Evidence of substantial recombination among Trypanosoma cruzi II strains from Minas Gerais

Infection, Genetics and Evolution

Volumn 22, Issue , 2014, Pages 183-191

  Baptista, Rodrigo de Paula ^a   D'Ávila, Daniella Alchaar ^a   Segatto, Marcela ^a   Valle, Ítalo Faria do ^a   Franco, Glória Regina ^a   Valadares, Helder Magno Silva ^b   Gontijo, Eliane Dias ^a   Galvão, Lúcia Maria da Cunha ^a,c   Pena, Sérgio Danilo Junho ^a   Chiari, Egler ^a   Machado, Carlos Renato ^a   Macedo, Andréa Mara ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

Author keywords

Clonality; Population substructuring; Recombination; Sex reproduction; Trypanosoma cruzi II; Wahlund effect

Indexed keywords

ARTICLE; BRAZIL; COMPARATIVE STUDY; CONTROLLED STUDY; DNA POLYMORPHISM; GENE CLUSTER; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC ASSOCIATION; GENETIC DISTANCE; GENOTYPE; GEOGRAPHICAL VARIATION (SPECIES); HAPLOTYPE; HARDY WEINBERG DISTRIBUTION LAW; HOMOLOGOUS RECOMBINATION; HUMAN; INDEL MUTATION; INHERITANCE; MICROSATELLITE MARKER; MOLECULAR CLONING; NONHUMAN; POPULATION GENETIC PARAMETERS; POPULATION GENETIC STRUCTURE; PRIORITY JOURNAL; STRAIN DIFFERENCE; STRUCTURE ANALYSIS; TRYPANOSOMA CRUZI;

TRYPANOSOMA CRUZI;

CLONALITY; POPULATION SUBSTRUCTURING; RECOMBINATION; SEX REPRODUCTION; TRYPANOSOMA CRUZI II; WAHLUND EFFECT;

BRAZIL; CHAGAS DISEASE; DNA, PROTOZOAN; HAPLOTYPES; HUMANS; LINKAGE DISEQUILIBRIUM; MICROSATELLITE REPEATS; RECOMBINATION, GENETIC; TRYPANOSOMA CRUZI;

EID: 84896731588     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2013.11.021     Document Type: Article

References (50)

1. Balloux F., Lehmann L., de Meeus T. The population genetics of clonal and partially clonal diploids. Genetics 2003, 164:1635-1644.
2. Baptista C.S., Vencio R.Z., Abdala S., Carranza J.C., Westenberger S.J., Silva M.N., Pereira C.A., Galvao L.M., Gontijo E.D., Chiari E., Sturm N.R., Zingales B. Differential transcription profiles in Trypanosoma cruzi associated with clinical forms of Chagas disease: maxicircle NADH dehydrogenase subunit 7 gene truncation in asymptomatic patient isolates. Mol. Biochem. Parasitol. 2006, 150:236-248.
3. Barnabé C., Brenière S.F. Scarce events of mitochondrial introgression in Trypanosoma cruzi: new case with a Bolivian strain. Infect. Genet. Evol. 2012, 12:1879-1883.
4. Bastien P., Blaineau C., Pages M. Leishmania: sex, lies and karyotype. Parasitol. Today 1992, 8:174-177.
5. Bengtsson B.O. Genetic variation in organisms with sexual and asexual reproduction. J. Evol. Biol. 2003, 16:189-199.
6. Bogliolo A.R., Lauria-Pires L., Gibson W.C. Polymorphisms in Trypanosoma cruzi: evidence of genetic recombination. Acta Trop. 1996, 61:31-40.
7. Brisse S., Henriksson J., Barnabe C., Douzery E.J., Berkvens D., Serrano M., De Carvalho M.R., Buck G.A., Dujardin J.C., Tibayrenc M. Evidence for genetic exchange and hybridization in Trypanosoma cruzi based on nucleotide sequences and molecular karyotype. Infect. Genet. Evol. 2003, 2:173-183.
8. Burgos J.M., Altcheh J., Bisio M., Duffy T., Valadares H.M., Seidenstein M.E., Piccinali R., Freitas J.M., Levin M.J., Macchi L., Macedo A.M., Freilij H., Schijman A.G. Direct molecular profiling of minicircle signatures and lineages of Trypanosoma cruzi bloodstream populations causing congenital Chagas disease. Int. J. Parasitol. 2007, 37:1319-1327.
9. Carranza J.C., Valadares H.M., D'Avila D.A., Baptista R.P., Moreno M., Galvao L.M., Chiari E., Sturm N.R., Gontijo E.D., Macedo A.M., Zingales B. Trypanosoma cruzi maxicircle heterogeneity in Chagas disease patients from Brazil. Int. J. Parasitol. 2009, 39:963-973.
10. Carrasco H.J., Frame I.A., Valente S.A., Miles M.A. Genetic exchange as a possible source of genomic diversity in sylvatic populations of Trypanosoma cruzi. Am. J. Trop. Med. Hyg. 1996, 54:418-424.
11. D'Avila D.A., Macedo A.M., Valadares H.M., Gontijo E.D., de Castro A.M., Machado C.R., Chiari E., Galvao L.M. Probing population dynamics of Trypanosoma cruzi during progression of the chronic phase in chagasic patients. J. Clin. Microbiol. 2009, 47:1718-1725.
12. de Freitas J.M., Augusto-Pinto L., Pimenta J.R., Bastos-Rodrigues L., Goncalves V.F., Teixeira S.M., Chiari E., Junqueira A.C., Fernandes O., Macedo A.M., Machado C.R., Pena S.D. Ancestral genomes, sex, and the population structure of Trypanosoma cruzi. PLoS Pathog. 2006, 2:e24.
13. Devera R., Fernandes O., Coura J.R. Should Trypanosoma cruzi be called "cruzi" complex? a review of the parasite diversity and the potential of selecting population after in vitro culturing and mice infection. Mem. Inst. Oswaldo Cruz 2003, 98:1-12.
14. Evanno G., Regnaut S., Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 2005, 14:2611-2620.
15. Excoffier L., Laval G., Schneider S. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol. Bioinform. Online 2005, 1:47-50.
16. Forster P., Rohl A., Lunnemann P., Brinkmann C., Zerjal T., Tyler-Smith C., Brinkmann B. A short tandem repeat-based phylogeny for the human Y chromosome. Am. J. Hum. Genet. 2000, 67:182-196.
17. Gaunt M.W., Yeo M., Frame I.A., Stothard J.R., Carrasco H.J., Taylor M.C., Mena S.S., Veazey P., Miles G.A., Acosta N., de Arias A.R., Miles M.A. Mechanism of genetic exchange in American trypanosomes. Nature 2003, 421:936-939.
18. Lewis M.D., Llewellyn M.S., Yeo M., Acosta N., Gaunt M.W., Miles M.A. Recent, independent and anthropogenic origins of Trypanosoma cruzi hybrids. PLoS Negl. Trop. Dis. 2011, 5:e1363.
19. Llewellyn M.S., Miles M.A., Carrasco H.J., Lewis M.D., Yeo M., Vargas J., Torrico F., Diosque P., Valente V., Valente S.A., Gaunt M.W. Genome-scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection. PLoS Pathog. 2009, 5:e1000410.
20. Llewellyn M.S., Lewis M.D., Acosta N., Yeo M., Carrasco H.J., Segovia M., Vargas J., Torrico F., Miles M.A., Gaunt M.W. Trypanosoma cruzi IIc: phylogenetic and phylogeographic insights from sequence and microsatellite analysis and potential impact on emergent Chagas disease. PLoS Negl. Trop. Dis. 2009, 1:e510.
21. Macedo A.M., Pena S.D. Genetic variability of Trypanosoma cruzi: implications for the pathogenesis of Chagas disease. Parasitol. Today 1998, 14:119-124.
22. Macedo A.M., Martins M.S., Chiari E., Pena S.D. DNA fingerprinting of Trypanosoma cruzi: a new tool for characterization of strains and clones. Mol. Biochem. Parasitol. 1992, 55:147-153.
23. Macedo A.M., Pimenta J.R., Aguiar R.S., Melo A.I., Chiari E., Zingales B., Pena S.D., Oliveira R.P. Usefulness of microsatellite typing in population genetic studies of Trypanosoma cruzi. Mem. Inst. Oswaldo Cruz 2001, 96:407-413.
24. Macedo A.M., Rodrigues C.M., Oliveira R.P., Franco G.R., Machado C.R., Pena S.D.J., Valadares H.M.S. Contribution of Trypanosoma cruzi polymorphic microsatellite analyses in refining epidemiology aspects of Chagas disease. Rev. Soc. Bras. Med. Trop. 2009, 42:80-86.
25. Machado C.A., Ayala F.J. Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi. Proc. Natl. Acad. Sci. USA 2001, 98:7396-7401.
26. Mark Welch D.B., Meselson M. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 2000, 288:1211-1215.
27. Messenger L.A., Llewellyn M.S., Bhattacharyya T., Franzén O., Lewis M.D., Ramírez J.D., Carrasco H.J., Andersson B., Miles M.A. Multiple mitochondrial introgression events and heteroplasmy in Trypanosoma cruzi revealed by maxicircle MLST and next generation sequencing. PLoS Negl. Trop. Dis. 2012, 6:e1584.
28. Ocaña-Mayorga S., Llewellyn M.S., Costales J.A., Miles M.A., Grijalva M.J. Sex, subdivision, and domestic dispersal of Trypanosoma cruzi lineage I in southern Ecuador. PLoS Negl. Trop. Dis. 2010, 4:e915.
29. Oliveira R.P., Broude N.E., Macedo A.M., Cantor C.R., Smith C.L., Pena S.D. Probing the genetic population structure of Trypanosoma cruzi with polymorphic microsatellites. Proc. Natl. Acad. Sci. USA 1998, 95:3776-3780.
30. Pinto C.M., Kalko E.K., Cottontail I., Wellinghausen N., Cottontail V.M. TcBat a bat-exclusive lineage of Trypanosoma cruzi in the Panama Canal Zone, with comments on its classification and the use of the 18S rRNA gene for lineage identification. Infect. Genet. Evol. 2012, 12:1328-1332.
31. Poulin R., Morand S. Geographical distances and the similarity among parasite communities of conspecific host populations. Parasitology 1999, 119(Pt 4):369-374.
32. Pritchard J.K., Stephens M., Donnelly P. Inference of population structure from multilocus genotype data. Genetics 2000, 155:945-959.
33. Ramirez J.D., Duque M.C., Montilla M., Cucunuba Z., Guhl F. Natural and emergent Trypanosoma cruzi I genotypes revealed by mitochondrial (Cytb) and nuclear (SSU rDNA) genetic markers. Exp. Parasitol. 2012, 132:487-494.
34. Raymond M., Rousset F. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 1995, 86:248-249.
35. Souto R.P., Fernandes O., Macedo A.M., Campbell D.A., Zingales B. DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol. Biochem. Parasitol. 1996, 83:141-152.
36. Stephens M., Smith N.J., Donnelly P. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 2001, 68:978-989.
37. Sturm N.R., Vargas N.S., Westenberger S.J., Zingales B., Campbell D.A. Evidence for multiple hybrid groups in Trypanosoma cruzi. Int. J. Parasitol. 2003, 33:269-279.
38. Tibayrenc M., Ayala F.J. The clonal theory of parasitic protozoa: 12years on. Trends Parasitol. 2002, 18:405-410.
39. Tibayrenc M., Ayala F.J. How clonal are Trypanosoma and Leishmania?. Trends Parasitol. 2013, 29:264-269.
40. Tibayrenc M., Ward P., Moya A., Ayala F.J. Natural populations of Trypanosoma cruzi, the agent of Chagas disease, have a complex multiclonal structure. Proc. Natl. Acad. Sci. USA 1986, 83:115-119.
41. Tibayrenc M., Kjellberg F., Ayala F.J. A clonal theory of parasitic protozoa: the population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas, and Trypanosoma and their medical and taxonomical consequences. Proc. Natl. Acad. Sci. USA 1990, 87:2414-2418.
42. Tibayrenc M., Kjellberg F., Arnaud J., Oury B., Breniere S.F., Darde M.L., Ayala F.J. Are eukaryotic microorganisms clonal or sexual? A population genetics vantage. Proc. Natl. Acad. Sci. USA 1991, 88:5129-5133.
43. Tomazi L., Kawashita S.Y., Pereira P.M., Zingales B., Briones M.R. Haplotype distribution of five nuclear genes based on network genealogies and Bayesian inference indicates that Trypanosoma cruzi hybrid strains are polyphyletic. Genet. Mol. Res. 2009, 8:458-476.
44. Valadares H.M., Pimenta J.R., de Freitas J.M., Duffy T., Bartholomeu D.C., Oliveira Rde P., Chiari E., Moreira Mda C., Filho G.B., Schijman A.G., Franco G.R., Machado C.R., Pena S.D., Macedo A.M. Genetic profiling of Trypanosoma cruzi directly in infected tissues using nested PCR of polymorphic microsatellites. Int. J. Parasitol. 2008, 38:839-850.
45. Venegas J., Conoepan W., Pichuantes S., Miranda S., Jercic M.I., Gajardo M., Sanchez G. Phylogenetic analysis of microsatellite markers further supports the two hybridization events hypothesis as the origin of the Trypanosoma cruzi lineages. Parasitol. Res. 2009, 105:191-199.
46. Wahlund S. Zusammensetzung von population und korrelationserscheinung vom standpunkt der vererbungslehre aus betrachtet. Hereditas 1928, 11:65-106.
47. Westenberger S.J., Barnabe C., Campbell D.A., Sturm N.R. Two hybridization events define the population structure of Trypanosoma cruzi. Genetics 2005, 171:527-543.
48. Zhang Q., Tibayrenc M., Ayala F.J. Linkage disequilibrium in natural populations of Trypanosoma cruzi (flagellate), the agent of Chagas' disease. J. Protozool. 1988, 35:81-85.
49. Zingales B., Andrade S.G., Briones M.R., Campbell D.A., Chiari E., Fernandes O., Guhl F., Lages-Silva E., Macedo A.M., Machado C.R., Miles M.A., Romanha A.J., Sturm N.R., Tibayrenc M., Schijman A.G. A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Mem. Inst. Oswaldo Cruz 2009, 104:1051-1054.
50. Zingales B., Miles M.A., Campbell D.A., Tibayrenc M., Macedo A.M., Teixeira M.M.G., Schijman A.G., Llewellyn M.S., Lages-Silva E., Machado C.R., Andrade S.G., Sturm N.R. The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infect. Genet. Evol. 2012, 12:240-253.