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. 2006 Mar;2(3):e24.
doi: 10.1371/journal.ppat.0020024. Epub 2006 Mar 31.

Ancestral genomes, sex, and the population structure of Trypanosoma cruzi

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Ancestral genomes, sex, and the population structure of Trypanosoma cruzi

Jorge M de Freitas et al. PLoS Pathog. 2006 Mar.

Abstract

Acquisition of detailed knowledge of the structure and evolution of Trypanosoma cruzi populations is essential for control of Chagas disease. We profiled 75 strains of the parasite with five nuclear microsatellite loci, 24Salpha RNA genes, and sequence polymorphisms in the mitochondrial cytochrome oxidase subunit II gene. We also used sequences available in GenBank for the mitochondrial genes cytochrome B and NADH dehydrogenase subunit 1. A multidimensional scaling plot (MDS) based in microsatellite data divided the parasites into four clusters corresponding to T. cruzi I (MDS-cluster A), T. cruzi II (MDS-cluster C), a third group of T. cruzi strains (MDS-cluster B), and hybrid strains (MDS-cluster BH). The first two clusters matched respectively mitochondrial clades A and C, while the other two belonged to mitochondrial clade B. The 24Salpha rDNA and microsatellite profiling data were combined into multilocus genotypes that were analyzed by the haplotype reconstruction program PHASE. We identified 141 haplotypes that were clearly distributed into three haplogroups (X, Y, and Z). All strains belonging to T. cruzi I (MDS-cluster A) were Z/Z, the T. cruzi II strains (MDS-cluster C) were Y/Y, and those belonging to MDS-cluster B (unclassified T. cruzi) had X/X haplogroup genotypes. The strains grouped in the MDS-cluster BH were X/Y, confirming their hybrid character. Based on these results we propose the following minimal scenario for T. cruzi evolution. In a distant past there were at a minimum three ancestral lineages that we may call, respectively, T. cruzi I, T. cruzi II, and T. cruzi III. At least two hybridization events involving T. cruzi II and T. cruzi III produced evolutionarily viable progeny. In both events, the mitochondrial recipient (as identified by the mitochondrial clade of the hybrid strains) was T. cruzi II and the mitochondrial donor was T. cruzi III.

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Conflict of interest statement

Competing interests. The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Multidimensional Scaling Plot of 75 T. cruzi Strains Genotyped for Five Microsatellites
Only outliers and the prototypical strains of Brisse et al. [26] are named in the plot. Arrowheads indicate strains 222 and 115. The strains in the areas delimited by ellipsoids are the following: MDS-cluster A: 1001, 1004, 1006, 1502, 1523, A83, A87, Col18/05, Colombiana, Cuíca, Cutia, D7, Gambacl1, Rb1, Rb2, Rb6, SE, X10cl1, 402, Mas1cl1, 84, 207, 209, 239, 577, 578, 580, 581, 803, 1005, 1014, 1043, 1931, 183744, 169/1; MDS-cluster C: 200pm, 84Ti, Be62, CPI11/94, CPI95/94, Esmeraldo, Gil, GLT564, GLT593, GMS, GOCH, Ig539, JAF, JG, JHF, JSM, MPD, OPS27/94, Tu18 cl11, Y; MDS-cluster B: 115, 222, 226, 231, 3663, 3869, 4182, M5631cl5; MDS-cluster BH: M6241cl6, 167, 1022, c182, CLBrener, MNcl2, NR, SC43 cl1, SO3, Tulacl2.
Figure 2
Figure 2. Sequence of a 290–Base Pair Fragment of the Mitochondrial COII Gene of 41 Strains of T. cruzi
Only the variable nucleotides are shown. T. cruzi III refers to sublineage IIc, and "Hybrids" indicate the strains belonging to sublineages IId and IIe of Brisse et al [26]. Two AluI restriction sites are indicated. RFLP analysis of these two sites allows unambiguous classification of T. cruzi strains to the three mitochondrial clades as shown on the right hand side.
Figure 3
Figure 3. NJ Trees Obtained from the Sequences of Three Mitochondrial Genes of T. cruzi: COII, CYb, and ND1
The numbers in the three main branches indicate the percentage bootstrap values. For COII the strains the following clades are displayed: clade A: 1004, 1006, 1502, Col18/05, Cuica, Cutia, RBI, RbII, SilvioX10; clade B: sublineage IIc—222, 231, 3869, M6241, Mn, sublineages IId and IIe—CLBrener, 1022, SO3, Tula; clade C: 1014, 1043, 169/1, 1931, 200pm, 209, 577, 578, 580, 581, 803, 84Ti, Be62, Esmeraldo, GLT593, GMS, Ig539, JG, JHF, Mas1, MPD, TU18, Y. For CYb the strains are as follows: clade A: Cuica, SC13, Tehuentepec, X10; clade B: sublineage IIc—M5631, M6241, X109/2, sublineages IId and IIe—92.80, CL, Guateque, MN, SC43, Tulahuen, X57; clade C: CBB, Esmeraldo, TU18. For ND1 the strains are as follows: clade A: 133, 26, 85/818, A80, A92, CEPA, CUICA, CUTIA, Esquilo, MAV, OPS21, P0AC, P209, SABP3, SC13, SO34, TEH, V121, Vin, X10; clade B: sublineage IIc—CM, M6241, X109/2, X110/8, X9/3, sublineages IId and IIe—CL, 86/2036, 86–1, EPP, P251, P63, PSC-O, SO3, Tulahuen, VMV4; clade C: CBB, Esmeraldo, MBV, MCV, MSC2, TU18, X-300.
Figure 4
Figure 4. Median Joining Network of the Haplotypes Identified by the PHASE Software
Figure 5
Figure 5. Diagram Depicting the Proposed Model for the Evolution of T. cruzi Strains
The mitochondrial clade was typed by RFLP of the COII maxicircle gene, the MDS clusters were established by multidimensional scaling of microsatellite data, the haplogroups were established by haplotype estimation from multilocal genotypes followed by median joining network analysis, and the RAPD/multilocus enzyme electrophoresis typing was obtained from Brisse et al. [26].

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