Microevolution of Trypanosoma cruzi reveals hybridization and clonal mechanisms driving rapid genome diversification

Protozoa and fungi are known to have extraordinarily diverse mechanisms of genetic exchange. However, the presence and epidemiological relevance of genetic exchange in Trypanosoma cruzi, the agent of Chagas disease, has been controversial and debated for many years. Field studies have identified bot...

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Main Authors: Gabriel Machado Matos, Michael D Lewis, Carlos Talavera-López, Matthew Yeo, Edmundo C Grisard, Louisa A Messenger, Michael A Miles, Björn Andersson
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-05-01
Series:eLife
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Online Access:https://elifesciences.org/articles/75237
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author Gabriel Machado Matos
Michael D Lewis
Carlos Talavera-López
Matthew Yeo
Edmundo C Grisard
Louisa A Messenger
Michael A Miles
Björn Andersson
author_facet Gabriel Machado Matos
Michael D Lewis
Carlos Talavera-López
Matthew Yeo
Edmundo C Grisard
Louisa A Messenger
Michael A Miles
Björn Andersson
author_sort Gabriel Machado Matos
collection DOAJ
description Protozoa and fungi are known to have extraordinarily diverse mechanisms of genetic exchange. However, the presence and epidemiological relevance of genetic exchange in Trypanosoma cruzi, the agent of Chagas disease, has been controversial and debated for many years. Field studies have identified both predominantly clonal and sexually recombining natural populations. Two of six natural T. cruzi lineages (TcV and TcVI) show hybrid mosaicism, using analysis of single-gene locus markers. The formation of hybrid strains in vitro has been achieved and this provides a framework to study the mechanisms and adaptive significance of genetic exchange. Using whole genome sequencing of a set of experimental hybrids strains, we have confirmed that hybrid formation initially results in tetraploid parasites. The hybrid progeny showed novel mutations that were not attributable to either (diploid) parent showing an increase in amino acid changes. In long-term culture, up to 800 generations, there was a variable but gradual erosion of progeny genomes towards triploidy, yet retention of elevated copy number was observed at several core housekeeping loci. Our findings indicate hybrid formation by fusion of diploid T. cruzi, followed by sporadic genome erosion, but with substantial potential for adaptive evolution, as has been described as a genetic feature of other organisms, such as some fungi.
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spelling doaj.art-54b78a580153477c8d8183ed3a7e93292022-12-22T04:29:02ZengeLife Sciences Publications LtdeLife2050-084X2022-05-011110.7554/eLife.75237Microevolution of Trypanosoma cruzi reveals hybridization and clonal mechanisms driving rapid genome diversificationGabriel Machado Matos0https://orcid.org/0000-0003-3744-2673Michael D Lewis1Carlos Talavera-López2Matthew Yeo3Edmundo C Grisard4Louisa A Messenger5Michael A Miles6Björn Andersson7https://orcid.org/0000-0002-4624-0259Departamento de Biologia Celular, Embriologia e Genética, Universidade Federal de Santa Catarina, Florianopolis, Brazil; Department of Cell and Molecular Biology, Karolinska Institute, Stockholm, SwedenFaculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United KingdomDepartment of Cell and Molecular Biology, Karolinska Institute, Stockholm, Sweden; Institute of Computational Biology, Computational Health Centre, Helmholtz Munich, Munich, GermanyFaculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United KingdomDepartamento de Microbiologia, Imunologia e Parasitologia, Universidade Federal de Santa Catarina, Florianopolis, BrazilFaculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United KingdomFaculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United KingdomDepartment of Cell and Molecular Biology, Karolinska Institute, Stockholm, SwedenProtozoa and fungi are known to have extraordinarily diverse mechanisms of genetic exchange. However, the presence and epidemiological relevance of genetic exchange in Trypanosoma cruzi, the agent of Chagas disease, has been controversial and debated for many years. Field studies have identified both predominantly clonal and sexually recombining natural populations. Two of six natural T. cruzi lineages (TcV and TcVI) show hybrid mosaicism, using analysis of single-gene locus markers. The formation of hybrid strains in vitro has been achieved and this provides a framework to study the mechanisms and adaptive significance of genetic exchange. Using whole genome sequencing of a set of experimental hybrids strains, we have confirmed that hybrid formation initially results in tetraploid parasites. The hybrid progeny showed novel mutations that were not attributable to either (diploid) parent showing an increase in amino acid changes. In long-term culture, up to 800 generations, there was a variable but gradual erosion of progeny genomes towards triploidy, yet retention of elevated copy number was observed at several core housekeeping loci. Our findings indicate hybrid formation by fusion of diploid T. cruzi, followed by sporadic genome erosion, but with substantial potential for adaptive evolution, as has been described as a genetic feature of other organisms, such as some fungi.https://elifesciences.org/articles/75237Trypanosoma cruzigenetic exchangehybrid formationcomparative genomicsmicroevolutionrecombination
spellingShingle Gabriel Machado Matos
Michael D Lewis
Carlos Talavera-López
Matthew Yeo
Edmundo C Grisard
Louisa A Messenger
Michael A Miles
Björn Andersson
Microevolution of Trypanosoma cruzi reveals hybridization and clonal mechanisms driving rapid genome diversification
eLife
Trypanosoma cruzi
genetic exchange
hybrid formation
comparative genomics
microevolution
recombination
title Microevolution of Trypanosoma cruzi reveals hybridization and clonal mechanisms driving rapid genome diversification
title_full Microevolution of Trypanosoma cruzi reveals hybridization and clonal mechanisms driving rapid genome diversification
title_fullStr Microevolution of Trypanosoma cruzi reveals hybridization and clonal mechanisms driving rapid genome diversification
title_full_unstemmed Microevolution of Trypanosoma cruzi reveals hybridization and clonal mechanisms driving rapid genome diversification
title_short Microevolution of Trypanosoma cruzi reveals hybridization and clonal mechanisms driving rapid genome diversification
title_sort microevolution of trypanosoma cruzi reveals hybridization and clonal mechanisms driving rapid genome diversification
topic Trypanosoma cruzi
genetic exchange
hybrid formation
comparative genomics
microevolution
recombination
url https://elifesciences.org/articles/75237
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