Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environment

  1. Zachary David Blount  Is a corresponding author
  2. Rohan Maddamsetti  Is a corresponding author
  3. Nkrumah A Grant  Is a corresponding author
  4. Sumaya T Ahmed
  5. Tanush Jagdish
  6. Jessica A Baxter
  7. Brooke A Sommerfeld
  8. Alice Tillman
  9. Jeremy Moore
  10. Joan L Slonczewski
  11. Jeffrey E Barrick
  12. Richard E Lenski
  1. Michigan State University, United States
  2. Harvard Medical School, United States
  3. Kenyon College, United States
  4. University of Texas at Austin, United States

Abstract

Evolutionary innovations allow populations to colonize new ecological niches. We previously reported that aerobic growth on citrate (Cit+) evolved in an Escherichia coli population during adaptation to a minimal glucose medium containing citrate (DM25). Cit+ variants can also grow in citrate-only medium (DM0), a novel environment for E. coli. To study adaptation to this new niche, we founded two sets of Cit+ populations and evolved them for 2,500 generations in DM0 or DM25. The evolved lineages acquired numerous parallel mutations, many mediated by transposable elements. Several also evolved amplifications of regions containing the maeA gene. Unexpectedly, some evolved populations and clones show apparent declines in fitness. We also found evidence of substantial cell death in Cit+ clones. Our results thus demonstrate rapid novel trait refinement and adaptation to the novel citrate niche, while also suggesting a recalcitrant mismatch between E. coli physiology and growth on citrate.

Data availability

All analysis and statistical scripts have been deposited at www.datadryad.org (https://doi.org/10.5061/dryad.7wm37pvpp). RNA-Seq data have been deposited in the NCBI SRA under accession PRJNA553503. Genome sequencing data have been deposited in the NCBI SRA under accession PRJNA595472. Analysis code is also available at: https://github.com/rohanmaddamsetti/DM0-evolution.

The following data sets were generated

Article and author information

Author details

  1. Zachary David Blount

    Microbiology and Molecular Genetics; BEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, United States
    For correspondence
    zachary.david.blount@gmail.com
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5153-0034
  2. Rohan Maddamsetti

    Systems Biology, Harvard Medical School, Boston, United States
    For correspondence
    rohan.maddamsetti@gmail.com
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3370-092X
  3. Nkrumah A Grant

    Microbiology and Molecular Genetics, Michigan State University, East Lansing, United States
    For correspondence
    grantnkr@msu.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4555-5283
  4. Sumaya T Ahmed

    Biology, Kenyon College, Gambier, United States
    Competing interests
    No competing interests declared.
  5. Tanush Jagdish

    Systems Biology; BEACON Center for the Study of Evolution in Action, Harvard Medical School, Cambridge, United States
    Competing interests
    No competing interests declared.
  6. Jessica A Baxter

    Microbiology and Molecular Genetics, Michigan State University, East Lansing, United States
    Competing interests
    No competing interests declared.
  7. Brooke A Sommerfeld

    Microbiology and Molecular Genetics, Michigan State University, East Lansing, United States
    Competing interests
    No competing interests declared.
  8. Alice Tillman

    Biology, Kenyon College, Gambier, United States
    Competing interests
    No competing interests declared.
  9. Jeremy Moore

    Biology, Kenyon College, Gambier, United States
    Competing interests
    No competing interests declared.
  10. Joan L Slonczewski

    Biology, Kenyon College, Gambier, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3484-1564
  11. Jeffrey E Barrick

    Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, United States
    Competing interests
    Jeffrey E Barrick, Jeffrey E. Barrick is the owner of Evolvomics LLC..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0888-7358
  12. Richard E Lenski

    Microbiology and Molecular Genetics; BEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, United States
    Competing interests
    No competing interests declared.

Funding

Michigan State University (Ralph Evans Award)

  • Zachary David Blount

Kenyon College (Individual Faculty Development Award)

  • Zachary David Blount

Michigan State University (Rufolph Hugh Award)

  • Nkrumah A Grant

National Science Foundation (DEB-1451740)

  • Richard E Lenski

National Science Foundation (DBI-0939454)

  • Richard E Lenski

USDA National Institute of Food and Agriculture (MICL02253)

  • Richard E Lenski

National Science Foundation (MCB-1923077)

  • Joan L Slonczewski

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

Reviewing Editor

  1. Paul B Rainey, Max Planck Institute for Evolutionary Biology, Germany

Version history

  1. Received: January 23, 2020
  2. Accepted: May 28, 2020
  3. Accepted Manuscript published: May 29, 2020 (version 1)
  4. Version of Record published: June 17, 2020 (version 2)
  5. Version of Record updated: June 23, 2020 (version 3)

Copyright

© 2020, Blount 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. Zachary David Blount
  2. Rohan Maddamsetti
  3. Nkrumah A Grant
  4. Sumaya T Ahmed
  5. Tanush Jagdish
  6. Jessica A Baxter
  7. Brooke A Sommerfeld
  8. Alice Tillman
  9. Jeremy Moore
  10. Joan L Slonczewski
  11. Jeffrey E Barrick
  12. Richard E Lenski
(2020)
Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environment
eLife 9:e55414.
https://doi.org/10.7554/eLife.55414

Share this article

https://doi.org/10.7554/eLife.55414

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