Osmotic spreading of <i>Bacillus subtilis</i> biofilms driven by an extracellular matrix

TLDR

Bacterial biofilms form organized communities on surfaces, secreting a polymeric matrix rich in sugars and proteins, and in Bacillus subtilis the exopolysaccharide (EPS) component is linked to inhibition of flagella‑mediated motility, yet no physical mechanism for spreading has been identified. The study proposes that EPS secretion drives surface motility by creating osmotic pressure gradients in the extracellular space and examines how this mechanism may affect nutrient uptake and the reduced fitness of matrix‑deficient mutants. A simple polymer‑solution physics model shows that EPS‑generated osmotic pressure gradients quantitatively explain biofilm growth, thickening, and spreading. The switch to EPS secretion leads to slow biofilm expansion, with flagella‑null strains spreading as fast as wild type but much faster than EPS mutants, and the model’s predictions agree with experimental measurements, highlighting the role of osmotic motility in nutrient uptake and mutant fitness.

Abstract

Bacterial biofilms are organized communities of cells living in association with surfaces. The hallmark of biofilm formation is the secretion of a polymeric matrix rich in sugars and proteins in the extracellular space. In Bacillus subtilis , secretion of the exopolysaccharide (EPS) component of the extracellular matrix is genetically coupled to the inhibition of flagella-mediated motility. The onset of this switch results in slow expansion of the biofilm on a substrate. Different strains have radically different capabilities in surface colonization: Flagella-null strains spread at the same rate as wild type, while both are dramatically faster than EPS mutants. Multiple functions have been attributed to the EPS, but none of these provides a physical mechanism for generating spreading. We propose that the secretion of EPS drives surface motility by generating osmotic pressure gradients in the extracellular space. A simple mathematical model based on the physics of polymer solutions shows quantitative agreement with experimental measurements of biofilm growth, thickening, and spreading. We discuss the implications of this osmotically driven type of surface motility for nutrient uptake that may elucidate the reduced fitness of the matrix-deficient mutant strains.