Respiratory heterogeneity shapes biofilm formation and host colonization in uropathogenic Escherichia coli

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 quantified and localized the expression of two Escherichia coli cytochrome oxidases in cells found in the biofilm state and defined their contribution to biofilm architecture. These studies elucidated a role for the high-affinity quinol oxidase cytochrome bd in matrix production and biofilm resident protection. Cytochrome bd was the most abundantly expressed respiratory complex in the biofilm community and was localized in the biofilm interior. Depletion of the cytochrome bd-expressing subpopulation led to decreased extracellular matrix and increased sensitivity of the community to exogenous stresses. Interrogation of the distribution of cytochrome 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 towards a bet-hedging mechanism in which heterogeneous expression of respiratory complexes ensures respiratory plasticity of E. coli across diverse host niches.