Biofilm microenvironment induces a widespread adaptive amino-acid fermentation pathway conferring strong fitness advantage in Escherichia coli.

Bacterial metabolism has been studied primarily in liquid cultures, and exploration of other natural growth conditions may reveal new aspects of bacterial biology. Here, we investigate metabolic changes occurring when Escherichia coli grows as surface-attached biofilms, a common but still poorly cha...

Full description

Bibliographic Details
Main Authors: Sylvie Létoffé, Sabina Chalabaev, José Dugay, Franziska Stressmann, Bianca Audrain, Jean-Charles Portais, Fabien Letisse, Jean-Marc Ghigo
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-05-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC5459495?pdf=render
id doaj-ebab11cd73914eb485f5f2e6cefdd636
record_format Article
spelling doaj-ebab11cd73914eb485f5f2e6cefdd6362020-11-25T02:23:50ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042017-05-01135e100680010.1371/journal.pgen.1006800Biofilm microenvironment induces a widespread adaptive amino-acid fermentation pathway conferring strong fitness advantage in Escherichia coli.Sylvie LétofféSabina ChalabaevJosé DugayFranziska StressmannBianca AudrainJean-Charles PortaisFabien LetisseJean-Marc GhigoBacterial metabolism has been studied primarily in liquid cultures, and exploration of other natural growth conditions may reveal new aspects of bacterial biology. Here, we investigate metabolic changes occurring when Escherichia coli grows as surface-attached biofilms, a common but still poorly characterized bacterial lifestyle. We show that E. coli adapts to hypoxic conditions prevailing within biofilms by reducing the amino acid threonine into 1-propanol, an important industrial commodity not known to be naturally produced by Enterobacteriaceae. We demonstrate that threonine degradation corresponds to a fermentation process maintaining cellular redox balance, which confers a strong fitness advantage during anaerobic and biofilm growth but not in aerobic conditions. Whereas our study identifies a fermentation pathway known in Clostridia but previously undocumented in Enterobacteriaceae, it also provides novel insight into how growth in anaerobic biofilm microenvironments can trigger adaptive metabolic pathways edging out competition with in mixed bacterial communities.http://europepmc.org/articles/PMC5459495?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Sylvie Létoffé
Sabina Chalabaev
José Dugay
Franziska Stressmann
Bianca Audrain
Jean-Charles Portais
Fabien Letisse
Jean-Marc Ghigo
spellingShingle Sylvie Létoffé
Sabina Chalabaev
José Dugay
Franziska Stressmann
Bianca Audrain
Jean-Charles Portais
Fabien Letisse
Jean-Marc Ghigo
Biofilm microenvironment induces a widespread adaptive amino-acid fermentation pathway conferring strong fitness advantage in Escherichia coli.
PLoS Genetics
author_facet Sylvie Létoffé
Sabina Chalabaev
José Dugay
Franziska Stressmann
Bianca Audrain
Jean-Charles Portais
Fabien Letisse
Jean-Marc Ghigo
author_sort Sylvie Létoffé
title Biofilm microenvironment induces a widespread adaptive amino-acid fermentation pathway conferring strong fitness advantage in Escherichia coli.
title_short Biofilm microenvironment induces a widespread adaptive amino-acid fermentation pathway conferring strong fitness advantage in Escherichia coli.
title_full Biofilm microenvironment induces a widespread adaptive amino-acid fermentation pathway conferring strong fitness advantage in Escherichia coli.
title_fullStr Biofilm microenvironment induces a widespread adaptive amino-acid fermentation pathway conferring strong fitness advantage in Escherichia coli.
title_full_unstemmed Biofilm microenvironment induces a widespread adaptive amino-acid fermentation pathway conferring strong fitness advantage in Escherichia coli.
title_sort biofilm microenvironment induces a widespread adaptive amino-acid fermentation pathway conferring strong fitness advantage in escherichia coli.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2017-05-01
description Bacterial metabolism has been studied primarily in liquid cultures, and exploration of other natural growth conditions may reveal new aspects of bacterial biology. Here, we investigate metabolic changes occurring when Escherichia coli grows as surface-attached biofilms, a common but still poorly characterized bacterial lifestyle. We show that E. coli adapts to hypoxic conditions prevailing within biofilms by reducing the amino acid threonine into 1-propanol, an important industrial commodity not known to be naturally produced by Enterobacteriaceae. We demonstrate that threonine degradation corresponds to a fermentation process maintaining cellular redox balance, which confers a strong fitness advantage during anaerobic and biofilm growth but not in aerobic conditions. Whereas our study identifies a fermentation pathway known in Clostridia but previously undocumented in Enterobacteriaceae, it also provides novel insight into how growth in anaerobic biofilm microenvironments can trigger adaptive metabolic pathways edging out competition with in mixed bacterial communities.
url http://europepmc.org/articles/PMC5459495?pdf=render
work_keys_str_mv AT sylvieletoffe biofilmmicroenvironmentinducesawidespreadadaptiveaminoacidfermentationpathwayconferringstrongfitnessadvantageinescherichiacoli
AT sabinachalabaev biofilmmicroenvironmentinducesawidespreadadaptiveaminoacidfermentationpathwayconferringstrongfitnessadvantageinescherichiacoli
AT josedugay biofilmmicroenvironmentinducesawidespreadadaptiveaminoacidfermentationpathwayconferringstrongfitnessadvantageinescherichiacoli
AT franziskastressmann biofilmmicroenvironmentinducesawidespreadadaptiveaminoacidfermentationpathwayconferringstrongfitnessadvantageinescherichiacoli
AT biancaaudrain biofilmmicroenvironmentinducesawidespreadadaptiveaminoacidfermentationpathwayconferringstrongfitnessadvantageinescherichiacoli
AT jeancharlesportais biofilmmicroenvironmentinducesawidespreadadaptiveaminoacidfermentationpathwayconferringstrongfitnessadvantageinescherichiacoli
AT fabienletisse biofilmmicroenvironmentinducesawidespreadadaptiveaminoacidfermentationpathwayconferringstrongfitnessadvantageinescherichiacoli
AT jeanmarcghigo biofilmmicroenvironmentinducesawidespreadadaptiveaminoacidfermentationpathwayconferringstrongfitnessadvantageinescherichiacoli
_version_ 1724856859655929856