Comparative genomics of Cryptosporidium parvum reveals the emergence of an outbreak-associated population in Europe and its spread to the United States
Greta Bellinzona
(1)
,
Tiago Nardi
(1)
,
Michele Castelli
(1)
,
Gherard Batisti Biffignandi
(1)
,
Karim Adjou
(2)
,
Martha Betson
(3)
,
Yannick Blanchard
(4)
,
Ioana Bujila
(5)
,
Rachel Chalmers
(6, 7)
,
Rebecca Davidson
(8)
,
Nicoletta d'Avino
(9)
,
Tuulia Enbom
(10)
,
Jacinto Gomes
(11)
,
Gregory Karadjian
(2)
,
Christian Klotz
(12)
,
Emma Östlund
(13)
,
Judith Plutzer
(14)
,
Ruska Rimhanen-Finne
(15)
,
Guy Robinson
(6, 7)
,
Anna Rosa Sannella
(16)
,
Jacek Sroka
(17)
,
Christen Rune Stensvold
(18)
,
Karin Troell
(13)
,
Paolo Vatta
(16)
,
Barbora Zalewska
(19)
,
Claudio Bandi
(20)
,
Davide Sassera
(1, 21)
,
Simone Cacciò
(16)
1
UNIPV -
Università degli Studi di Pavia = University of Pavia
2 BIPAR - Biologie moléculaire et immunologie parasitaires et fongiques
3 UNIS - University of Surrey
4 GVB - Génétique Virale et Biosécurité
5 Public Health Agency of Sweden
6 Public Health Wales [Cardiff, Royaume uni]
7 Swansea University
8 Norwegian Veterinary Institute [Bergen]
9 IZSUM - Istituto Zooprofilattico Sperimentale dell'Umbria e delle Marche
10 Finnish Food Authority
11 INIAV - Instituto Nacional de Investigação Agrária e Veterinária = National Institute for Agrarian and Veterinary Research [Oeiras, Portugal]
12 RKI - Robert Koch Institute [Berlin]
13 SVA - National Veterinary Institute [Uppsala]
14 OKI - National Institute for Public Education
15 FIHW - Finnish Institute for Health and Welfare
16 ISS - Istituto Superiore di Sanità = National Institute of Health
17 NVRI - National Veterinary Research Institute [Pulawy, Pologne]
18 Statens Serum Institut [Copenhagen]
19 VRI - Veterinary Research Institute [Brno]
20 UNIMI - Università degli Studi di Milano = University of Milan
21 IRCCS Pavia - ICS Maugeri - Istituti Clinici Scientifici Maugeri [Pavia]
2 BIPAR - Biologie moléculaire et immunologie parasitaires et fongiques
3 UNIS - University of Surrey
4 GVB - Génétique Virale et Biosécurité
5 Public Health Agency of Sweden
6 Public Health Wales [Cardiff, Royaume uni]
7 Swansea University
8 Norwegian Veterinary Institute [Bergen]
9 IZSUM - Istituto Zooprofilattico Sperimentale dell'Umbria e delle Marche
10 Finnish Food Authority
11 INIAV - Instituto Nacional de Investigação Agrária e Veterinária = National Institute for Agrarian and Veterinary Research [Oeiras, Portugal]
12 RKI - Robert Koch Institute [Berlin]
13 SVA - National Veterinary Institute [Uppsala]
14 OKI - National Institute for Public Education
15 FIHW - Finnish Institute for Health and Welfare
16 ISS - Istituto Superiore di Sanità = National Institute of Health
17 NVRI - National Veterinary Research Institute [Pulawy, Pologne]
18 Statens Serum Institut [Copenhagen]
19 VRI - Veterinary Research Institute [Brno]
20 UNIMI - Università degli Studi di Milano = University of Milan
21 IRCCS Pavia - ICS Maugeri - Istituti Clinici Scientifici Maugeri [Pavia]
Greta Bellinzona
- Fonction : Auteur
- PersonId : 1399820
- ORCID : 0000-0001-7050-8940
Tiago Nardi
- Fonction : Auteur
- PersonId : 1170197
- ORCID : 0000-0002-1248-9873
Michele Castelli
- Fonction : Auteur
- PersonId : 1399821
- ORCID : 0000-0003-2177-5772
Karim Adjou
- Fonction : Auteur
- PersonId : 1178854
- IdHAL : enva-07072023
- ORCID : 0000-0003-4043-0876
- IdRef : 135403812
Gregory Karadjian
- Fonction : Auteur
- PersonId : 1238524
- IdHAL : gregory-karadjian
- ORCID : 0000-0001-8224-521X
- IdRef : 194671720
Davide Sassera
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- Fonction : Auteur correspondant
- PersonId : 1095979
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Simone Cacciò
- Fonction : Auteur correspondant
Résumé
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.
