Emergence of active nematics in chaining bacterial biofilms

Abstract

Growing tissue and bacterial colonies are active matter systems where cell divisions and cellular motion generate active stress. Although they operate in the non-equilibrium regime, these biological systems can form large-scale ordered structures. How mechanical instabilities drive the dynamics of active matter systems and form ordered structures are not well understood. Here, we use chaining Bacillus subtilis , also known as a biofilm, to study the relation between mechanical instabilities and nematic ordering. We find that bacterial biofilms have intrinsic length scales above which a series of mechanical instabilities occur. Localized stress and friction drive buckling and edge instabilities which further create nematically aligned structures and topological defects. We also observe that topological defects control stress distribution and initiate the formation of sporulation sites by creating three-dimensional structures. In this study we propose an alternative active matter platform to study the essential roles of mechanics in growing biological tissue.

Pattern formation and polarity sorting of driven actin filaments on lipid membranes

“…Additionally, topological defects, already well studied in the context of active nematics ( 24 , 51 , 62 – 66 ), play a role not only in the accumulation of particles ( 52 , 67 ) but also in shaping the dynamics. We find indeed that +1/2 topological defects act as “nematic wedges,” a particularly effective polarity-sorting mechanism.…”

Binding self-propelled topological defects in active turbulence

“…Intriguingly, the functional role of topological defects has also been recently identified in a growing number of biological processes. Striking examples are cytoskeletal topological defects determining growth axis of animal Hydra [11,12], defects in cell orientation governing cell death and extrusion in epithelial tissues [13], defects in bacterial biofilms leading to layer formation [14], and defects as local hot spots of mound formation in neural stem cells [15].…”

Microbial Active Matter: A Topological Framework

“…The constellation of topological defects and their dynamics within colonies of different bacterial morphologies have been described as two and three dimensional active nematic systems [51,[53][54][55]. Theoretically, the shape of growing bacterial colonies was explained using continuum approach wherein cells were treated as active gel growing in an isotropic liquid [53].…”

“…Growth of bacterial monolayers under soft agarose surfaces demonstrated that topological defects were created at a constant rate, with the motility of +1/2 defects biased toward the colony periphery [54]. More recently, studies on bacterial monolayers were extended to analyze multilayer morphologies, capturing the early developmental stages of bacterial biofilms [51,55,56]. Analytical modeling and numerical simulations have revealed that the transition from mono to multilayered morphology (in bacterial colonies of rod-shaped cells) is triggered by a competition between the growth-induced in-plane active stresses and vertical restoring forces due to the cell-substrate interactions [51].…”

“…In the limit of high cell numbers, the occurrence of the first division in the colony can be approximated as a Poisson process, the rate of which gives the order parameter of the transition, revealing the mixed deterministic-stochastic nature of the process. For bacterial colonies of chain-shaped cells, the multilayered structure emerged due to an interplay of mechanical stress accumulation and friction, resulting in buckling and edge instabilities [55]. The buckling sites were characterized by nucleation of topological defects that initiated the formation of three-dimensional sporulation points.…”