Dynamic proteome trade-offs regulate bacterial cell size and growth in fluctuating nutrient environments

Bacteria dynamically regulate cell size and growth to thrive in changing environments. While previous studies have characterized bacterial growth physiology at steady-state, a quantitative understanding of bacterial physiology in time-varying environments is lacking. Here we develop a quantitative theory connecting bacterial growth and division rates to proteome allocation in time-varying nutrient environments. In such environments, cell size and growth are regulated by trade-offs between prioritization of biomass accumulation or division, resulting in decoupling of single-cell growth rate from population growth rate. Specifically, bacteria transiently prioritize biomass accumulation over production of division machinery during nutrient upshifts, while prioritizing division over growth during downshifts. When subjected to pulsatile nutrient concentration, we find that bacteria exhibit a transient memory of previous metabolic states due to the slow dynamics of proteome reallocation. This allows for faster adaptation to previously seen environments and results in division control which is dependent on the time-profile of fluctuations.