Unraveling Escherichia coli’s Cloak: Identification of Phosphoethanolamine Cellulose, Its Functions, and Applications

Abstract

Bacterial biofilms are complex, multicellular communities made up of bacteria enmeshed in a self-produced extracellular matrix (ECM) that protects against environmental stress. The ECM often comprises insoluble components, which complicates the study of biofilm composition, structure, and function. Wrinkled, agar-grown Escherichia coli biofilms require 2 insoluble macromolecules: curli amyloid fibers and cellulosic polymers. We quantified these components with solid-state nuclear magnetic resonance (NMR) and determined that curli contributed 85% of the isolated uropathogenic E coli ECM dry mass. The remaining 15% was cellulosic, but, surprisingly, was not ordinary cellulose. We tracked the identity of the unanticipated peak in the 13C NMR spectrum of the cellulosic component and discovered that E coli secrete phosphoethanolamine (pEtN)-modified cellulose. Cellulose is the most abundant biopolymer on the planet, and this marked the first identification of a naturally, chemically modified cellulose. To investigate potential roles of pEtN cellulose, we customized a newly designed live-cell monolayer rheometer and demonstrated that pEtN cellulose facilitated E coli attachment to bladder epithelial cells and acted as a glue, keeping curli cell associated. The discovery of pEtN cellulose opens questions regarding its biological function(s) and provides opportunities in materials science to explore this newly discovered biopolymer.