Intra-species diversity and panmictic structure of cryptosporidium parvum populations in cattle farms in Northern Spain

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Ramo, Ana ^a   Quílez, Joaquín ^a   Monteagudo, Luis ^a   Del Cacho, Emilio ^a   Sánchez Acedo, Caridad ^a  

^a UNIVERSITY OF ZARAGOZA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALGORITHM; ALLELE; ARTICLE; BAYES THEOREM; CATTLE FARMING; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; GENE LOCUS; GENETIC VARIABILITY; HAPLOTYPE; INFECTION RATE; LINKAGE ANALYSIS; MIXED INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; SPAIN; SPECIES DIVERSITY; STRUCTURE ANALYSIS; VARIABLE NUMBER OF TANDEM REPEAT; ANIMAL; BOVINE; GENETIC LINKAGE; GENETIC VARIATION; GENETICS; HOST PARASITE INTERACTION; ISOLATION AND PURIFICATION; PARASITOLOGY;

ANIMALS; BAYES THEOREM; CATTLE; CRYPTOSPORIDIUM PARVUM; GENETIC LINKAGE; GENETIC VARIATION; HOST-PARASITE INTERACTIONS; MINISATELLITE REPEATS; SPAIN;

EID: 84959440125     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0148811     Document Type: Article

References (46)

1. Chalmers RM, Katzer F. Looking for Cryptosporidium: the application of advances in detection and diagnosis. Trends Parasitol. 2013; 29: 237-251. doi: 10.1016/j.pt.2013.03.001 PMID: 23566713
2. Drumo R, Widmer G, Morrison LJ, Tait A, Grelloni V, D'Avino N, et al. Evidence of host-associated populations of Cryptosporidium parvum in Italy. Appl Environ Microbiol. 2012; 78: 3523-3529. doi: 10.1128/AEM.07686-11 PMID: 22389374
3. Quílez J, Vergara-Castiblanco C, Monteagudo L, Del Cacho E, Sánchez-Acedo C. Host association of Cryptosporidium parvum populations infecting domestic ruminants in Spain. Appl Environ Microbiol. 2013; 79: 5363-5371. doi: 10.1128/AEM.01168-13 PMID: 23811515
4. Wang R, Zhang L, Axén C, Bjorkman C, Jian F, Amer S, et al. Cryptosporidium parvum IId family: clonal population and dispersal from Western Asia to other geographical regions. Sci Rep. 2014; 4: 4202. doi: 10.1038/srep04208 PMID: 24572610
5. Cacciò SM, de Waele V, Widmer G. Geographical segregation of Cryptosporidium parvum multilocus genotypes in Europe. Infect Genet Evol. 2015; 31: 245-249. doi: 10.1016/j.meegid.2015.02.008 PMID: 25687913
6. Tanriverdi S, Blain JC, Deng B, Ferdig MT, Widmer G. Genetic crosses in the apicomplexan parasite Cryptosporidium parvum define recombination parameters. Mol Microbiol. 2007; 63: 1432-1439. doi: 10.1111/j.1365-2958.2007.05594.x PMID: 17302818
7. Widmer G, Sullivan S. Genomics and population biology of Cryptosporidium species. Parasite Immunol. 2012; 34: 61-71. doi: 10.1111/j.1365-3024.2011.01301.x PMID: 21595702
8. Waldron LS, Power ML. Fluorescence analysis detects gp60 subtype diversity in Cryptosporidium infections. Infect Genet Evol. 2011; 11: 1388-1395. doi: 10.1016/j.meegid.2011.05.008 PMID: 21609784
9. Grinberg A, Biggs PJ, Dukkipati VS, George TT. Extensive intra-host genetic diversity uncovered in Cryptosporidium parvum using Next Generation Sequencing. Infect Genet Evol. 2013; 15: 18-24. doi: 10.1016/j.meegid.2012.08.017 PMID: 22981926
10. Ramo A, Quílez J, Del Cacho E, Sánchez-Acedo C. Optimization of a fragment size analysis tool for identification of Cryptosporidium species and GP60 alleles infecting domestic ruminants. Vet Parasitol. 2014; 205: 466-471. doi: 10.1016/j.vetpar.2014.08.025 PMID: 25224787
11. Ryan U, Fayer R, Xiao L. Cryptosporidium species in humans and animals: current understanding and research needs. Parasitology. 2014; 141: 1667-1685. doi: 10.1017/S0031182014001085 PMID: 25111501
12. García A, Rui-Santa-Quiteria JA, Orden JA, Cid D, Sanz R, Gómez-Bautista M, et al. Rotavirus and concurrent infections with other enteropathogens in neonatal diarrheic diary calves in Spain. Comp Immunol Microbiol Infect Dis. 2000; 23: 175-183. doi: 10.1016/S0147-9571(99)00071-5 PMID: 10855663
13. Castro-Hermida JA, González-Losada YA, Ares-Mazás E. Prevalence of and risk factors involved in the spread of neonatal bovine cryptosporidiosis in Galicia (NW Spain). Vet Parasitol. 2002; 106: 1-10. doi: 10.1016/S0304-4017(02)00036-5 PMID: 11992706
14. Quilez J, Torres E, Chalmers RM, Robinson G, Del Cacho E, Sanchez-Acedo C. Cryptosporidium species and subtype analysis from dairy calves in Spain. Parasitology. 2008; 135: 1613-1620. doi: 10.1017/S0031182008005088 PMID: 18980704
15. Díaz P, Hadfield SJ, Quílez J, Soilán M, López C, Panadero R, et al. Assessment of three methods for multilocus fragment typing of Cryptosporidium parvum from domestic ruminants in North West Spain. Vet Parasitol. 2012; 186: 188-195. doi: 10.1016/j.vetpar.2011.11.039 PMID: 22154970
16. Quílez J, Vergara-Castiblanco C, Monteagudo L, Del Cacho E, Sánchez-Acedo C. Multilocus fragment typing and genetic structure of Cryptosporidium parvum isolates from diarrheic preweaned calves in Spain. Appl Environ Microbiol. 2011; 77: 7779-7786. doi: 10.1128/AEM.00751-11 PMID: 21908632
17. Gatei W, Das P, Dutta P, Sen A, Cama V, Lal AA, et al. Multilocus sequence typing and genetic structure of Cryptosporidium hominis from children in Kolkata, India. Infect Genet Evol. 2007; 7: 197-205. doi: 10.1016/j.meegid.2006.08.006 PMID: 17010677
18. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. Primer3 - new capabilities and interfaces. Nucleic Acids Res. 2012; 40: e115. doi: 10.1093/nar/gks596 PMID: 22730293
19. Quílez J, Hadfield SJ, Ramo A, Vergara-Castiblanco C, Chalmers RM. Validation of fragment analysis by capillary electrophoresis to resolve mixed infections by Cryptospordium parvum subpopulations. Parasitol Res. 2014; 113: 1821-1825. doi: 10.1007/s00436-014-3828-6 PMID: 24609235
20. Tanrivendi S, Widmer G. Different evolution of repetitive sequences in Cryptosporidium parvum and Cryptsoporidium hominis. Infect Genet Evol. 2006; 6:113-122. doi: 10.1016/j.meegid.2005.02.002 PMID: 16503512
21. Mallon M, MacLeod A, Wastling J, Smith H, Reilly B, Tait A. Population structures and the role of genetic Exchange in the zoonotic pathogen Cryptosporidium parvum. J Mol Evol. 2003; 56: 407-417. doi: 10.1007/s00239-002-2412-3 PMID: 12664161
22. Chalmers RM, Ferguson C, Cacciò S, Gasser RB, Abs El Osta YG, Heijnen L, et al. Direct comparison of selected methods for genetic categorisation of Cryptosporidium parvum and Cryptosporidium hominis species. Int J Parasitol. 2005; 35: 197-410. doi: 10.1016/j.ijpara.2005.01.001
23. Hunter PR, Gaston MA. Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J Clin Microbiol. 1988; 26: 2465-2466. PMID: 3069867
24. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol. 2004; 186: 1518-1530. doi: 10.1128/JB.186.5.1518-1530.2004 PMID: 14973027
25. Haubold B, Hudson RR. LIAN 3.0: detecting linkage disequilibrium in multilocus data. Linkage Analysis. Bioinformatics. 2000; 16: 847-548. doi: 10.1093/bioinformatics/16.9.847 PMID: 11108709
26. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000; 155: 945-959. doi: 10.1186/s12862-015-0488-9 PMID: 10835412
27. Cockerham CC, Weir BS. Estimation of gene flow from F-Statistics. 1993; 47: 855-863. doi: 10.2307/ 2410189
28. Robinson G, Chalmers RM. Assessment of polymorphic genetic markers for multi-locus typing of Cryptosporidium parvum and Cryptosporidium hominis. Exp Parasitol. 2012; 132: 200-215. doi: 10.1016/j. exppara.2012.06.016 PMID: 22781277
29. De Waele V, Van den Broeck F, Huyse T, McGrath G, Higgins I, Speybroeck N, et al. Panmictic Structure of the Cryptosporidium parvum population in irish calves: influence of prevalence and host movement. Appl Environ Microbiol. 2013; 79: 2534-2541. doi: 10.1128/AEM.03613-12 PMID: 23396342
30. Hotchkiss EJ, Gilray JA, Brennan ML, Christley RM, Morrison LJ, Jonsson NN, et al. Development of a framework for genotyping bovine-derived Cryptosporidium parvum, using a multilocus fragment typing tool. Parasit Vectors. 2015; 8: 500. doi: 10.1186/s13071-015-1107-8 PMID: 26427625
31. Morrison LJ, Mallon ME, Smith HV, MacLeod A, Xiao L, Tait A. The population structure of the Cryptosporidium parvum population in Scotland: a complex picture. Infect Genet Evol. 2008; 8: 121-129. doi: 10.1016/j.meegid.2007.10.010 PMID: 18077222
32. Herges GR, Widmer G, Clark ME, Khan E, Giddings CW, Brewer M, et al. Evidence that Cryptosporidium parvum populations are panmictic and unstructured in the upper Midwest of the United States. Appl Environ Microbiol. 2012; 78: 8096-8101. doi: 10.1128/AEM.02105-12 PMID: 22983961
33. Ng J, MacKenzie B, Ryan U. Longitudinal multi-locus molecular characterization of sporadic Australian human clinical cases of cryptosporidiosis from 2005 to 2008. Exp Parasitol. 2010; 125: 348-356. Epub 2010/03/04. doi: 10.1016/j.exppara.2010.02.017 PMID: 20206624
34. Ramo A, Quílez J, Vergara-Castiblanco C, Monteagudo L, Del Cacho E, Clavel A. Multilocus typing and population structure of Cryptosporidium from children in Zaragoza, Spain. Infect Genet Evol. 2015; 31: 190-197. doi: 10.1016/j.meegid.2015.01.023
35. Hunter PR, Hadfield SJ, Wilkinson D, Lake IR, Harrison FCD, Chalmers RM. Subtypes of Cryptosporidium parvum in humans and disease risk. Emerg Infect Dis. 2007; 13: 82-88. doi: 10.3201/eid1301. 060481 PMID: 17370519
36. Mallon M, MacLeod A, Wastling J, Smith H, Reilly B, Tait A. Multilocus genotyping of Cryptosporidium parvum Type 2: population genetics and sub-structuring. Infect Genet Evol. 2003; 3: 207-218. doi: 10.1016/S1567-1348(03)00089-3 PMID: 14522184
37. Mercado R, Peña S, Ozaki LS, Fredes F, Godoy J. Multiple Cryptosporidium parvum subtypes detected in a unique isolate of a Chilean neonatal calf with diarrhea. Parasitol Res. 2015; 114: 1985-1988. doi: 10.1007/s00436-015-4364-8 PMID: 25673079
38. Brook EJ, Anthony Hart C, French NP, Christley RM. Molecular epidemiology of Cryptosporidium subtypes in cattle in England. Vet J. 2009; 179: 378-382 PMID: 18083583
39. Peng MM, Wilson ML, Holland RE, Meshnick SR, Xiao L. Genetic diversity of Cryptosporidium spp. in cattle in Michigan: implications for understanding the transmission dynamics. Parasitol Res. 2003; 90: 175-180. doi: 10.1007/s00436-003-0834-5 PMID: 12783304
40. Tanriverdi S, Markovics A, Arslan MO, Itik A, Shkap V, Widmer G. Emergence of distinct genotypes of Cryptosporidium parvum in structured host populations. Appl Environ Microbiol. 2006; 72: 2507-2513. doi: 10.1128/AEM.72.4.2507-2513.2006 PMID: 16597950
41. Feng Y, Torres E, Li N, Wang L, Bowman D, Xiao L. Population genetic characterisation of dominant Cryptosporidium parvum subtype IIaA15G2R1. Int J Parasitol. 2013; 43: 1141-1147. doi: 10.1016/j. ijpara.2013.09.002 PMID: 24126186
42. Li N, Xiao L, Cama VA, Ortega Y, Gilman RH, Guo M, Feng Y. Genetic recombination and Cryptosporidium hominis virulent subtype IbA10G2. Emerg Infect Dis. 2013; 19: 1573-1582. doi: 10.3201/ eid1910.121361 PMID: 24050210
43. Feng Y, Tiao N, Li N, Hlavsa M, Xiao L. Multilocus Sequence Typing of an Emerging Cryptosporidium hominis Subtype in the United States. J Clin Microbiol. 2014; 52: 524-530. doi: 10.1128/JCM.02973-13 PMID: 24478483
44. Guo Y, Tang K, Rowe LA, Li N, Roellig DM, Knipe K, Frace M, Yang C, Feng Y, Xiao L. Comparative genomic analysis reveals occurrence of genetic recombination in virulent Cryptosporidium hominis subtypes and telomeric gene duplications in Cryptosporidium parvum. BMC Genomics. 2015; 16: 1-18. doi: 10.1186/s12864-015-1517-1 PMID: 25903370
45. Tanriverdi S, Grinberg A, Chalmers RM, Hunter PR, Petrovic Z, Akiyoshi DE, London E, Zhang L, Tzipori S, Tumwine JK, Widmer G. Inferences about the global population structures of Cryptosporidium parvum and Cryptosporidium hominis. Appl Environ Microbiol. 2008; 74: 7227-7234. doi: 10.1128/ AEM.01576-08 PMID: 18836013
46. Castro-Hermida JA, González-Losada YA, Mezo-Menéndez M, Ares-Mazás E. A study of cryptosporidiosis in a cohort of neonatal calves. Vet Parasitol. 2002; 106: 11-17. doi: 10.1016/S0304-4017(02) 00038-9 PMID: 11992707