Energy allocation theory for bacterial growth control in and out of steady state

Abstract

Efficient allocation of energy resources to key physiological functions allows living organisms to grow and thrive in diverse environments and adapt to a wide range of perturbations. To quantitatively understand how unicellular organisms utilize their energy resources in response to changes in growth environment, we introduce a theory of dynamic energy allocation which describes cellular growth dynamics based on partitioning of metabolizable energy into key physiological functions: growth, division, cell shape regulation, energy storage and loss through dissipation. By optimizing the energy flux for growth, we develop the equations governing the time evolution of cell morphology and growth rate in diverse environments. The resulting model accurately captures experimentally observed dependencies of bacterial cell size on growth rate, superlinear scaling of metabolic rate with cell size, and predicts nutrient-dependent trade-offs between energy expended for growth, division, and shape maintenance. By calibrating model parameters with available experimental data for the model organism E. coli, our model is capable of describing bacterial growth control in dynamic conditions, particularly during nutrient shifts and osmotic shocks. The model captures these perturbations with minimal added complexity and our unified approach predicts the driving factors behind a wide range of observed morphological and growth phenomena.