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.

Metrics

  • 7,094
    views
  • 577
    downloads
  • 19
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Evolutionary Biology
    2. Immunology and Inflammation
    Mark S Lee, Peter J Tuohy ... Michael S Kuhns
    Research Advance

    CD4+ T cell activation is driven by five-module receptor complexes. The T cell receptor (TCR) is the receptor module that binds composite surfaces of peptide antigens embedded within MHCII molecules (pMHCII). It associates with three signaling modules (CD3γε, CD3δε, and CD3ζζ) to form TCR-CD3 complexes. CD4 is the coreceptor module. It reciprocally associates with TCR-CD3-pMHCII assemblies on the outside of a CD4+ T cells and with the Src kinase, LCK, on the inside. Previously, we reported that the CD4 transmembrane GGXXG and cytoplasmic juxtamembrane (C/F)CV+C motifs found in eutherian (placental mammal) CD4 have constituent residues that evolved under purifying selection (Lee et al., 2022). Expressing mutants of these motifs together in T cell hybridomas increased CD4-LCK association but reduced CD3ζ, ZAP70, and PLCγ1 phosphorylation levels, as well as IL-2 production, in response to agonist pMHCII. Because these mutants preferentially localized CD4-LCK pairs to non-raft membrane fractions, one explanation for our results was that they impaired proximal signaling by sequestering LCK away from TCR-CD3. An alternative hypothesis is that the mutations directly impacted signaling because the motifs normally play an LCK-independent role in signaling. The goal of this study was to discriminate between these possibilities. Using T cell hybridomas, our results indicate that: intracellular CD4-LCK interactions are not necessary for pMHCII-specific signal initiation; the GGXXG and (C/F)CV+C motifs are key determinants of CD4-mediated pMHCII-specific signal amplification; the GGXXG and (C/F)CV+C motifs exert their functions independently of direct CD4-LCK association. These data provide a mechanistic explanation for why residues within these motifs are under purifying selection in jawed vertebrates. The results are also important to consider for biomimetic engineering of synthetic receptors.

    1. Evolutionary Biology
    Robert Horvath, Nikolaos Minadakis ... Anne C Roulin
    Research Article

    Understanding how plants adapt to changing environments and the potential contribution of transposable elements (TEs) to this process is a key question in evolutionary genomics. While TEs have recently been put forward as active players in the context of adaptation, few studies have thoroughly investigated their precise role in plant evolution. Here, we used the wild Mediterranean grass Brachypodium distachyon as a model species to identify and quantify the forces acting on TEs during the adaptation of this species to various conditions, across its entire geographic range. Using sequencing data from more than 320 natural B. distachyon accessions and a suite of population genomics approaches, we reveal that putatively adaptive TE polymorphisms are rare in wild B. distachyon populations. After accounting for changes in past TE activity, we show that only a small proportion of TE polymorphisms evolved neutrally (<10%), while the vast majority of them are under moderate purifying selection regardless of their distance to genes. TE polymorphisms should not be ignored when conducting evolutionary studies, as they can be linked to adaptation. However, our study clearly shows that while they have a large potential to cause phenotypic variation in B. distachyon, they are not favored during evolution and adaptation over other types of mutations (such as point mutations) in this species.