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

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 me...

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Main Authors: Zachary D Blount, Rohan Maddamsetti, Nkrumah A Grant, Sumaya T Ahmed, Tanush Jagdish, Jessica A Baxter, Brooke A Sommerfeld, Alice Tillman, Jeremy Moore, Joan L Slonczewski, Jeffrey E Barrick, Richard E Lenski
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/55414
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spelling doaj-c5355242932347aa9132cbee0e7a1b652021-05-05T21:09:19ZengeLife Sciences Publications LtdeLife2050-084X2020-05-01910.7554/eLife.55414Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environmentZachary D Blount0https://orcid.org/0000-0001-5153-0034Rohan Maddamsetti1https://orcid.org/0000-0003-3370-092XNkrumah A Grant2https://orcid.org/0000-0002-4555-5283Sumaya T Ahmed3Tanush Jagdish4Jessica A Baxter5Brooke A Sommerfeld6Alice Tillman7Jeremy Moore8Joan L Slonczewski9https://orcid.org/0000-0003-3484-1564Jeffrey E Barrick10https://orcid.org/0000-0003-0888-7358Richard E Lenski11https://orcid.org/0000-0002-1064-8375Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, United States; The BEACON Center for the Study of Evolution in Action, East Lansing, United StatesDepartment of Biomedical Engineering, Duke University, Durham, United StatesDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, United States; The BEACON Center for the Study of Evolution in Action, East Lansing, United StatesDepartment of Biology, Kenyon College, Gambier, United StatesThe BEACON Center for the Study of Evolution in Action, East Lansing, United States; Program for Systems, Synthetic, and Quantitative Biology, Harvard University, Cambridge, United StatesDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, United StatesDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, United StatesDepartment of Biology, Kenyon College, Gambier, United StatesDepartment of Biology, Kenyon College, Gambier, United StatesDepartment of Biology, Kenyon College, Gambier, United StatesThe BEACON Center for the Study of Evolution in Action, East Lansing, United States; Department of Molecular Biosciences, The University of Texas, Austin, United StatesDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, United States; The BEACON Center for the Study of Evolution in Action, East Lansing, United StatesEvolutionary 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 niche, we founded two sets of Cit+ populations and evolved them for 2500 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 trait refinement and adaptation to the new citrate niche, while also suggesting a recalcitrant mismatch between E. coli physiology and growth on citrate.https://elifesciences.org/articles/55414adaptationexperimental evolutiongenomicsgene amplificationevolutionary innovationniche invasion
collection DOAJ
language English
format Article
sources DOAJ
author Zachary D Blount
Rohan Maddamsetti
Nkrumah A Grant
Sumaya T Ahmed
Tanush Jagdish
Jessica A Baxter
Brooke A Sommerfeld
Alice Tillman
Jeremy Moore
Joan L Slonczewski
Jeffrey E Barrick
Richard E Lenski
spellingShingle Zachary D Blount
Rohan Maddamsetti
Nkrumah A Grant
Sumaya T Ahmed
Tanush Jagdish
Jessica A Baxter
Brooke A Sommerfeld
Alice Tillman
Jeremy Moore
Joan L Slonczewski
Jeffrey E Barrick
Richard E Lenski
Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environment
eLife
adaptation
experimental evolution
genomics
gene amplification
evolutionary innovation
niche invasion
author_facet Zachary D Blount
Rohan Maddamsetti
Nkrumah A Grant
Sumaya T Ahmed
Tanush Jagdish
Jessica A Baxter
Brooke A Sommerfeld
Alice Tillman
Jeremy Moore
Joan L Slonczewski
Jeffrey E Barrick
Richard E Lenski
author_sort Zachary D Blount
title Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environment
title_short Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environment
title_full Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environment
title_fullStr Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environment
title_full_unstemmed Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environment
title_sort genomic and phenotypic evolution of escherichia coli in a novel citrate-only resource environment
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-05-01
description 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 niche, we founded two sets of Cit+ populations and evolved them for 2500 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 trait refinement and adaptation to the new citrate niche, while also suggesting a recalcitrant mismatch between E. coli physiology and growth on citrate.
topic adaptation
experimental evolution
genomics
gene amplification
evolutionary innovation
niche invasion
url https://elifesciences.org/articles/55414
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