Genome Evolution of Trypanosoma cruzi

Abstract

The protozoan parasite Trypanosoma cruzi is the etiologic agent of Chagas disease which is a major public health problem in Latin America. T. cruzi isolates have been classified into six main lineages (TcI–TcVI) based on genetics, phylogeographical and epidemiological studies. Its genome is complex, with a high variability among isolates, mainly as result of differences in the amount of repetitive sequences such as multigenic families encoding surface proteins and retrotransposons. Despite genome size variation and karyotype polymorphism, T. cruzi exhibits high conservation of chromosome structure with large syntenic groups conserved among all isolates. Comparison between Trypanosoma brucei and T. cruzi genomes suggests the occurrence of fusion and split events involving the chromosomes of these two species.

Key Concepts:

  • Trypanosoma cruzi chromatin is poorly condensed during cell division, which precludes the use of conventional cytogenetic analysis.

  • Chromosomal bands can be separated by Pulsed‐Field Gel Electrophoresis (PFGE). A chromosomal band may contain co‐migrating chromosomes, which are not necessarily homologous.

  • The exact number of chromosomes remains unknown.

  • T. cruzi is essentially diploid, although some larger aneuploid fragments have been described.

  • Six distinct T. cruzi lineages have been proposed on the basis of geographical, phylogenetic and epidemiological studies.

  • Large syntenic regions are conserved among T. cruzi isolates and also between trypanosomatids. T. cruzi lineages exhibit a striking conservation of chromosome structure.

  • The T. cruzi centromeric region consists of a GC‐rich strand‐switch domain composed mainly of degenerated retrotransposons.

  • T. cruzi telomeres are composed of tandem repeats of the hexamer TTAGGG followed by a 189 bp species‐specific sequence.

  • The subtelomeric region is enriched with members of surface protein gene families and could be a site of generation of new variants of surface antigens.

  • The mapping of the syntenic regions on T. cruzi chromosomal bands provides evidence of the occurrence of fusion and split events involving T. brucei and T. cruzi chromosomes.

Keywords: Trypanosoma cruzi; genome size; repetitive sequences; multigenic families; chromosome assembly; synteny; chromosomal evolution

Figure 1.

Molecular karyotype of isolates from different Trypanosoma cruzi lineages. Chromosomal bands were separated by Pulsed Field Gel Electrophoresis (PFGE) and stained with ethidium bromide. The following isolates were used: clone DM28c (DM), G (G) and Trycc:1161 (Trycc) strains (TcI), Y strain (Y) and clone Esmeraldo‐cl3 (Esm) (TcII), SO3‐cl5 (SO3) (TcV) and CL Brener (TcVI). Sizes of Hansenula wingei. (H.w.) chromosomal bands used as reference pattern are indicated at left in megabases.

Figure 2.

Schematic representation of the chromosomal end of Trypanosoma cruzi. The red box represented the telomere with the single strand followed by the telomeric repeat and the blue box the 189 bp telomeric junction. The subtelomeric region is enriched with Retrotransposons Hot Spot (RHS) genes (green box), trans‐sialidase (pink box), and Dispersed Gene Family 1 (DGF‐1) (yellow box) genes. The retrotransposons (light blue) are also abundant in subtelomeric region. The grey box represents the interstitial chromosomal region. Schematic drawing according the results of Chiurillo et al. () and Kim et al. ().

Figure 3.

Split and fusion events between T. cruzi and T. brucei chromosomes. (a) Comparison between homologous regions of T. cruzi and T. brucei chromosomes Tb11 and Tb9. The homologous regions of chromosomes located in XVIII and V bands (green box) and the end of chromosome located in XVI band (blue box) comprise the beginning and the end of Tb9, respectively. The beginning of chromosome located in XVI band and the entire T. cruzi chromosomes located in bands IX and VII, XII, and XI and I were assigned to different regions of Tb11. Soft and dark grey blocks represent T. cruzi and T. brucei chromosomes, respectively. (b) Chromosomal bands of clone CL Brener separated by PFGE and stained with ethidium bromide. Chromosomal bands were numbered by roman numbers (I–XX) starting with the small bands. (c) Markers XM_803658 and katanin located in T. cruzi homologous regions to Tb9 were hybridised with chromosomal bands of clone CL Brener. (d) Markers located in T. cruzi homologous regions to Tb11 were hybridised with chromosomal bands of clone CL Brener. Modified from Souza et al. doi:10.1371/journal.pone.0023042. Paper published under Creative Commons Attribution License (CCAL) license terms (http://creativecommons.org/licenses/by/2.5/).

Figure 4.

Models of evolution of trypanosome genome. In the first model (a) the common ancestor had large chromosomes as observed in T. brucei and several events of cleavage generated smaller chromosomes of T. cruzi. The second model (b) the common ancestor had small chromosomes as observed in T. cruzi and fusion events lead to the formation of large chromosomes observed in T. brucei.

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Further Reading

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Souza, Renata T, Marini, Marjorie M, and da Silveira, José Franco(Jun 2012) Genome Evolution of Trypanosoma cruzi. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023977]