Influence of Metal Cations on the Viscoelastic Properties of Escherichia coli Biofilms

Biofilms frequently cause complications in various areas of human life, e.g., in medicine and in the food industry. More recently, biofilms are discussed as new types of living materials with tunable mechanical properties. In particular, Escherichia coli produces a matrix composed of amyloid-forming curli and phosphoethanolamine-modified cellulose fibers in response to suboptimal environmental conditions. It is currently unknown how the interaction between these fibers contributes to the overall mechanical properties of the formed biofilms and if extrinsic control parameters can be utilized to manipulate these properties. Using shear rheology, we show that biofilms formed by the E. coli K-12 strain AR3110 stiffen by a factor of 2 when exposed to the trivalent metal cations Al(III) and Fe(III), while no such response is observed for the bivalent cations Zn(II) and Ca(II). Strains producing only one matrix component did not show any stiffening response to either cation or even a small softening. No stiffening response was further observed when strains producing only one type of fiber were co-cultured or simply mixed after biofilm growth. These results suggest that the E. coli biofilm matrix is a uniquely structured composite material when both matrix fibers are produced from the same bacterium. While the exact interaction mechanism between curli, phosphoethanolamine-modified cellulose, and trivalent metal cations is currently not known, our results highlight the potential of using extrinsic parameters to understand and control the interplay between biofilm structure and mechanical properties. This will ultimately aid in the development of better strategies for controlling biofilm growth.