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Dynamics and genetic diversification of Escherichia coli during experimental adaptation to an anaerobic environment

BACKGROUND: Many bacteria are facultative anaerobes, and can proliferate in both anoxic and oxic environments. Under anaerobic conditions, fermentation is the primary means of energy generation in contrast to respiration. Furthermore, the rates and spectra of spontaneous mutations that arise during...

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Autores principales: Finn, Thomas J., Shewaramani, Sonal, Leahy, Sinead C., Janssen, Peter H., Moon, Christina D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5419217/
https://www.ncbi.nlm.nih.gov/pubmed/28480139
http://dx.doi.org/10.7717/peerj.3244
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author Finn, Thomas J.
Shewaramani, Sonal
Leahy, Sinead C.
Janssen, Peter H.
Moon, Christina D.
author_facet Finn, Thomas J.
Shewaramani, Sonal
Leahy, Sinead C.
Janssen, Peter H.
Moon, Christina D.
author_sort Finn, Thomas J.
collection PubMed
description BACKGROUND: Many bacteria are facultative anaerobes, and can proliferate in both anoxic and oxic environments. Under anaerobic conditions, fermentation is the primary means of energy generation in contrast to respiration. Furthermore, the rates and spectra of spontaneous mutations that arise during anaerobic growth differ to those under aerobic growth. A long-term selection experiment was undertaken to investigate the genetic changes that underpin how the facultative anaerobe, Escherichia coli, adapts to anaerobic environments. METHODS: Twenty-one populations of E. coli REL4536, an aerobically evolved 10,000th generation descendent of the E. coli B strain, REL606, were established from a clonal ancestral culture. These were serially sub-cultured for 2,000 generations in a defined minimal glucose medium in strict aerobic and strict anaerobic environments, as well as in a treatment that fluctuated between the two environments. The competitive fitness of the evolving lineages was assessed at approximately 0, 1,000 and 2,000 generations, in both the environment of selection and the alternative environment. Whole genome re-sequencing was performed on random colonies from all lineages after 2,000-generations. Mutations were identified relative to the ancestral genome, and based on the extent of parallelism, traits that were likely to have contributed towards adaptation were inferred. RESULTS: There were increases in fitness relative to the ancestor among anaerobically evolved lineages when tested in the anaerobic environment, but no increases were found in the aerobic environment. For lineages that had evolved under the fluctuating regime, relative fitness increased significantly in the anaerobic environment, but did not increase in the aerobic environment. The aerobically-evolved lineages did not increase in fitness when tested in either the aerobic or anaerobic environments. The strictly anaerobic lineages adapted more rapidly to the anaerobic environment than did the fluctuating lineages. Two main strategies appeared to predominate during adaptation to the anaerobic environment: modification of energy generation pathways, and inactivation of non-essential functions. Fermentation pathways appeared to alter through selection for mutations in genes such as nadR, adhE, dcuS/R, and pflB. Mutations were frequently identified in genes for presumably dispensable functions such as toxin-antitoxin systems, prophages, virulence and amino acid transport. Adaptation of the fluctuating lineages to the anaerobic environments involved mutations affecting traits similar to those observed in the anaerobically evolved lineages. DISCUSSION: There appeared to be strong selective pressure for activities that conferred cell yield advantages during anaerobic growth, which include restoring activities that had previously been inactivated under long-term continuous aerobic evolution of the ancestor.
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spelling pubmed-54192172017-05-05 Dynamics and genetic diversification of Escherichia coli during experimental adaptation to an anaerobic environment Finn, Thomas J. Shewaramani, Sonal Leahy, Sinead C. Janssen, Peter H. Moon, Christina D. PeerJ Evolutionary Studies BACKGROUND: Many bacteria are facultative anaerobes, and can proliferate in both anoxic and oxic environments. Under anaerobic conditions, fermentation is the primary means of energy generation in contrast to respiration. Furthermore, the rates and spectra of spontaneous mutations that arise during anaerobic growth differ to those under aerobic growth. A long-term selection experiment was undertaken to investigate the genetic changes that underpin how the facultative anaerobe, Escherichia coli, adapts to anaerobic environments. METHODS: Twenty-one populations of E. coli REL4536, an aerobically evolved 10,000th generation descendent of the E. coli B strain, REL606, were established from a clonal ancestral culture. These were serially sub-cultured for 2,000 generations in a defined minimal glucose medium in strict aerobic and strict anaerobic environments, as well as in a treatment that fluctuated between the two environments. The competitive fitness of the evolving lineages was assessed at approximately 0, 1,000 and 2,000 generations, in both the environment of selection and the alternative environment. Whole genome re-sequencing was performed on random colonies from all lineages after 2,000-generations. Mutations were identified relative to the ancestral genome, and based on the extent of parallelism, traits that were likely to have contributed towards adaptation were inferred. RESULTS: There were increases in fitness relative to the ancestor among anaerobically evolved lineages when tested in the anaerobic environment, but no increases were found in the aerobic environment. For lineages that had evolved under the fluctuating regime, relative fitness increased significantly in the anaerobic environment, but did not increase in the aerobic environment. The aerobically-evolved lineages did not increase in fitness when tested in either the aerobic or anaerobic environments. The strictly anaerobic lineages adapted more rapidly to the anaerobic environment than did the fluctuating lineages. Two main strategies appeared to predominate during adaptation to the anaerobic environment: modification of energy generation pathways, and inactivation of non-essential functions. Fermentation pathways appeared to alter through selection for mutations in genes such as nadR, adhE, dcuS/R, and pflB. Mutations were frequently identified in genes for presumably dispensable functions such as toxin-antitoxin systems, prophages, virulence and amino acid transport. Adaptation of the fluctuating lineages to the anaerobic environments involved mutations affecting traits similar to those observed in the anaerobically evolved lineages. DISCUSSION: There appeared to be strong selective pressure for activities that conferred cell yield advantages during anaerobic growth, which include restoring activities that had previously been inactivated under long-term continuous aerobic evolution of the ancestor. PeerJ Inc. 2017-05-03 /pmc/articles/PMC5419217/ /pubmed/28480139 http://dx.doi.org/10.7717/peerj.3244 Text en ©2017 Finn et al. http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Evolutionary Studies
Finn, Thomas J.
Shewaramani, Sonal
Leahy, Sinead C.
Janssen, Peter H.
Moon, Christina D.
Dynamics and genetic diversification of Escherichia coli during experimental adaptation to an anaerobic environment
title Dynamics and genetic diversification of Escherichia coli during experimental adaptation to an anaerobic environment
title_full Dynamics and genetic diversification of Escherichia coli during experimental adaptation to an anaerobic environment
title_fullStr Dynamics and genetic diversification of Escherichia coli during experimental adaptation to an anaerobic environment
title_full_unstemmed Dynamics and genetic diversification of Escherichia coli during experimental adaptation to an anaerobic environment
title_short Dynamics and genetic diversification of Escherichia coli during experimental adaptation to an anaerobic environment
title_sort dynamics and genetic diversification of escherichia coli during experimental adaptation to an anaerobic environment
topic Evolutionary Studies
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5419217/
https://www.ncbi.nlm.nih.gov/pubmed/28480139
http://dx.doi.org/10.7717/peerj.3244
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