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Analyses of 32 Loci Clarify Phylogenetic Relationships among Trypanosoma cruzi Lineages and Support a Single Hybridization prior to Human Contact

DOI: 10.1371/journal.pntd.0001272

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Abstract:

Background The genetic diversity of Trypanosoma cruzi, the etiological agent of Chagas disease, has been traditionally divided in two major groups, T. cruzi I and II, corresponding to discrete typing units TcI and TcII-VI under a recently proposed nomenclature. The two major groups of T. cruzi seem to differ in important biological characteristics, and are thus thought to represent a natural division relevant for epidemiological studies and development of prophylaxis. To understand the potential connection between the different manifestations of Chagas disease and variability of T. cruzi strains, it is essential to have a correct reconstruction of the evolutionary history of T. cruzi. Methodology/Principal Findings Nucleotide sequences from 32 unlinked loci (>26 Kilobases of aligned sequence) were used to reconstruct the evolutionary history of strains representing the known genetic variability of T. cruzi. Thorough phylogenetic analyses show that the original classification of T. cruzi in two major lineages does not reflect its evolutionary history and that there is only strong evidence for one major and recent hybridization event in the history of this species. Furthermore, estimates of divergence times using Bayesian methods show that current extant lineages of T. cruzi diverged very recently, within the last 3 million years, and that the major hybridization event leading to hybrid lineages TcV and TcVI occurred less than 1 million years ago, well before the contact of T. cruzi with humans in South America. Conclusions/Significance The described phylogenetic relationships among the six major genetic subdivisions of T. cruzi should serve as guidelines for targeted epidemiological and prophylaxis studies. We suggest that it is important to reconsider conclusions from previous studies that have attempted to uncover important biological differences between the two originally defined major lineages of T. cruzi especially if those conclusions were obtained from single or few strains.

References

[1]  WHO (2002) Control of Chagas disease: second report of the WHO expert committee. Geneva, Switzerland: UNDP/World Bank/WHO. Technical Report Series 905:
[2]  Miles MA, Feliciangeli MD, de Arias AR (2003) American trypanosomiasis (Chagas' disease) and the role of molecular epidemiology in guiding control strategies. BMJ 326: 1444–1448. doi: 10.1136/bmj.326.7404.1444
[3]  Barrett MP, Burchmore RJ, Stich A, Lazzari JO, Frasch AC, et al. (2003) The trypanosomiases. Lancet 362: 1469–1480. doi: 10.1016/S0140-6736(03)14694-6
[4]  Miles MA, Souza A, Povoa M, Shaw JJ, Lainson R, et al. (1978) Isozymic heterogeneity of Trypanosoma cruzi in the first autochthonous patients with Chagas' disease in Amazonian Brazil. Nature 272: 819–821. doi: 10.1038/272819a0
[5]  Tibayrenc M, Ward P, Moya A, Ayala FJ (1986) Natural populations of Trypanosoma cruzi, the agent of Chagas disease, have a complex multiclonal structure. Proc Natl Acad Sci USA 83: 115–119. doi: 10.1073/pnas.83.1.115
[6]  Tibayrenc M, Ayala FJ (1988) Isozyme variability in Trypanosoma cruzi, the agent of Chagas' disease: Genetical, taxonomical, and epidemiological significance. Evolution 42: 277–292. doi: 10.2307/2409232
[7]  Souto RP, Zingales B (1993) Sensitive detection and strain classification of Trypanosoma cruzi by amplification of a ribosomal RNA sequence. Mol Biochem Parasitol 62: 45–52. doi: 10.1016/0166-6851(93)90176-X
[8]  Brisse S, Barnabe C, Tibayrenc M (2000) Identification of six Trypanosoma cruzi phylogenetic lineages by random amplified polymorphic DNA and multilocus enzyme electrophoresis. Int J Parasitol 30: 35–44. doi: 10.1016/S0020-7519(99)00168-X
[9]  Brisse S, Dujardin J, Tibayrenc M (2000) Identification of six trypanosoma cruzi lineages by sequence-characterised amplified region markers. Mol Biochem Parasitol 111: 95–105. doi: 10.1016/S0166-6851(00)00302-9
[10]  Machado CA, Ayala FJ (2001) Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi. Proc Natl Acad Sci USA 98: 7396–7401. doi: 10.1073/pnas.121187198
[11]  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 Pathog 2: e24. doi: 10.1371/journal.ppat.0020024
[12]  Llewellyn MS, Miles MA, Carrasco HJ, Lewis MD, Yeo M, et al. (2009) Genome-scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection. PLoS Pathog 5: e1000410. doi: 10.1371/journal.ppat.1000410
[13]  Telleria J, Biron DG, Brizard JP, Demettre E, Seveno M, et al. (2010) Phylogenetic character mapping of proteomic diversity shows high correlation with subspecific phylogenetic diversity in Trypanosoma cruzi. Proc Natl Acad Sci USA.
[14]  Tibayrenc M (2010) Modelling the Transmission of Trypanosoma cruzi: The Need for an Integrated Genetic Epidemiological and Population Genomics Approach. In: Michael E, Spear RC, editors. Modelling Parasite Transmission and Control. Austin,, TX: Landes. pp. 200–211.
[15]  Bogliolo AR, Lauria-Pires L, Gibson WC (1996) Polymorphism in Trypanosoma cruzi: evidence of genetic recombination. Acta Trop 61: 31–40. doi: 10.1016/0001-706X(95)00138-5
[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.
[17]  Brisse S, Barnabe C, Banuls AL, Sidibe I, Noel S, et al. (1998) A phylogenetic analysis of the Trypanosoma cruzi genome project CL Brener reference strain by multilocus enzyme electrophoresis and multiprimer random amplified polymorphic DNA fingerprinting. Mol Biochem Parasitol 92: 253–263. doi: 10.1016/S0166-6851(98)00005-X
[18]  Machado CA, Ayala FJ (2002) Sequence variation in the dihydrofolate reductase-thymidylate synthase (DHFR-TS) and trypanothione reductase (TR) genes of Trypanosoma cruzi. Mol Biochem Parasitol 121: 33–47. doi: 10.1016/S0166-6851(02)00019-1
[19]  Brisse S, Henriksson J, Barnabe C, Douzery EJ, Berkvens D, et al. (2003) Evidence for genetic exchange and hybridization in Trypanosoma cruzi based on nucleotide sequences and molecular karyotype. Infect Genet Evol 2: 173–183. doi: 10.1016/S1567-1348(02)00097-7
[20]  Sturm NR, Vargas NS, Westenberger SJ, Zingales B, Campbell DA (2003) Evidence for multiple hybrid groups in Trypanosoma cruzi. Int J Parasitol 33: 269–279. doi: 10.1016/S0020-7519(02)00264-3
[21]  Gaunt MW, Yeo M, Frame IA, Stothard JR, Carrasco HJ, et al. (2003) Mechanism of genetic exchange in American trypanosomes. Nature 421: 936–939. doi: 10.1038/nature01438
[22]  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 Int 53: 337–344. doi: 10.1016/j.parint.2004.06.001
[23]  Westenberger SJ, Barnabe C, Campbell DA, Sturm NR (2005) Two hybridization events define the population structure of Trypanosoma cruzi. Genetics 171: 527–543. doi: 10.1534/genetics.104.038745
[24]  Ocana-Mayorga S, Llewellyn MS, Costales JA, Miles MA, Grijalva MJ (2010) Sex, subdivision, and domestic dispersal of Trypanosoma cruzi lineage I in southern Ecuador. PLoS Negl Trop Dis 4: e915. doi: 10.1371/journal.pntd.0000915
[25]  Tibayrenc M, Neubauer K, Barnabe C, Guerrini F, Skarecky D, et al. (1993) Genetic characterization of six parasitic protozoa: parity between random-primer DNA typing and multilocus enzyme electrophoresis. Proc Natl Acad Sci USA 90: 1335–1339. doi: 10.1073/pnas.90.4.1335
[26]  Tibayrenc M (1995) Population genetics of parasitic protozoa and other microorganisms. Adv Parasitol 36: 47–115. doi: 10.1016/s0065-308x(08)60490-x
[27]  Souto RP, Fernandes O, Macedo AM, Campbell DA, Zingales B (1996) DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol Biochem Parasitol 83: 141–152. doi: 10.1016/S0166-6851(96)02755-7
[28]  Nunes LR, de Carvalho MR, Buck GA (1997) Trypanosoma cruzi strains partition into two groups based on the structure and function of the spliced leader RNA and rRNA gene promoters. Mol Biochem Parasitol 86: 211–224. doi: 10.1016/S0166-6851(97)02857-0
[29]  Zingales B, Stolf BS, Souto RP, Fernandes O, Briones MR (1999) Epidemiology, biochemistry and evolution of Trypanosoma cruzi lineages based on ribosomal RNA sequences. Mem Inst Oswaldo Cruz 94: 159–164. doi: 10.1590/S0074-02761999000700020
[30]  Anon (1999) Recommendations from a satellite meeting. Mem Inst Oswaldo Cruz 94: 429–432. doi: 10.1590/s0074-02761999000700085
[31]  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(Pt 5): 513–526. doi: 10.1017/S0031182099005661
[32]  Zingales B, Andrade SG, Briones MRS, Campbell DA, Chiari E, et al. (2009) A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Mem Inst Oswaldo Cruz 104: 1051–1054. doi: 10.1590/S0074-02762009000700021
[33]  Andrade S, Ga MJB (1997) Biodemes and zymodemes of Trypanosoma cruzi strains: correlations with clinical data and experimental pathology. Rev Soc Bras Med Trop 30: 27–35. doi: 10.1590/S0037-86821997000100006
[34]  Laurent JP, Barnabe C, Quesney V, Noel S, Tibayrenc M (1997) Impact of clonal evolution on the biological diversity of Trypanosoma cruzi. Parasitology 114(Pt 3): 213–218. doi: 10.1017/S0031182096008414
[35]  Revollo S, Oury B, Laurent JP, Barnabe C, Quesney V, et al. (1998) Trypanosoma cruzi: impact of clonal evolution of the parasite on its biological and medical properties. Exp Parasitol 89: 30–39. doi: 10.1006/expr.1998.4216
[36]  Luquetti AO, Miles MA, Rassi A, de Rezende JM, de Souza AA, et al. (1986) Trypanosoma cruzi: zymodemes associated with acute and chronic Chagas' disease in central Brazil. Trans R Soc Trop Med Hyg 80: 462–470. doi: 10.1016/0035-9203(86)90347-0
[37]  Breniere SF, Bosseno MF, Telleria J, Bastrenta B, Yacsik N, et al. (1998) Different behavior of two Trypanosoma cruzi major clones: Transmission and circulation in young Bolivian patients. Exp Parasitol 89: 285–295. doi: 10.1006/expr.1998.4295
[38]  Zingales B, Souto RP, Mangia RH, Lisboa CV, Campbell DA, Coura JR, Jansen A, Fernandes O (1998) Molecular epidemiology of American trypanosomiasis in Brazil based on dimorphisms of rRNA and mini-exon gene sequences. Int J Parasitol 28: 105–112. doi: 10.1016/S0020-7519(97)00178-1
[39]  Coura JR, Junqueira ACV, Fernandes O, Valente SAS, Miles MA (2002) Emerging Chagas disease in Amazonian Brazil. Trends Parasitol 18: 171–176. doi: 10.1016/S1471-4922(01)02200-0
[40]  Di Noia JM, Buscaglia CA, De Marchi CR, Almeida IC, Frasch ACC (2002) A Trypanosoma cruzi small surface molecule provides the first immunological evidence that Chagas' disease is due to a single parasite lineage. J Exp Med 195: 401–413. doi: 10.1084/jem.20011433
[41]  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. doi: 10.1016/j.ijpara.2004.10.024
[42]  Montilla M, Guhl F, Jaramillo C, Nicholls S, Barnabe C, et al. (2002) Isoenzyme clustering of Trypanosomatidae Colombian populations. Am J Trop Med Hyg 66: 394–400.
[43]  Tomazi L, Kawashita SY, Pereira PM, Zingales B, Briones MR (2009) Haplotype distribution of five nuclear genes based on network genealogies and Bayesian inference indicates that Trypanosoma cruzi hybrid strains are polyphyletic. Genet Mol Res 8: 458–476. doi: 10.4238/vol8-2gmr591
[44]  Robello C, Gamarro F, Castanys S, Alvarez-Valin F (2000) Evolutionary relationships in Trypanosoma cruzi: molecular phylogenetics supports the existence of a new major lineage of strains. Gene 246: 331–338. doi: 10.1016/S0378-1119(00)00074-3
[45]  Augusto-Pinto L, Teixeira SM, Pena SD, Machado CR (2003) Single-nucleotide polymorphisms of the Trypanosoma cruzi MSH2 gene support the existence of three phylogenetic lineages presenting differences in mismatch-repair efficiency. Genetics 164: 117–126.
[46]  Subileau M, Barnabe C, Douzery EJ, Diosque P, Tibayrenc M (2009) Trypanosoma cruzi: new insights on ecophylogeny and hybridization by multigene sequencing of three nuclear and one maxicircle genes. Exp Parasitol 122: 328–337. doi: 10.1016/j.exppara.2009.04.008
[47]  Kawashita SY, Sanson GF, Fernandes O, Zingales B, Briones MR (2001) Maximum-likelihood divergence date estimates based on rRNA gene sequences suggest two scenarios of Trypanosoma cruzi intraspecific evolution. Mol Biol Evol 18: 2250–2259. doi: 10.1093/oxfordjournals.molbev.a003771
[48]  Broutin H, Tarrieu F, Tibayrenc M, Oury B, Barnabe C (2006) Phylogenetic analysis of the glucose-6-phosphate isomerase gene in Trypanosoma cruzi. Exp Parasitol 113: 1–7. doi: 10.1016/j.exppara.2005.11.014
[49]  Llewellyn MS, Lewis MD, Acosta N, Yeo M, Carrasco HJ, et al. (2009) Trypanosoma cruzi IIc: phylogenetic and phylogeographic insights from sequence and microsatellite analysis and potential impact on emergent Chagas disease. PLoS Negl Trop Dis 3: e510. doi: 10.1371/journal.pntd.0000510
[50]  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. doi: 10.1126/science.1112631
[51]  Rozen DE, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, editors. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, NJ: Humana Press. pp. 365–386.
[52]  Weatherly DB, Boehlke C, Tarleton RL (2009) Chromosome level assembly of the hybrid Trypanosoma cruzi genome. BMC Genomics 10: 255. doi: 10.1186/1471-2164-10-255
[53]  Rambaut A (2002) Se-Al. Sequence alignment editor. V2.0a11 ed. Oxford, UK: University of Oxford.
[54]  Posada D, Crandall A (1998) ModelTest: Testing the model of DNA substitution. Bioinformatics 14: 817–818. doi: 10.1093/bioinformatics/14.9.817
[55]  Swofford DL (1998) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sunderland, , MA: Sinauer Associates.
[56]  Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. doi: 10.1093/bioinformatics/17.8.754
[57]  Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. doi: 10.1093/bioinformatics/btg180
[58]  Farris JS, Kallersjo M, Kluge AG, Bult C (1994) Testing significance of congruence. Cladistics 10: 315–319. doi: 10.1006/clad.1994.1021
[59]  Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16: 1114–1116. doi: 10.1093/oxfordjournals.molbev.a026201
[60]  Castoe TA, de Koning APJ, Kim HM, Gu WJ, Noonan BP, et al. (2009) Evidence for an ancient adaptive episode of convergent molecular evolution. Proc Natl Acad Sci USA 106: 8986–8991. doi: 10.1073/pnas.0900233106
[61]  Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591. doi: 10.1093/molbev/msm088
[62]  Yang Z, Swanson WJ (2002) Codon-substitution models to detect adaptive evolution that account for heterogeneous selective pressures among site classes. Mol Biol Evol 19: 49–57. doi: 10.1093/oxfordjournals.molbev.a003981
[63]  Swanson WJ, Nielsen R, Yang Q (2003) Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol 20: 18–20. doi: 10.1093/oxfordjournals.molbev.a004233
[64]  Felsenstein J (1988) Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22: 521–565. doi: 10.1146/annurev.ge.22.120188.002513
[65]  Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214. doi: 10.1186/1471-2148-7-214
[66]  Hay WW, DeConto RM, Wold CN, Wilson KM, Voigt S, et al. (1999) Alternative global Cretaceous paleogeography. In: Barrera E, Johnson CC, editors. Evolution of the Cretaceous ocean-climate system. Boulder, , CO: Geological Society of America. pp. 1–47.
[67]  Drummond A, Ho S, Rawlence N, Rambaut A (2007) A Rough Guide to beast 1.4. New Zealand: University of Auckland.
[68]  El-Sayed NM, Myler PJ, Blandin G, Berriman M, Crabtree J, et al. (2005) Comparative genomics of trypanosomatid parasitic protozoa. Science 309: 404–409. doi: 10.1126/science.1112181
[69]  Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680. doi: 10.1093/nar/22.22.4673
[70]  Valdes J, Taylor MC, Cross MA, Ligtenberg MJ, Rudenko G, et al. (1996) The viral thymidine kinase gene as a tool for the study of mutagenesis in Trypanosoma brucei. Nucleic Acids Res 24: 1809–1815. doi: 10.1093/nar/24.10.1809
[71]  Lynch M (2010) Evolution of the mutation rate. Trends Genet 26: 345–352. doi: 10.1016/j.tig.2010.05.003
[72]  Franzen O, Ochaya S, Sherwood E, Lewis MD, Llewellyn MS, et al. (2011) Shotgun sequencing analysis of Trypanosoma cruzi I Sylvio X10/1 and comparison with T. cruzi VI CL Brener. PLoS Negl Trop Dis 5: e984. doi: 10.1371/journal.pntd.0000984
[73]  Maddison DR, Donoghue MJ, Maddison DR (1984) Outgroup analysis and Parsimony. Syst Zool 33: 83–103. doi: 10.2307/2413134
[74]  Lake JA, de la Cruz VF, Ferreira PC, Morel C, Simpson L (1988) Evolution of parasitism: kinetoplastid protozoan history reconstructed from mitochondrial rRNA gene sequences. Proc Natl Acad Sci USA 85: 4779–4783. doi: 10.1073/pnas.85.13.4779
[75]  Stevens JR, Noyes HA, Dover GA, Gibson WC (1999) The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. Parasitology 118: 107–116. doi: 10.1017/S0031182098003473
[76]  Briones MRS, Souto RP, Stolf BS, Zingales B (1999) The evolution of two Trypanosoma cruzi subgroups inferred from rRNA genes can be correlated with the interchange of American mammalian faunas in the Cenozoic and has implications to pathogenicity and host specificity. Mol Biochem Parasitol 104: 219–232. doi: 10.1016/S0166-6851(99)00155-3
[77]  Gaunt M, Miles M (2000) The ecotopes and evolution of triatomine bugs (triatominae) and their associated trypanosomes. Mem Inst Oswaldo Cruz 95: 557–565. doi: 10.1590/S0074-02762000000400019
[78]  Li W-H (1997) Molecular evolution. Sunderland, , MA: Sinauer Associates.
[79]  Nei M (1987) Molecular Evolutionary Genetics. New York, , NY: Columbia University Press.
[80]  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 USA 106: 209–214. doi: 10.1073/pnas.0811080106
[81]  Schofield C (2000) Trypanosoma cruzi: the vector-parasite paradox. Mem Inst Oswaldo Cruz 95: 535–544. doi: 10.1590/S0074-02762000000400016
[82]  Gorla DE, Dujardin JP, Schofield CJ (1997) Biosystematics of Old World Triatominae. Acta Trop 63: 127–140. doi: 10.1016/S0001-706X(97)87188-4
[83]  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. doi: 10.1046/j.1365-294X.2003.01802.x
[84]  Gilbert C, Schaack S, Pace JK 2nd, Brindley PJ, Feschotte C (2010) A role for host-parasite interactions in the horizontal transfer of transposons across phyla. Nature 464: 1347–1350. doi: 10.1038/nature08939
[85]  Sturm NR, Campbell DA (2010) Alternative lifestyles: the population structure of Trypanosoma cruzi. Acta Trop 115: 35–43. doi: 10.1016/j.actatropica.2009.08.018

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