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The Selective Advantage of the lac Operon for Escherichia coli Is Conditional on Diet and Microbiota Composition

The lac operon is one of the best known gene regulatory circuits and constitutes a landmark example of how bacteria tune their metabolism to nutritional conditions. It is nearly ubiquitous in Escherichia coli strains justifying the use of its phenotype, the ability to consume lactose, for species id...

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Autores principales: Pinto, Catarina, Melo-Miranda, Rita, Gordo, Isabel, Sousa, Ana
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8333865/
https://www.ncbi.nlm.nih.gov/pubmed/34367115
http://dx.doi.org/10.3389/fmicb.2021.709259
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author Pinto, Catarina
Melo-Miranda, Rita
Gordo, Isabel
Sousa, Ana
author_facet Pinto, Catarina
Melo-Miranda, Rita
Gordo, Isabel
Sousa, Ana
author_sort Pinto, Catarina
collection PubMed
description The lac operon is one of the best known gene regulatory circuits and constitutes a landmark example of how bacteria tune their metabolism to nutritional conditions. It is nearly ubiquitous in Escherichia coli strains justifying the use of its phenotype, the ability to consume lactose, for species identification. Lactose is the primary sugar found in milk, which is abundant in mammals during the first weeks of life. However, lactose is virtually non-existent after the weaning period, with humans being an exception as many consume dairy products throughout their lives. The absence of lactose during adulthood in most mammals and the rarity of lactose in the environment, means that the selective pressure for maintaining the lac operon could be weak for long periods of time. Despite the ability to metabolize lactose being a hallmark of E. coli’s success when colonizing its primary habitat, the mammalian intestine, the selective value of this trait remains unknown in this ecosystem during adulthood. Here we determine the competitive advantage conferred by the lac operon to a commensal strain of E. coli when colonizing the mouse gut. We find that its benefit, which can be as high as 11%, is contingent on the presence of lactose in the diet and on the presence of other microbiota members in the gut, but the operon is never deleterious. These results help explaining the pervasiveness of the lac operon in E. coli, but also its polymorphism, as lac-negative E. coli strains albeit rare can naturally occur in the gut.
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spelling pubmed-83338652021-08-05 The Selective Advantage of the lac Operon for Escherichia coli Is Conditional on Diet and Microbiota Composition Pinto, Catarina Melo-Miranda, Rita Gordo, Isabel Sousa, Ana Front Microbiol Microbiology The lac operon is one of the best known gene regulatory circuits and constitutes a landmark example of how bacteria tune their metabolism to nutritional conditions. It is nearly ubiquitous in Escherichia coli strains justifying the use of its phenotype, the ability to consume lactose, for species identification. Lactose is the primary sugar found in milk, which is abundant in mammals during the first weeks of life. However, lactose is virtually non-existent after the weaning period, with humans being an exception as many consume dairy products throughout their lives. The absence of lactose during adulthood in most mammals and the rarity of lactose in the environment, means that the selective pressure for maintaining the lac operon could be weak for long periods of time. Despite the ability to metabolize lactose being a hallmark of E. coli’s success when colonizing its primary habitat, the mammalian intestine, the selective value of this trait remains unknown in this ecosystem during adulthood. Here we determine the competitive advantage conferred by the lac operon to a commensal strain of E. coli when colonizing the mouse gut. We find that its benefit, which can be as high as 11%, is contingent on the presence of lactose in the diet and on the presence of other microbiota members in the gut, but the operon is never deleterious. These results help explaining the pervasiveness of the lac operon in E. coli, but also its polymorphism, as lac-negative E. coli strains albeit rare can naturally occur in the gut. Frontiers Media S.A. 2021-07-21 /pmc/articles/PMC8333865/ /pubmed/34367115 http://dx.doi.org/10.3389/fmicb.2021.709259 Text en Copyright © 2021 Pinto, Melo-Miranda, Gordo and Sousa. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Pinto, Catarina
Melo-Miranda, Rita
Gordo, Isabel
Sousa, Ana
The Selective Advantage of the lac Operon for Escherichia coli Is Conditional on Diet and Microbiota Composition
title The Selective Advantage of the lac Operon for Escherichia coli Is Conditional on Diet and Microbiota Composition
title_full The Selective Advantage of the lac Operon for Escherichia coli Is Conditional on Diet and Microbiota Composition
title_fullStr The Selective Advantage of the lac Operon for Escherichia coli Is Conditional on Diet and Microbiota Composition
title_full_unstemmed The Selective Advantage of the lac Operon for Escherichia coli Is Conditional on Diet and Microbiota Composition
title_short The Selective Advantage of the lac Operon for Escherichia coli Is Conditional on Diet and Microbiota Composition
title_sort selective advantage of the lac operon for escherichia coli is conditional on diet and microbiota composition
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8333865/
https://www.ncbi.nlm.nih.gov/pubmed/34367115
http://dx.doi.org/10.3389/fmicb.2021.709259
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