Tags

Type your tag names separated by a space and hit enter

Respiratory Heterogeneity Shapes Biofilm Formation and Host Colonization in Uropathogenic Escherichia coli.

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.

Links

  • PMC Free PDF
  • PMC Free Full Text
  • FREE Publisher Full Text
  • Authors+Show Affiliations

    ,

    Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee, USA.

    ,

    Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee, USA.

    ,

    Department of Chemistry, Stanford University, Stanford, California, USA.

    ,

    Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee, USA.

    ,

    Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee, USA.

    ,

    Division of Pediatric Urology, Vanderbilt University Medical Center, Nashville, Tennessee, USA.

    ,

    Vanderbilt University, Nashville, Tennessee, USA.

    ,

    Vanderbilt University, Nashville, Tennessee, USA.

    ,

    Division of Pediatric Urology, Vanderbilt University Medical Center, Nashville, Tennessee, USA.

    ,

    Department of Chemistry, Stanford University, Stanford, California, USA.

    Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee, USA maria.hadjifrangiskou@vumc.org. Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, Tennessee, USA.

    Source

    mBio 10:2 2019 04 02 pg

    MeSH

    Aerobiosis
    Anaerobiosis
    Biofilms
    Biological Variation, Population
    Genetic Heterogeneity
    Oxidation-Reduction
    Oxidoreductases
    Oxygen
    Uropathogenic Escherichia coli

    Pub Type(s)

    Journal Article
    Research Support, N.I.H., Extramural
    Research Support, Non-U.S. Gov't
    Research Support, U.S. Gov't, Non-P.H.S.

    Language

    eng

    PubMed ID

    30940709

    Citation

    Beebout, Connor J., et al. "Respiratory Heterogeneity Shapes Biofilm Formation and Host Colonization in Uropathogenic Escherichia Coli." MBio, vol. 10, no. 2, 2019.
    Beebout CJ, Eberly AR, Werby SH, et al. Respiratory Heterogeneity Shapes Biofilm Formation and Host Colonization in Uropathogenic Escherichia coli. MBio. 2019;10(2).
    Beebout, C. J., Eberly, A. R., Werby, S. H., Reasoner, S. A., Brannon, J. R., De, S., ... Hadjifrangiskou, M. (2019). Respiratory Heterogeneity Shapes Biofilm Formation and Host Colonization in Uropathogenic Escherichia coli. MBio, 10(2), doi:10.1128/mBio.02400-18.
    Beebout CJ, et al. Respiratory Heterogeneity Shapes Biofilm Formation and Host Colonization in Uropathogenic Escherichia Coli. MBio. 2019 04 2;10(2) PubMed PMID: 30940709.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Respiratory Heterogeneity Shapes Biofilm Formation and Host Colonization in Uropathogenic Escherichia coli. AU - Beebout,Connor J, AU - Eberly,Allison R, AU - Werby,Sabrina H, AU - Reasoner,Seth A, AU - Brannon,John R, AU - De,Shuvro, AU - Fitzgerald,Madison J, AU - Huggins,Marissa M, AU - Clayton,Douglass B, AU - Cegelski,Lynette, AU - Hadjifrangiskou,Maria, Y1 - 2019/04/02/ PY - 2019/4/4/entrez PY - 2019/4/4/pubmed PY - 2019/5/21/medline KW - Escherichia coli KW - biofilms KW - heterogeneity KW - oxygen gradients KW - respiration KW - urinary tract infection JF - mBio JO - MBio VL - 10 IS - 2 N2 - 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. SN - 2150-7511 UR - https://www.unboundmedicine.com/medline/citation/30940709/Respiratory_Heterogeneity_Shapes_Biofilm_Formation_and_Host_Colonization_in_Uropathogenic_Escherichia_coli L2 - http://mbio.asm.org/cgi/pmidlookup?view=long&pmid=30940709 DB - PRIME DP - Unbound Medicine ER -