Cellulose as an architectural element in spatially structured Escherichia coli biofilms.

TitleCellulose as an architectural element in spatially structured Escherichia coli biofilms.
Publication TypeJournal Article
Year of Publication2013
AuthorsSerra, DO, Richter, AM, Hengge, R
JournalJ Bacteriol
Volume195
Issue24
Pagination5540-54
Date Published2013 Dec
ISSN1098-5530
KeywordsBacterial Proteins, Biofilms, Cellulose, Escherichia coli K12, Microscopy, Electron, Scanning, Microscopy, Fluorescence, Point Mutation
Abstract

Morphological form in multicellular aggregates emerges from the interplay of genetic constitution and environmental signals. Bacterial macrocolony biofilms, which form intricate three-dimensional structures, such as large and often radially oriented ridges, concentric rings, and elaborate wrinkles, provide a unique opportunity to understand this interplay of "nature and nurture" in morphogenesis at the molecular level. Macrocolony morphology depends on self-produced extracellular matrix components. In Escherichia coli, these are stationary phase-induced amyloid curli fibers and cellulose. While the widely used "domesticated" E. coli K-12 laboratory strains are unable to generate cellulose, we could restore cellulose production and macrocolony morphology of E. coli K-12 strain W3110 by "repairing" a single chromosomal SNP in the bcs operon. Using scanning electron and fluorescence microscopy, cellulose filaments, sheets and nanocomposites with curli fibers were localized in situ at cellular resolution within the physiologically two-layered macrocolony biofilms of this "de-domesticated" strain. As an architectural element, cellulose confers cohesion and elasticity, i.e., tissue-like properties that-together with the cell-encasing curli fiber network and geometrical constraints in a growing colony-explain the formation of long and high ridges and elaborate wrinkles of wild-type macrocolonies. In contrast, a biofilm matrix consisting of the curli fiber network only is brittle and breaks into a pattern of concentric dome-shaped rings separated by deep crevices. These studies now set the stage for clarifying how regulatory networks and in particular c-di-GMP signaling operate in the three-dimensional space of highly structured and "tissue-like" bacterial biofilms.

DOI10.1128/JB.00946-13
Alternate JournalJ. Bacteriol.