Respiratory Heterogeneity Shapes Biofilm Formation and Host Colonization in
Uropathogenic Escherichia coli.
Authors Beebout CJ, Eberly AR, Werby SH, Reasoner SA, Brannon JR, De S, Fitzgerald MJ,
Huggins MM, Clayton DB, Cegelski L, Hadjifrangiskou M
Submitted By Maria Hadjifrangiskou on 4/8/2019
Status Published
Journal mBio
Year 2019
Date Published
Volume : Pages 10 : Not Specified
PubMed Reference 30940709
Abstract Biofilms are multicellular bacterial communities encased in a self-secreted
extracellular matrix comprised of polysaccharides, proteinaceous fibers, and
DNA. Organization of these components lends spatial organization to the biofilm
community such that biofilm residents can benefit from the production of common
goods while being protected from exogenous insults. Spatial organization is
driven by the presence of chemical gradients, such as oxygen. Here we show that
two quinol oxidases found in Escherichia coli and other bacteria organize along
the biofilm oxygen gradient and that this spatially coordinated expression
controls architectural integrity. Cytochrome bd, a high-affinity quinol oxidase
required for aerobic respiration under hypoxic conditions, is the most
abundantly expressed respiratory complex in the biofilm community. Depletion of
the cytochrome bd-expressing subpopulation compromises biofilm complexity by
reducing the abundance of secreted extracellular matrix as well as increasing
cellular sensitivity to exogenous stresses. Interrogation of the distribution of
quinol oxidases in the planktonic state revealed that ~15% of the population
expresses cytochrome bd at atmospheric oxygen concentration, and this population
dominates during acute urinary tract infection. These data point toward a
bet-hedging mechanism in which heterogeneous expression of respiratory complexes
ensures respiratory plasticity of E. coli across diverse host niches.IMPORTANCE
Biofilms are multicellular bacterial communities encased in a self-secreted
extracellular matrix comprised of polysaccharides, proteinaceous fibers, and
DNA. Organization of these components lends spatial organization in the biofilm
community. Here we demonstrate that oxygen gradients in uropathogenic
Escherichia coli (UPEC) biofilms lead to spatially distinct expression programs
for quinol oxidases-components of the terminal electron transport chain. Our
studies reveal that the cytochrome bd-expressing subpopulation is critical for
biofilm development and matrix production. In addition, we show that quinol
oxidases are heterogeneously expressed in planktonic populations and that this
respiratory heterogeneity provides a fitness advantage during infection. These
studies define the contributions of quinol oxidases to biofilm physiology and
suggest the presence of respiratory bet-hedging behavior in UPEC.


Investigators with authorship
NameInstitution
Maria HadjifrangiskouVanderbilt University

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