Vanhille Campos, Christian; (2025) Modelling out-of-equilibrium molecular self-organisation in the cell. Doctoral thesis (Ph.D), UCL (University College London).

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Abstract

Cells, which constitute the fundamental units of life, rely on complex physical and chemical processes to maintain their structure, organisation, and function. Central to these processes is the ability of biomolecules to self-organise into large-scale functional structures with particular physical properties that are fundamental to their role in cellular activity, such as cytoskeletal filaments and lipid membranes. Notably, these self-organisation phenomena are often driven out of equilibrium, continuously dissipating energy to perform functional work in the cell. However, due to the complexity of bridging the molecular and cellular scales, understanding the mechanisms underlying this dynamic and functional self-organisation remains a significant challenge. This thesis aims to provide new insights into out-of-equilibrium molecular self-organisation in the cell by introducing minimal coarse-grained models that capture the essential physical and chemical properties of the system. We focus on two fundamental biological processes: the response of lipid vesicles to damage and changes in their environment, and the treadmilling dynamics of cytoskeletal filaments, particularly the bacterial division protein FtsZ. These models provide unique insights into the physical mechanisms underlying the function and behaviour of these biological systems. In the case of lipid vesicles, we reveal the physical mechanisms by which they dynamically adapt to osmotic gradients and pore damage, which has implications for understanding proto-cell development and organelle function. For cytoskeletal filaments, we uncover a novel mechanism by which FtsZ treadmilling naturally leads to collective order, critical for bacterial division. Additionally, we delineate general design principles underlying treadmilling monomers that can be exploited experimentally to develop a new class of synthetic machinery. Overall, this work advances our understanding of functional molecular self-organisation in the cell, providing fundamental insights into the physical mechanisms underlying a myriad of essential biological processes.

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