Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-23T07:29:48.297Z Has data issue: false hasContentIssue false
  • English
  • Français

Evaluation of the multispecies coalescent method to explore intra-Trypanosoma cruzi I relationships and genetic diversity

Published online by Cambridge University Press:  03 May 2019

César Gómez-Hernández ,
Sergio D. Pérez ,
Karine Rezende-Oliveira ,
Cecilia G. Barbosa ,
Eliane Lages-Silva ,
Luis Eduardo Ramírez  and
Juan David Ramírez Open the ORCID record for Juan David Ramírez [Opens in a new window]
César Gómez-Hernández
Affiliation:
Laboratorio de Parasitologia, Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
Sergio D. Pérez
Affiliation:
Grupo de Investigaciones Microbiológicas-UR (GIMUR), Programa de Biología, Facultad de Ciencias Naturales y Matemáticas, Universidad del Rosario, Bogotá, Colombia
Karine Rezende-Oliveira
Affiliation:
Laboratorio de Ciências Biomédicas, Universidade Federal de Uberlândia, Campus do Pontal, Ituiutaba, Minas Gerais, Brazil
Cecilia G. Barbosa
Affiliation:
Laboratorio de Parasitologia, Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
Eliane Lages-Silva
Affiliation:
Laboratorio de Parasitologia, Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
Luis Eduardo Ramírez
Affiliation:
Laboratorio de Parasitologia, Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
Juan David Ramírez*
Affiliation:
Grupo de Investigaciones Microbiológicas-UR (GIMUR), Programa de Biología, Facultad de Ciencias Naturales y Matemáticas, Universidad del Rosario, Bogotá, Colombia
*
Author for correspondence: Juan David Ramírez, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Chagas Disease is a zoonosis caused by the parasite Trypanosoma cruzi. Several high-resolution markers have subdivided T. cruzi taxon into at least seven lineages or Discrete Typing Units (DTUs) (TcI-TcVI and TcBat). Trypanosoma cruzi I is the most diverse and geographically widespread DTU. Recently a TcI genotype related to domestic cycles was proposed and named as TcIDOM. Herein, we combined traditional markers and housekeeping genes and applied a Multispecies Coalescent method to explore intra-TcI relationships, lineage boundaries and genetic diversity in a random set of isolates and DNA sequences retrieved from Genbank from different countries in the Americas. We found further evidence supporting TcIDOM as an independent and emerging genotype of TcI at least in Colombia and Venezuela. We also found evidence of high phylogenetic incongruence between parasite's gene trees (including introgression) and embedded species trees, and a lack of genetic structure among geography and hosts, illustrating the complex dynamics and epidemiology of TcI across the Americas. These findings provide novel insights into T. cruzi systematics and epidemiology and support the need to assess parasite diversity and lineage boundaries through hypothesis testing using different approaches to those traditionally employed, including the Bayesian Multispecies coalescent method.

Keywords

Chagas diseasediscrete typing unitgenotypehousekeeping geneslineagemultispecies coalescent
Type
Research Article
Information
Parasitology , Volume 146 , Issue 8 , July 2019 , pp. 1063 - 1074
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors made equal contributions.

References

Barnabé, C, Mobarec, HI, Jurado, MR, Cortez, JA and Brenière, SF (2016) Reconsideration of the seven discrete typing units within the species Trypanosoma cruzi, a new proposal of three reliable mitochondrial clades. Infect Genet Evol. 39, 176–186.Google Scholar
Bouckaert, R and Drummond, A (2017) Bmodeltest: bayesian phylogenetic site model averaging and model comparison. BMC Evolutionary Biology 17, 42.Google Scholar
Bouckaert, R, Heled, J, Kühnert, D, Vaughan, T, Wu, C, Xie, D, … Drummond, A (2014) BEAST 2: a software platform for bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537.Google Scholar
Brenière, S, Waleckx, E and Barnabé, C (2016) Over six thousand Trypanosoma cruzi strains classified into Discrete Typing Units (DTUs): attempt at an inventory. PLOS Neglected Tropical Diseases 10, e0004792.Google Scholar
Brisse, S, Barnabé, C, Bañuls, A, Sidibé, I, Noël, S and Tibayrenc, M (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. Molecular and Biochemical Parasitology 92, 253–263.Google Scholar
Brisse, S, Henriksson, J, Barnabé, C, Douzery, E, Berkvens, D, Serrano, M, … Tibayrenc, M (2003) Evidence for genetic exchange and hybridization in Trypanosoma cruzi based on nucleotide sequences and molecular karyotype. Infection, Genetics and Evolution 2, 173–183.Google Scholar
Burgos, J, Altcheh, J, Bisio, M, Duffy, T, Valadares, H, Seidenstein, M, … Schijman, A (2007) Direct molecular profiling of minicircle signatures and lineages of Trypanosoma cruzi bloodstream populations causing congenital Chagas disease. International Journal for Parasitology 37, 1319–1327.Google Scholar
Burgos, J, Diez, M, Vigliano, C, Bisio, M, Risso, M, Duffy, T, … Schijman, A (2010) Molecular identification of Trypanosoma cruzi discrete typing units in end-stage chronic chagas heart disease and reactivation after heart transplantation. Clinical Infectious Diseases 51, 485–495.Google Scholar
Cosentino, R and Agüero, F (2012) A simple strain typing assay for Trypanosoma cruzi: discrimination of major evolutionary lineages from a single amplification product. PLoS Neglected Tropical Diseases 6, e1777.Google Scholar
Cottontail, V, Kalko, E, Cottontail, I, Wellinghausen, N, Tschapka, M, Perkins, S and Pinto, C (2014) High local diversity of Trypanosoma in a common bat species, and implications for the biogeography and taxonomy of the T. cruzi clade. PLoS ONE 9, e108603.Google Scholar
Cruz, L, Vivas, A, Montilla, M, Hernández, C, Flórez, C, Parra, E and Ramírez, JD (2015) Comparative study of the biological properties of Trypanosoma cruzi I genotypes in a murine experimental model. Infection, Genetics and Evolution 29, 110–117.Google Scholar
Cura, C, Mejía-Jaramillo, A, Duffy, T, Burgos, J, Rodriguero, M, Cardinal, M, … Gürtler, R (2010) Trypanosoma cruzi I genotypes in different geographical regions and transmission cycles based on a microsatellite motif of the intergenic spacer of spliced-leader genes. International Journal for Parasitology 40, 1599–1607.Google Scholar
de Freitas, J, Augusto-Pinto, L, Pimenta, J, Bastos-Rodrigues, L, Gonçalves, V, Teixeira, S, … Pena, S (2006) Ancestral genomes, sex, and the population structure of Trypanosoma cruzi. PLoS Pathogens 2, e24.Google Scholar
Degnan, JH and Rosenberg, NA (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends in Ecology & Evolution 24, 332–340.Google Scholar
De Meeûs, T, McCoy, KD, Prugnolle, F, Chevillon, C, Durand, P, Hurtrez-Bousses, S and Renaud, FJI and Genetics and Evolution. (2007) Population genetics and molecular epidemiology or how to “débusquer la bête”. 7, 308–332.Google Scholar
Diosque, P, Tomasini, N, Lauthier, J, Messenger, L, Monje Rumi, M, Ragone, P, … Yeo, M (2014) Optimized Multilocus Sequence Typing (MLST) scheme for Trypanosoma cruzi. PLoS Neglected Tropical Diseases 8, e3117.Google Scholar
Edgar, R (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.Google Scholar
Flores-Lopez, CA and Machado, CA (2011) Analyses of 32 loci clarify phylogenetic relationships among Trypanosoma cruzi lineages and support a single hybridization prior to human contact. PLoS Neglected Tropical Diseases 5, e1272.Google Scholar
Fujita, M, Leaché, A, Burbrink, F, McGuire, J and Moritz, C (2012) Coalescent-based species delimitation in an integrative taxonomy. Trends in Ecology & Evolution 27, 480–488.Google Scholar
Gómez-Hernández, C, Rezende-Oliveira, K, Nascentes, G, Batista, L, Kappel, H, Martinez-Ibarra, J, … Ramírez, L (2011) Molecular characterization of Trypanosoma cruzi Mexican strains and their behavior in the mouse experimental model. Revista da Sociedade Brasileira de Medicina Tropical 44, 684–690.Google Scholar
Gómez-Palacio, A, Lopera, J, Rojas, W, Bedoya, G, Cantillo-Barraza, O, Marín-Suarez, J, … Mejía-Jaramillo, A (2016) Multilocus analysis indicates that Trypanosoma cruzi I genetic substructure associated with sylvatic and domestic cycles is not an attribute conserved throughout Colombia. Infection, Genetics and Evolution 38, 35–43.Google Scholar
Hall, B, Meredith, E and Wilkinson, S (2012) Targeting the substrate preference of a type I nitroreductase to develop antitrypanosomal quinone-based prodrugs. Antimicrobial Agents and Chemotherapy 56, 5821–5830.Google Scholar
Heled, J and Drummond, A (2009) Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution 27, 570–580.Google Scholar
Herrera, C, Bargues, M, Fajardo, A, Montilla, M, Triana, O, Vallejo, G and Guhl, F (2007) Identifying four Trypanosoma cruzi I isolate haplotypes from different geographic regions in Colombia. Infection, Genetics and Evolution 7, 535–539.Google Scholar
Herrera, C, Guhl, F, Falla, A, Fajardo, A, Montilla, M, Adolfo Vallejo, G and Bargues, M (2009) Genetic variability and phylogenetic relationships with in Trypanosoma cruzi I isolated in Colombia based on miniexon gene sequences. Journal of Parasitology Research 1–9, pii: 897364.Google Scholar
Hey, J and Pinho, C (2012) Population genetics and objectivity in species diagnosis. Evolution 66, 1413–1429.Google Scholar
Jansen, A, Xavier, SCC and Roque, A (2017) Ecological aspects of Trypanosoma cruzi. American Trypanosomiasis Chagas Disease: One Hundred Years of Research: Elsevier.Google Scholar
Joly, S, McLenachan, PA and Lockhart, P (2009) A statistical approach for distinguishing hybridization and incomplete lineage sorting. The American Naturalist 174, E54–E70.Google Scholar
Justi, SA and Galvão, C (2017) The evolutionary origin of diversity in chagas disease vectors. Trends in Parasitology 33, 42–52.Google Scholar
Lauthier, J, Tomasini, N, Barnabé, C, Rumi, M, D'Amato, A, Ragone, P, … Diosque, P (2012) Candidate targets for multilocus sequence typing of Trypanosoma cruzi: validation using parasite stocks from the Chaco Region and a set of reference strains. Infection, Genetics and Evolution 12, 350–358.Google Scholar
Leaché, AD, Koo, MS, Spencer, CL, Papenfuss, TJ, Fisher, RN and McGuire, JA (2009) Quantifying ecological, morphological, and genetic variation to delimit species in the coast horned lizard species complex (Phrynosoma). PNAS 106, 12418–12423.Google Scholar
Leigh, J and Bryant, D (2015) Popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.Google Scholar
Letunic, I and Bork, P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Research 4, 1.Google Scholar
Lewis, MD, Llewellyn, MS, Yeo, M, Acosta, N, Gaunt, MW and Miles, MA (2011) Recent, independent and anthropogenic origins of Trypanosoma cruzi hybrids. PLoS Neglected Tropical Diseases 5, e1363.Google Scholar
León, CM, Hernández, C, Montilla, M and Ramírez, JD (2015) Retrospective distribution of Trypanosoma cruzi I genotypes in Colombia. Memórias do Instituto Oswaldo Cruz 110, 387–393.Google Scholar
León, C, Montilla, M, Vanegas, R, Castillo, M, Parra, E and Ramírez, JD (2016) Murine models susceptibility to distinct Trypanosoma cruzi I genotypes infection. Parasitology 144, 512–519.Google Scholar
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics (Oxford, England) 25, 1451–1452.Google Scholar
Lima, V, Jansen, A, Messenger, L, Miles, M and Llewellyn, M (2014) Wild Trypanosoma cruzi I genetic diversity in Brazil suggests admixture and disturbance in parasite populations from the Atlantic Forest region. Parasites and Vectors 7, 263.Google Scholar
Lima, L, Espinosa-Álvarez, O, Ortiz, PA, Trejo-Varón, JA, Carranza, JC, Pinto, CM, Serrano, MG, Buck, GA, Camargo, EP, Teixeira, MM (2015) Genetic diversity of Trypanosoma cruzi in bats, and multilocus phylogenetic and phylogeographical analyses supporting Tcbat as an independent DTU (discrete typing unit). Acta Trop 151, 166–77.Google Scholar
Llewellyn, M, Lewis, M, Acosta, N, Yeo, M, Carrasco, H, Segovia, M, … Gaunt, M (2009 a) Trypanosoma cruzi IIc: phylogenetic and phylogeographic insights from sequence and microsatellite analysis and potential impact on emergent chagas disease. PLoS Neglected Tropical Diseases 3, e510.Google Scholar
Llewellyn, MS, Miles, MA, Carrasco, HJ, Lewis, MD, Yeo, M, Vargas, J, Torrico, F, Diosque, P, Valente, V, Valente, SA and Gaunt, MW (2009 b) Genome-Scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection. PLoS Pathogens 5, e1000410.Google Scholar
Llewellyn, MS, Miles, MA, Carrasco, HJ, L, MD, Yeo, M, Vargas, J, … Gaunt, MW (2009 c) Genome-scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection. PLoS Pathogens 5, e1000410.Google Scholar
Marcili, A, Lima, L, Cavazzana, M, Junqueira, AC, Veludo, HH, Maia Da Silva, F, … Teixeira, MM (2009) A new genotype of Trypanosoma cruzi associated with bats evidenced by phylogenetic analyses using SSU rDNA, cytochrome b and Histone H2B genes and genotyping based on ITS1 rDNA. Parasitology 136, 641–655.Google Scholar
Messenger, L, Llewellyn, M, Bhattacharyya, T, Franzén, O, Lewis, M, Ramírez, J, … Miles, M (2012) Multiple mitochondrial introgression events and heteroplasmy in Trypanosoma cruzi revealed by maxicircle MLST and next generation sequencing. PLoS Neglected Tropical Diseases 6, e1584.Google Scholar
Nicholas, KB, Nicholas, HBJ and Deerfield, DWI (1997) Genedoc: analysis and visualization of genetic variation. EMBNEW News 4.Google Scholar
Ogilvie, H, Bouckaert, R and Drummond, A (2017) StarBEAST2 brings faster species tree inference and accurate estimates of substitution rates. Molecular Biology and Evolution 34, 2101–2114.Google Scholar
Poveda, C, Higuera, A, Urbano, P and Ramírez, J (2017) Ecology of Trypanosoma cruzi I genotypes across Rhodnius prolixus captured in Attalea butyracea palms. Infection, Genetics and Evolution 49, 146–150.Google Scholar
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Tracer v1.6. Disponible en. Available at http://tree.bio.ed.ac.uk/software/tracer/.Google Scholar
Ramírez, J and Llewellyn, M (2014) Reproductive clonality in protozoan pathogens-truth or artefact? Molecular Ecology 23, 4195–4202.Google Scholar
Ramírez, J and Hernández, C (2018) Trypanosoma cruzi I: Towards the need of genetic subdivision?, Part II. Acta Tropica, In Press, Corrected Proof.Google Scholar
Ramírez, J, Duque, M and Guhl, F (2011) Phylogenetic reconstruction based on Cytochrome b (Cytb) gene sequences reveals distinct genotypes within Colombian Trypanosoma cruzi I populations. Acta Tropica 119, 61–65.Google Scholar
Ramírez, J, Guhl, F, Messenger, L, Lewis, M, Montilla, M, Cucunuba, Z, … Llewellyn, M (2012) Contemporary cryptic sexuality in Trypanosoma cruzi. Molecular Ecology 21, 4216–4226.Google Scholar
Ramírez, J, Tapia-Calle, G and Guhl, F (2013) Genetic structure of Trypanosoma cruzi in Colombia revealed by a High-throughput Nuclear Multilocus Sequence Typing (nMLST) approach. BMC Genetics 14, 96.Google Scholar
Ramírez, JD, Hernández, C, Montilla, M, Zambrano, P, Flórez, AC, Parra, E and Cucunubá, ZM (2014) First report of human Trypanosoma cruzi infection attributed to TcBat genotype. Zoonosis and Public Health 61, 477–479.Google Scholar
Shapiro, BJ, Leducq, JB and Mallet, J (2016) What Is Speciation? PLoS Genet. 12, e1005860.Google Scholar
Tomasini, N and Diosque, P (2015) Evolution of Trypanosoma cruzi: clarifying hybridisations, mitochondrial introgressions and phylogenetic relationships between major lineages. Memórias do Instituto Oswaldo Cruz 110, 403–413.Google Scholar
Tomasini, N, Lauthier, J, Rumi, M, Ragone, P, D'Amato, A, Brandan, C, … Diosque, P (2011) Interest and limitations of Spliced Leader Intergenic Region sequences for analyzing Trypanosoma cruzi I phylogenetic diversity in the Argentinean Chaco. Infection, Genetics and Evolution 11, 300–307.Google Scholar
Westenberger, S, Barnabé, C, Campbell, DA and Sturm, NR (2005) Two hybridization events define the population structure of Trypanosoma cruzi. Genetics 171, 527–543.Google Scholar
(WHO), WHO (2016) Global Burden of Disease Estimates for 2000–2015. In. Geneva.Google Scholar
Yang, Z and Rannala, BJPOTNAOS (2010) Bayesian species delimitation using multilocus sequence data. 200913022.Google Scholar
Yeo, M, Mauricio, I, Messenger, L, Lewis, M, Llewellyn, M, Acosta, N, … Miles, M (2011) Multilocus Sequence Typing (MLST) for lineage assignment and high resolution diversity studies in Trypanosoma cruzi. PLoS Neglected Tropical Diseases 5, e1049.Google Scholar
Zingales, B, Miles, M, Campbell, D, Tibayrenc, M, Macedo, A, Teixeira, M, … Sturm, N (2012) The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infection, Genetics and Evolution 12, 240–253.Google Scholar
Zumaya-Estrada, F, Messenger, L, Lopez-Ordonez, T, Lewis, M, Flores-Lopez, C, Martínez-Ibarra, A, … Llewellyn, M (2012) North American import? Charting the origins of an enigmatic Trypanosoma cruzi domestic genotype. Parasites & Vectors 5, 226.Google Scholar
Supplementary material: File

Gómez-Hernández et al. supplementary material

Gómez-Hernández et al. supplementary material 1

Download Gómez-Hernández et al. supplementary material(File)
File 7.2 KB
Supplementary material: Image

Gómez-Hernández et al. supplementary material

Gómez-Hernández et al. supplementary material 2

Download Gómez-Hernández et al. supplementary material(Image)
Image 788.6 KB
Supplementary material: File

Gómez-Hernández et al. supplementary material

Gómez-Hernández et al. supplementary material 3

Download Gómez-Hernández et al. supplementary material(File)
File 15.4 KB
Supplementary material: File

Gómez-Hernández et al. supplementary material

Gómez-Hernández et al. supplementary material 4

Download Gómez-Hernández et al. supplementary material(File)
File 5.4 KB