Mechanoperception and morphogenesis of living architectures

Abstract

In this thesis, we elucidate how living systems form and maintain their architectures by studying two systems that exemplify, respectively, the statical and dynamical properties of cellular assemblies. We first introduce the concept of living architectures as a unit of organization that generalizes the notion of biological tissue (Chapter 1). We begin our study of living architectures by considering how cells in connective tissue can sense the mechanical properties of biopolymer networks, which serve as scaffolds upon which cells live inside and move through (Chapters 2 and 3). In Chapter 2, we investigate the linear response of these biopolymer scaffolds and show how their intrinsic structural disorder gives rise to extreme mechanical heterogeneity that limits mechanosensing. In Chapter 3, we generalize our results to the nonlinear response regime and uncover a mechanical focusing effect, in which mechanical heterogeneity decreases as the applied force is increased. We explain how geometrical nonlinearities produce mechanical focusing by developing a novel Disordered Effective Medium approach. Then, in Chapter 4, we turn to bacterial biofilms to explore the biophysical principles underlying the self-assembly of living architectures. We show how the presence of cell-to-surface adhesion allows biofilms to grow from a two-dimensional layer of founder cells into a three-dimensional structure with a vertically-aligned core. The interplay between cell growth and cell verticalization gives rise to an exotic mechanical state in which the effective surface pressure becomes constant throughout the growing core of the biofilm surface layer. This dynamical isobaricity determines the expansion speed of a biofilm cluster and thereby governs how cells access the third dimension. We conclude by discussing general biophysical principles of living architectures that emerge from our case studies (Chapter 5).