Experimental microevolution of Trypanosoma cruzi reveals hybridization and clonal mechanisms driving rapid diversification of genome sequence and structure

  1. Gabriel Machado Matos
  2. Michael D Lewis
  3. Carlos Talavera-López
  4. Matthew Yeo
  5. Edmundo C Grisard
  6. Louisa A Messenger
  7. Michael Miles
  8. Björn Andersson  Is a corresponding author
  1. Universidade Federal de Santa Catarina, Brazil
  2. London School of Hygiene and Tropical Medicine, United Kingdom
  3. Helmholtz Zentrum München, Germany
  4. Karolinska Institute, Sweden

Abstract

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.

Data availability

The data generated in this study have been submitted to the NCBI BioProject database (https://www.ncbi.nlm.nih.gov/bioproject/) under accession number PRJNA748998.

The following data sets were generated

Article and author information

Author details

  1. Gabriel Machado Matos

    Universidade Federal de Santa Catarina, Florianopolis, Brazil
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3744-2673
  2. Michael D Lewis

    Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Carlos Talavera-López

    Helmholtz Zentrum München, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Matthew Yeo

    Department of Infection Biology, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Edmundo C Grisard

    Universidade Federal de Santa Catarina, Florianopolis, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  6. Louisa A Messenger

    Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Michael Miles

    Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Björn Andersson

    Department of Cell and Molecular Biology, Karolinska Institute, Stockholm, Sweden
    For correspondence
    bjorn.andersson@ki.se
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4624-0259

Funding

Swedish Research Council, Bjorn Andersson, Michael Miles (Project Grant)

  • Gabriel Machado Matos

CAPES, Edmundo Grisard, Bjorn Andersson (Student Scholarship)

  • Björn Andersson

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Antoine Claessens, University of Montpellier, France

Version history

  1. Preprint posted: October 24, 2021 (view preprint)
  2. Received: November 3, 2021
  3. Accepted: April 22, 2022
  4. Accepted Manuscript published: May 10, 2022 (version 1)
  5. Version of Record published: May 12, 2022 (version 2)
  6. Version of Record updated: May 13, 2022 (version 3)

Copyright

© 2022, Matos et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Gabriel Machado Matos
  2. Michael D Lewis
  3. Carlos Talavera-López
  4. Matthew Yeo
  5. Edmundo C Grisard
  6. Louisa A Messenger
  7. Michael Miles
  8. Björn Andersson
(2022)
Experimental microevolution of Trypanosoma cruzi reveals hybridization and clonal mechanisms driving rapid diversification of genome sequence and structure
eLife 11:e75237.
https://doi.org/10.7554/eLife.75237

Share this article

https://doi.org/10.7554/eLife.75237

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