Corner Flows Induced by Surfactant-Producing Bacteria Bacillus subtilis and Pseudomonas fluorescens

Abstract

The spread of bacteria in soil is critical in soil biogeochemical cycles, soil and groundwater contamination, and the efficiency of soil-based bioremediation projects. However, the mechanistic understanding of bacterial spreading in soil remains incomplete due to a lack of direct observations. A mechanistic understanding of bacterial spreading in soil, which has both air and water in angular pore spaces, is critical to control pathogenic contamination of soil and to design bioremediation projects. A recent study (J. Q. Yang, J. E. Sanfilippo, N. Abbasi, Z. Gitai, et al., Proc Natl Acad Sci U S A 118:e2111060118, 2021, https://doi.org/10.1073/pnas.2111060118 ) shows that Pseudomonas aeruginosa can self-generate flows along sharp corners by producing rhamnolipids, a type of biosurfactants that change the hydrophobicity of solid surfaces. We hypothesize that other types of biosurfactants and biosurfactant-producing bacteria can also generate corner flows. Here, we first demonstrate that rhamnolipids and surfactin, biosurfactants with different chemical structures, can generate corner flows. We identify the critical concentrations of these two biosurfactants to generate corner flow. Second, we demonstrate that two common soil bacteria, Pseudomonas fluorescens and Bacillus subtilis (which produce rhamnolipids and surfactin, respectively), can generate corner flows along sharp corners at the speed of several millimeters per hour. We further show that a surfactin-deficient mutant of B. subtilis cannot generate corner flow. Third, we show that, similar to the finding for P. aeruginosa , the critical corner angle for P. fluorescens and B. subtilis to generate corner flows can be predicted from classic corner flow theories. Finally, we show that the height of corner flows is limited by the roundness of corners. Our results suggest that biosurfactant-induced corner flows are prevalent in soil and should be considered in the modeling and prediction of bacterial spreading in soil. The critical biosurfactant concentrations we identify and the mathematical models we propose will provide a theoretical foundation for future predictions of bacterial spreading in soil. IMPORTANCE The spread of bacteria in soil is critical in soil biogeochemical cycles, soil and groundwater contamination, and the efficiency of soil-based bioremediation projects. However, the mechanistic understanding of bacterial spreading in soil remains incomplete due to a lack of direct observations. Here, we simulate confined spaces of hydrocarbon-covered soil using a transparent material with similar hydrophobicity and visualize the spread of two common soil bacteria, Pseudomonas fluorescens and Bacillus subtilis . We show that both bacteria can generate corner flows at the velocity of several millimeters per hour by producing biosurfactants, soap-like chemicals. We provide quantitative equations to predict the critical corner angle for bacterial corner flow and the maximum distance of the corner spreading. We anticipate that bacterial corner flow is prevalent because biosurfactant-producing bacteria and angular pores are common in soil. Our results will help improve predictions of bacterial spreading in soil and facilitate the design of soil-related bioremediation projects.