Fine-tuning citrate synthase flux potentiates and refines metabolic innovation in the Lenski evolution experiment

  1. Erik M Quandt
  2. Jimmy Gollihar
  3. Zachary D Blount
  4. Andrew D Ellington
  5. George Georgiou
  6. Jeffrey E Barrick  Is a corresponding author
  1. University of Texas at Austin, United States
  2. Michigan State University, United States

Abstract

Evolutionary innovations that enable organisms to colonize new ecological niches are rare compared to gradual evolutionary changes in existing traits. We discovered that key mutations in the gltA gene, which encodes citrate synthase (CS), occurred both before and after Escherichia coli gained the ability to grow aerobically on citrate (Cit+ phenotype) during the Lenski long-term evolution experiment. The first gltA mutation, which increases CS activity by disrupting NADH-inhibition of this enzyme, is beneficial for growth on the acetate and contributed to preserving the rudimentary Cit+ trait from extinction when it first evolved. However, after Cit+ was refined by further mutations, this potentiating gltA mutation became deleterious to fitness. A second wave of beneficial gltA mutations then evolved that reduced CS activity to below the ancestral level. Thus, dynamic reorganization of central metabolism made colonizing this new nutrient niche contingent on both co-opting and overcoming a history of prior adaptation.

Article and author information

Author details

  1. Erik M Quandt

    Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jimmy Gollihar

    Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Zachary D Blount

    BEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Andrew D Ellington

    Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. George Georgiou

    Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Jeffrey E Barrick

    Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, United States
    For correspondence
    jbarrick@cm.utexas.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Daniel J Kliebenstein, University of Copenhagen, Denmark

Publication history

  1. Received: June 25, 2015
  2. Accepted: October 13, 2015
  3. Accepted Manuscript published: October 14, 2015 (version 1)
  4. Version of Record published: December 15, 2015 (version 2)

Copyright

© 2015, Quandt 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. Erik M Quandt
  2. Jimmy Gollihar
  3. Zachary D Blount
  4. Andrew D Ellington
  5. George Georgiou
  6. Jeffrey E Barrick
(2015)
Fine-tuning citrate synthase flux potentiates and refines metabolic innovation in the Lenski evolution experiment
eLife 4:e09696.
https://doi.org/10.7554/eLife.09696
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