Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environment
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.
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Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environmentDryad Digital Repository, doi:10.5061/dryad.7wm37pvpp.
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Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environmentNCBI Sequence Read Archive, PRJNA553503.
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Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environmentNCBI Sequence Read Archive, PRJNA553503.
Article and author information
Author details
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
- Paul B Rainey, Max Planck Institute for Evolutionary Biology, Germany
Publication history
- Received: January 23, 2020
- Accepted: May 28, 2020
- Accepted Manuscript published: May 29, 2020 (version 1)
- Version of Record published: June 17, 2020 (version 2)
- 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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Further reading
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- Evolutionary Biology
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Gene duplication is crucial to generating novel signaling pathways during evolution. However, it remains unclear how the redundant proteins produced by gene duplication ultimately acquire new interaction specificities to establish insulated paralogous signaling pathways. Here, we used ancestral sequence reconstruction to resurrect and characterize a bacterial two-component signaling system that duplicated in α-proteobacteria. We determined the interaction specificities of the signaling proteins that existed before and immediately after this duplication event and then identified key mutations responsible for establishing specificity in the two systems. Just three mutations, in only two of the four interacting proteins, were sufficient to establish specificity of the extant systems. Some of these mutations weakened interactions between paralogous systems to limit crosstalk. However, others strengthened interactions within a system, indicating that the ancestral interaction, although functional, had the potential to be strengthened. Our work suggests that protein-protein interactions with such latent potential may be highly amenable to duplication and divergence.
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- Evolutionary Biology
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