Mechanically-driven phase separation in a growing bacterial colony

• Published in: Proceedings of the National Academy of Sciences - PNAS 2015-04, Vol.112 (17), p.E2166-E2173
• Main Authors: Ghosh, Pushpita, Mondal, Jagannath, Ben-Jacob, Eshel, Levine, Herbert
• Format: Article
• Language: English
• Subjects: Bacteria; Bacteria - growth & development; Bacterial Physiological Phenomena; Biofilms; Biological Sciences; Cell growth; Models, Biological; Morphology; Physical Sciences; PNAS Plus; Polymers; Simulation
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1504948112

Significance Bacteria self-organize into a dense multicellular community known as a biofilm, in which cells are embedded in self-secreted extracellular polymeric substances (EPSs). A number of processes can contribute to spatial heterogeneity in a growing biofilm; among them, the effect of macromolecular crowding enhanced by the EPSs has largely remained unexplored. To understand the effect of macromolecular crowding in spontaneous spatial organization, we develop a computational model to investigate the explicit role of mechanical interactions in driving the collective behavior of bacterial cells in the presence of EPS particles in a colony growing on a solid substrate. Our findings demonstrate that an entropy-driven depletion interaction between bacteria and EPSs can induce significant phase separation and spatial heterogeneity in a biofilm. Secretion of extracellular polymeric substances (EPSs) by growing bacteria is an integral part of forming biofilm-like structures. In such dense systems, mechanical interactions among the structural components can be expected to significantly contribute to morphological properties. Here, we use a particle-based modeling approach to study the self-organization of nonmotile rod-shaped bacterial cells growing on a solid substrate in the presence of self-produced EPSs. In our simulation, all of the components interact mechanically via repulsive forces, occurring as the bacterial cells grow and divide (via consuming diffusing nutrient) and produce EPSs. Based on our simulation, we show that mechanical interactions control the collective behavior of the system. In particular, we find that the presence of nonadsorbing EPSs can lead to spontaneous aggregation of bacterial cells by a depletion attraction and thereby generates phase separated patterns in the nonequilibrium growing colony. Both repulsive interactions between cell and EPSs and the overall concentration of EPSs are important factors in the self-organization in a nonequilibrium growing colony. Furthermore, we investigate the interplay of mechanics with the nutrient diffusion and consumption by bacterial cells and observe that suppression of branch formation occurs due to EPSs compared with the case where no EPS is produced.