Genome-scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection

PLoS Pathogens

Volumn 5, Issue 5, 2009, Pages

  Llewellyn, Martin S ^a   Miles, Michael A ^a   Carrasco, Hernan J ^b   Lewis, Michael D ^a   Yeo, Matthew ^a   Vargas, Jorge ^c   Torrico, Faustino ^d   Diosque, Patricio ^e   Valente, Vera ^f   Valente, Sebastiao A ^f   Gaunt, Michael W ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b UNIVERSIDAD CENTRAL DE VENEZUELA   (Venezuela)

^c Centro Nacional de Enfermedades Tropicales   (Bolivia)

^d UNIVERSIDAD MAYOR DE SAN SIMÓN   (Bolivia)

^e UNIVERSIDAD NACIONAL DE SALTA   (Argentina)

^f INSTITUTO EVANDRO CHAGAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOGEOGRAPHY; GENE LOCUS; GENETIC LINKAGE; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOME; GENOTYPE; GEOGRAPHIC DISTRIBUTION; HETEROZYGOSITY; HOMOZYGOSITY; INFECTION; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PHYLOGENY; POPULATION STRUCTURE; RESERVOIR; SOUTH AMERICA; TRYPANOSOMA CRUZI; VENEZUELA; ANIMAL; CHAGAS DISEASE; EPIDEMIOLOGY; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENETICS; GENOMICS; HUMAN; METHODOLOGY; PARASITOLOGY; TOPOGRAPHY;

MAMMALIA; TRYPANOSOMA CRUZI;

MICROSATELLITE DNA;

ANIMALS; CHAGAS DISEASE; EPIDEMIOLOGY, MOLECULAR; GENE FREQUENCY; GENETIC VARIATION; GENOMICS; GENOTYPE; HUMANS; LINKAGE DISEQUILIBRIUM; MICROSATELLITE REPEATS; PHYLOGENY; TOPOGRAPHY, MEDICAL; TRYPANOSOMA CRUZI;

EID: 67249129142     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000410     Document Type: Article

References (61)

1. Machado CA, Ayala FJ (2001) Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi. Proc Natl Acad Sci U S A 98: 7396-7401. (Pubitemid 32567960)
2. Hoare CA (1972) The trypanosomes of mammals. Blackwell Scientific Publications. 749 p.
3. Lent H, Wygodzinksy P (1979) Revision of the Triatominae and their significance as vectors of Chagas disease. Bull Am Mus Nat Hist 163: 123-520.
4. Westenberger SJ, Barnabe C, Campbell DA, Sturm NR (2005) Two Hybridization Events Define the Population Structure of Trypanosoma cruzi. Genetics 171: 527-543. (Pubitemid 43156444)
5. de Freitas JM, Augusto-Pinto L, Pimenta JR, Bastos-Rodrigues L, Goncalves VF, et al. (2006) Ancestral Genomes, Sex, and the Population Structure of Trypanosoma cruzi. PLoS Pathogens 2: e24. doi:10.1371/journal.ppat.0020024.
6. Gaunt MW, Yeo M, Frame IA, Stothard JR, Carrasco HJ, et al. (2003) Mechanism of genetic exchange in American trypanosomes. Nature 421: 936-939. (Pubitemid 36288023)
7. Yeo M, Acosta N, Llewellyn M, Sanchez H, Adamson S, et al. (2005) Origins of Chagas disease: Didelphis species are natural hosts of Trypanosoma cruzi I and armadillos hosts of Trypanosoma cruzi II, including hybrids. Int J Parasitol 35: 225-233. (Pubitemid 40248717)
8. Miles MA, Cedillos RA, Povoa MM, de Souza AA, Prata A, et al. (1981) Do radically dissimilar Trypanosoma cruzi strains (zymodemes) cause Venezuelan and Brazilian forms of Chagas' disease? Lancet 1(8234): 1338-1340.
9. Anez N, Crisante G, da Silva FM, Rojas A, Carrasco H, et al. (2004) Predominance of lineage I among Trypanosoma cruzi isolates from Venezuelan patients with different clinical profiles of acute Chagas' disease. Trop Med Int Health 9: 1319-1326.
10. Miles MA, Yeo M, Gaunt M (2003) Genetic diversity of Typanosoma cruzi and the epidemiology of Chagas disease. In: Kelly JM, ed. Molecular mechanisms in the pathogenisis of Trypanosoma cruzi. New York: Kluwer Academic/Plenum.
11. Barnabe C, Brisse S, Tibayrenc M (2000) Population structure and genetic typing of Trypanosoma cruzi, the agent of Chagas disease: A multilocus enzyme electrophoresis approach. Parasitology 120: 513-526. (Pubitemid 30261023)
12. Lisboa CV, Mangia RH, Rubiao E, de Lima NR, das Chagas Xavier SC, et al. (2004) Trypanosoma cruzi transmission in a captive primate unit, Rio de Janeiro, Brazil. Acta Trop 90: 97-106.
13. O'Connor O, Bosseno MF, Barnabe C, Douzery EJ, Breniere SF (2007) Genetic clustering of Trypanosoma cruzi I lineage evidenced by intergenic miniexon gene sequencing. Infect Genet Evol 7: 587-593. (Pubitemid 47338286)
14. Herrera C, Bargues MD, Fajardo A, Montilla M, Triana O, et al. (2007) Identifying four Trypanosoma cruzi I isolate haplotypes from different geographic regions in Colombia. Infect, Genet Evol 7: 535-539. (Pubitemid 46825523)
15. Oliveira RP, Broude NE, Macedo AM, Cantor CR, Smith CL, et al. (1998) Probing the genetic population structure of Trypanosoma cruzi with polymorphic microsatellites. Proc Natl Acad Sci U S A 95: 3776-3780. (Pubitemid 28173205)
16. Carrasco HJ, Frame IA, Valente SA, Miles MA (1996) Genetic exchange as a possible source of genomic diversity in sylvatic populations of Trypanosoma cruzi. Am J Trop Med Hyg 54: 418-424. (Pubitemid 26126653)
17. Higo H, Miura S, Horio M, Mimori T, Hamano S, et al. (2004) Genotypic variation among lineages of Trypanosoma cruzi and its geographic aspects. Parasitol Intl 53: 337-344. (Pubitemid 39303615)
18. Coura JR, Junqueira AC, Fernandes O, Valente SA, Miles MA (2002) Emerging Chagas disease in Amazonian Brazil. Trends Parasitol 18: 171-176. (Pubitemid 34606845)
19. Morrison LJ, Mallon ME, Smith HV, MacLeod A, Xiao L, et al. (2008) The population structure of the Cryptosporidium parvum population in Scotland: A complex picture. Infect Genet Evol 8: 121-129.
20. MacLeod A, Tweedie A, Welburn SC, Maudlin I, Turner CM, et al. (2000) Minisatellite marker analysis of Trypanosoma brucei: Reconciliation of clonal, panmictic, and epidemic population genetic structures. Proc Natl Acad Sci U S A 97: 13442-13447.
21. Miles M, Toye P, Oswald S, Godfrey D (1977) The identification by isoenzyme patterns of two distinct strain-groups of Trypanosoma cruzi, circulating independently in a rural area of Brazil. Trans R Soc Trop Med Hyg 71: 217-225. (Pubitemid 8126905)
22. Tibayrenc M, Ayala FJ (2002) The clonal theory of parasitic protozoa: 12 years on. Trends Parasitol 18: 405-410.
23. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409-415. (Pubitemid 40994675)
24. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959. (Pubitemid 30397141)
25. Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89: 238-247. (Pubitemid 28292519)
26. Wahlund S (1928) Zusammensetzung von Population und Korrelationserscheinung vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas 11: 65-106.
27. Hamilton PB, Gibson WC, Stevens JR (2007) Patterns of co-evolution between trypanosomes and their hosts deduced from ribosomal RNA and protein-coding gene phylogenies. Mol Phylogenet Evol 44: 15-25. (Pubitemid 46829926)
28. Legey AP, Pinho AP, Xavier SC, Marchevsky R, Carreira JC, et al. (2003) Trypanosoma cruzi in marsupial didelphids (Philander frenata and Didelhis marsupialis): Differences in the humoral immune response in natural and experimental infections. Rev Soc Bras Med Trop 36: 241-248. (Pubitemid 36753347)
29. Carreira JC, Jansen AM, de Nazareth Meirelles M, Costa e Silva F, Lenzi HL (2001) Trypanosoma cruzi in the scent glands of Didelphis marsupialis: the kinetics of colonization. Exp Parasitol 97: 129-140.
30. Gaunt M, Miles M (2000) The ecotopes and evolution of triatomine bugs (triatominae) and their associated trypanosomes. Mem Inst Oswaldo Cruz 95: 557-565.
31. Barnabe C, Yaeger R, Pung O, Tibayrenc M (2001) Trypanosoma cruzi: A considerable phylogenetic divergence indicates that the agent of Chagas disease is indigenous to the native fauna of the United States. Exp Parasitol 99: 73-79. (Pubitemid 34038218)
32. Marshall L, Sempere T (1993) Evolution of the Neotropical Cenozoic land mammal fauna in its geochronologic, stratigraphic, and tectonic context. In: Goldblatt P, ed. Biological relationships between Africa and South America. New Haven (Connecticut): Yale University Press. pp 329-392.
33. Feliciangeli MD, Campbell-Lendrum D, Martinez C, Gonzalez D, Coleman P, et al. (2003) Chagas disease control in Venezuela: Lessons for the Andean region and beyond. Trends Parasitol 19: 44-49. (Pubitemid 35454013)
34. Fitzpatrick S, Feliciangeli MD, Sanchez-Martin MJ, Monteiro FA, Miles MA (2008) Molecular Genetics Reveal That Silvatic Rhodnius prolixus Do Colonise Rural Houses. PLoS Negl Trop Dis 2: e210. doi:10.1371/journal.pntd.0000210.
35. Koffi M, De Meeus T, Bucheton B, Solano P, Camara M, et al. (2009) Population genetics of Trypanosoma brucei gambiense, the agent of sleeping sickness in Western Africa. Proc Natl Acad Sci U S A 106: 209-214.
36. Gibson W (2002) Will the real Trypanosoma brucei rhodesiense please step forward? Trends Parasitol 18: 486-490.
37. Monteiro FA, Barrett TV, Fitzpatrick S, Cordon-Rosales C, Feliciangeli D, et al. (2003) Molecular phylogeography of the Amazonian Chagas disease vectors Rhodnius prolixus and R. robustus. Mol Ecol 12: 997-1006. (Pubitemid 36524292)
38. Cortez MR, Emperaire L, Piccinali R, Gurtler RE, Torrico F, et al. (2007) Sylvatic Triatoma infestans (Reduviidae, Triatominae) in the Andean valleys of Bolivia. Acta Trop 102: 47-54. (Pubitemid 46823961)
39. Medrano-Mercado N, Ugarte-Fernandez R, Butron V, Uber-Busek S, Guerra HL, et al. (2008) Urban transmission of Chagas disease in Cochabamba, Bolivia. Mem Inst Oswaldo Cruz 103: 423-430.
40. Schwenkenbecher JM, Wirth T, Schnur LF, Jaffe CL, Schallig H, et al. (2006) Microsatellite analysis reveals genetic structure of Leishmania tropica. Int J Parasitol 36: 237-246. (Pubitemid 43208990)
41. Kuhls K, Chicharro C, Canavate C, Cortes S, Campino L, et al. (2008) Differentiation and Gene Flow among European Populations of Leishmania infantum MON-1. PLoS Negl Trop Dis 2: e261. doi:10.1371/journal. pntd.0000261.
42. Al-Jawabreh A, Diezmann S, Muller M, Wirth T, Schnur LF, et al. (2008) Identification of geographically distributed sub-populations of Leishmania (Leishmania) major by microsatellite analysis. BMC Evol Biol 8: 183. (Pubitemid 351958453)
43. Balloux F, Lehmann L, de Meeus T (2003) The population genetics of clonal and partially clonal diploids. Genetics 164: 1635-1644. (Pubitemid 37102223)
44. De Meeus T, Lehmann L, Balloux F (2006) Molecular epidemiology of clonal diploids: A quick overview and a short DIY (do it yourself) notice. Infect Genet Evol 6: 163-170. (Pubitemid 43285823)
45. Mark Welch D, Meselson M (2000) Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288: 1211-1215. (Pubitemid 30367193)
46. Maynard Smith J, Smith NH, O'Rourke M, Spratt BG (1993) How Clonal are Bacteria? Proc Natl Acad Sci U S A 90: 4384-4388.
47. Birky CW Jr (1996) Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics 144: 427-437. (Pubitemid 26291950)
48. Forche A, Alby K, Schaefer D, Johnson AD, Berman J, et al. (2008) The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol 6: e110. doi:10.1371/ journal.pbio.0060110. (Pubitemid 351824743)
49. Spotorno OA, Córdova L, Solari IA (2008) Differentiation of Trypanosoma cruzi I subgroups through characterization of cytochrome b gene sequences. Infect Genet Evol 8: 898-900.
50. Westenberger SJ, Sturm NR, Campbell DA (2006) Trypanosoma cruzi 5S rRNA arrays define five groups and indicate the geographic origins of an ancestor of the heterozygous hybrids. Intl J Parasitol 36: 337-346. (Pubitemid 43376115)
51. Brisse S, Verhoef J, Tibayrenc M (2001) Characterisation of large and small subunit rRNA and mini-exon genes further supports the distinction of six Trypanosoma cruzi lineages. Int J Parasitol 31: 1218-1226. (Pubitemid 32762992)
52. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, eds. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa (New Jersey): Humana Press.
53. Goudet J (1995) FSTAT Version 1.2: A computer program to calculate F-statistics. J Heredity 86: 485-486.
54. Hurlbert S (1971) The non concept of species diversity: A critique and alternative parameters. Ecology 52: 577-586.
55. Gutiérrez J, Royo L, A ́ lvarez I, Goyache F (2005) MolKin v2.0: A computer program for genetic analysis of populations using molecular coancestry information. J Heredity 96: 718-721.
56. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 1: 47-50.
57. Rice W (1989) Analyzing tables with statistical tests. Evolution 43: 223-225.
58. Weir BS, Cockerman CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370. (Pubitemid 16277759)
59. Agapow PM, Burt A (2001) Indices of multilocus linkage disequilibrium. Mol Ecol Notes 1: 101-102. (Pubitemid 33691862)
60. Minch E, Ruíz-Linares A, Goldstein D, Feldman M, Cavalli-Sforza L (1995) MICROSAT-The Microsatellite Distance Program. Stanford: Stanford University Press.
61. Peakall R, Smouse P (2006) GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288-295.