 3 has recently emerged and expanded throughout Europe to then, possibly from the United Kingdom, reach the United States, where it also expanded. The reason(s) for the successful spread of population 3 remain elusive, although genes under selective pressure uniquely in this population were identified.
The zoonotic parasite Cryptosporidium parvum is a global cause of gastrointestinal disease in humans and ruminants. Sequence analysis of the highly polymorphic gp60 gene enabled the classification of C. parvum isolates into multiple groups (e.g., IIa, IIc, Id) and a large number of subtypes. In Europe, subtype IIaA15G2R1 is largely predominant and has been associated with many water- and food-borne outbreaks. In this study, we generated new whole-genome sequence (WGS) data from 123 human- and ruminant-derived isolates collected in 13 European countries and included other available WGS data from Europe, Egypt, China, and the United States (n = 72) in the largest comparative genomics study to date. We applied rigorous filters to exclude mixed infections and analyzed a data set from 141 isolates from the zoonotic groups IIa (n = 119) and IId (n = 22). Based on 28,047 high-quality, biallelic genomic SNPs, we identified three distinct and strongly supported populations: Isolates from China (IId) and Egypt (IIa and IId) formed population 1; a minority of European isolates (IIa and IId) formed population 2; and the majority of European (IIa, including all IIaA15G2R1 isolates) and all isolates from the United States (IIa) clustered in population 3. Based on analyses of the population structure, population genetics, and recombination, we show that population 3 has recently emerged and expanded throughout Europe to then, possibly from the United Kingdom, reach the United States, where it also expanded. The reason(s) for the successful spread of population 3 remain elusive, although genes under selective pressure uniquely in this population were identified.The zoonotic parasite Cryptosporidium parvum is a global cause of gastrointestinal disease in humans and ruminants. Sequence analysis of the highly polymorphic gp60 gene enabled the classification of C. parvum isolates into multiple groups (e.g., IIa, IIc, Id) and a large number of subtypes. In Europe, subtype IIaA15G2R1 is largely predominant and has been associated with many water- and food-borne outbreaks. In this study, we generated new whole-genome sequence (WGS) data from 123 human- and ruminant-derived isolates collected in 13 European countries and included other available WGS data from Europe, Egypt, China, and the United States (n = 72) in the largest comparative genomics study to date. We applied rigorous filters to exclude mixed infections and analyzed a data set from 141 isolates from the zoonotic groups IIa (n = 119) and IId (n = 22). Based on 28,047 high-quality, biallelic genomic SNPs, we identified three distinct and strongly supported populations: Isolates from China (IId) and Egypt (IIa and IId) formed population 1; a minority of European isolates (IIa and IId) formed population 2; and the majority of European (IIa, including all IIaA15G2R1 isolates) and all isolates from the United States (IIa) clustered in population 3. Based on analyses of the population structure, population genetics, and recombination, we show that population 3 has recently emerged and expanded throughout Europe to then, possibly from the United Kingdom, reach the United States, where it also expanded. The reason(s) for the successful spread of population 3 remain elusive, although genes under selective pressure uniquely in this population were identified.
Author Chalmers, Rachel
Castelli, Michele
Klotz, Christian
Nardi, Tiago
Sassera, Davide
Robinson, Guy
Blanchard, Yannick
Sroka, Jacek
Rimhanen-Finne, Ruska
Betson, Martha
Vatta, Paolo
Zalewska, Barbora
Bellinzona, Greta
D'Avino, Nicoletta
Bandi, Claudio
Östlund, Emma
Batisti Biffignandi, Gherard
Stensvold, Christen Rune
Gomes, Jacinto
Cacciò, Simone M.
Sannella, Anna Rosa
Troell, Karin
Plutzer, Judith
Davidson, Rebecca
Bujila, Ioana
Adjou, Karim
Enbom, Tuulia
Karadjian, Gregory
AuthorAffiliation 3 Department of Comparative Biomedical Sciences, School of Veterinary Medicine, University of Surrey, Guildford GU2 7AL, United Kingdom
13 Swedish Veterinary Agency, SE-751 89 Uppsala, Sweden
11 National Institute for Agricultural and Veterinary Research, 1300 Lisbon, Portugal
16 Department of Infectious Diseases, Istituto Superiore di Sanità, 00161 Rome, Italy
14 National Institute for Public Education, Budapest, 1007, Hungary
5 Department of Microbiology, Public Health Agency of Sweden, SE-171 82 Solna, Sweden
6 Cryptosporidium Reference Unit, Public Health Wales, Swansea SA2 8QA, United Kingdom
9 Istituto Zooprofilattico Sperimentale dell'Umbria e delle Marche, 06126 Perugia, Italy
8 Norwegian Veterinary Institute, N-1431 Ås, Norway
1 Department of Biology and Biotechnology, University of Pavia, 27100 Pavia, Italy
18 Statens Serum Institut, 2300 Copenhagen, Denmark
2 UMR BIPAR, Anses, Laboratoire de Santé Animale, INRAE, École Nationale Vétérinaire d'Alfort, 94700 Maisons-Alfort, France
20 Depa
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PublicationTitle Genome research
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Snippet The zoonotic parasite Cryptosporidium parvum is a global cause of gastrointestinal disease in humans and ruminants. Sequence analysis of the highly polymorphic...
The zoonotic parasite is a global cause of gastrointestinal disease in humans and ruminants. Sequence analysis of the highly polymorphic gene enabled the...
The zoonotic parasite Cryptosporidium parvum is a global cause of gastrointestinal disease in humans and ruminants. Sequence analysis of the highly polymorphic...
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StartPage 877
SubjectTerms Animals
China - epidemiology
Cryptosporidiosis - epidemiology
Cryptosporidiosis - parasitology
Cryptosporidium parvum
Cryptosporidium parvum - genetics
Disease Outbreaks
Egypt - epidemiology
Epidemics
Europe - epidemiology
Gastrointestinal diseases
Genome, Protozoan
Genomic analysis
Genomics
Genomics - methods
Humans
Life Sciences
Nucleotide sequence
Outbreaks
Phylogeny
Polymorphism, Single Nucleotide
Population genetics
Population structure
Sequence analysis
Single-nucleotide polymorphism
United States - epidemiology
Whole Genome Sequencing - methods
Zoonoses
Title Comparative genomics of Cryptosporidium parvum reveals the emergence of an outbreak-associated population in Europe and its spread to the United States
URI https://www.ncbi.nlm.nih.gov/pubmed/38977307
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https://pubmed.ncbi.nlm.nih.gov/PMC11293552
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