1. Biochemistry and Chemical Biology
  2. Genetics and Genomics
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Evolution of substrate specificity in a retained enzyme driven by gene loss

  1. Ana Lilia Juárez-Vázquez
  2. Janaka E Edirisinghe
  3. Ernesto A Verduzco-Castro
  4. Karolina Michalska
  5. Chenggang Wu
  6. Lianet Noda-García
  7. Gyorgy Babnigg
  8. Michael Endres
  9. Sofía Medina-Ruíz
  10. Julián Santoyo-Flores
  11. Mauricio Carrillo-Tripp
  12. Hung Ton-That
  13. Andrzej Joachimiak
  14. Christopher S Henry
  15. Francisco Barona-Gómez  Is a corresponding author
  1. Evolution of Metabolic Diversity Laboratory, Mexico
  2. Argonne National Laboratory, United States
  3. University of Texas Health Science Cent, United States
  4. Weizmann Institute of Science, Israel
  5. University of California, Berkeley, United States
  6. Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Mexico
  7. Centro de Investigación en Matemáticas, Mexico
  8. University of Texas Health Science Center, United States
Research Article
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Cite this article as: eLife 2017;6:e22679 doi: 10.7554/eLife.22679

Abstract

The connection between gene loss and the functional adaptation of retained proteins is still poorly understood. We apply phylogenomics and metabolic modeling to detect bacterial species that are evolving by gene loss, with the finding that Actinomycetaceae genomes from human cavities are undergoing sizable reductions, including loss of L-histidine and L-tryptophan biosynthesis. We observe that the dual-substrate phosphoribosyl isomerase A or priA gene, at which these pathways converge, appears to coevolve with the occurrence of trp and his genes. Characterization of a dozen PriA homologs shows that these enzymes adapt from bifunctionality in the largest genomes, to a monofunctional, yet not necessarily specialized, inefficient form in genomes undergoing reduction. These functional changes are accomplished via mutations, which result from relaxation of purifying selection, in residues structurally mapped after sequence and X-ray structural analyses. Our results show how gene loss can drive the evolution of substrate specificity from retained enzymes.

Article and author information

Author details

  1. Ana Lilia Juárez-Vázquez

    Evolution of Metabolic Diversity Laboratory, Irapuato, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  2. Janaka E Edirisinghe

    Computing, Environment and Life Sciences Directorate, Argonne National Laboratory, Lemont, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Ernesto A Verduzco-Castro

    Evolution of Metabolic Diversity Laboratory, Irapuato, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  4. Karolina Michalska

    Midwest Center for Structural Genomics, Biosciences Division, Argonne National Laboratory, Lemont, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Chenggang Wu

    Department of Microbiology and Molecular Genetics, University of Texas Health Science Cent, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Lianet Noda-García

    Department of Biological Chemistry, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  7. Gyorgy Babnigg

    Midwest Center for Structural Genomics, Biosciences Division, Argonne National Laboratory, Lemont, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Michael Endres

    Midwest Center for Structural Genomics, Biosciences Division, Argonne National Laboratory, Lemont, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Sofía Medina-Ruíz

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Julián Santoyo-Flores

    Laboratorio de la Diversidad Biomolecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Irapuato, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  11. Mauricio Carrillo-Tripp

    Ciencias de la Computación, Centro de Investigación en Matemáticas, Guanajuato, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  12. Hung Ton-That

    Department of Microbiology and Molecular Genetics, University of Texas Health Science Center, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Andrzej Joachimiak

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Christopher S Henry

    Computing, Environment and Life Sciences Directorate, Argonne National Laboratory, Lemont, United States
    Competing interests
    The authors declare that no competing interests exist.
  15. Francisco Barona-Gómez

    Evolution of Metabolic Diversity Laboratory, Irapuato, Mexico
    For correspondence
    francisco.barona@cinvestav.mx
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1492-9497

Funding

Consejo Nacional de Ciencia y Tecnología (132376,179290)

  • Ana Lilia Juárez-Vázquez
  • Ernesto A Verduzco-Castro
  • Julián Santoyo-Flores
  • Mauricio Carrillo-Tripp

National Institutes of Health (GM094585)

  • Karolina Michalska
  • Gyorgy Babnigg
  • Michael Endres
  • Andrzej Joachimiak

US Department of Energy (DE-AC02-06CH11357)

  • Andrzej Joachimiak
  • Christopher S Henry

National Science Foundation (1611952)

  • Janaka E Edirisinghe
  • Christopher S Henry

National Institute of Dental and Craniofacial Research (DE017382)

  • Chenggang Wu
  • Hung Ton-That

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

Reviewing Editor

  1. Alfonso Valencia, Barcelona Supercomputing Center - BSC, Spain

Publication history

  1. Received: October 25, 2016
  2. Accepted: March 25, 2017
  3. Accepted Manuscript published: March 31, 2017 (version 1)
  4. Version of Record published: April 25, 2017 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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