Physical constraints and biological regulations underlie universal osmoresponses

Abstract

Microorganisms constantly transition between environments with dramatically different external osmolarities. However, theories of microbial osmoresponses integrating physical constraints and biological regulation are lacking. Here, we propose such a theory, utilizing the separation of timescales for passive responses and biological regulations of osmolyte production and cell wall synthesis. We demonstrate that the two regulation strategies allow cells to adapt to a broad range of external osmolarity with a threshold value above which cells cannot grow, ubiquitous across bacteria and yeast. Intriguingly, the theory predicts a dramatic speedup of cell growth after an abrupt decrease in external osmolarity due to cell-wall synthesis regulation. Our theory rationalizes the unusually fast growth observed in fission yeast after an oscillatory osmotic perturbation, and the predicted growth rate peaks match quantitatively with experimental measurements. Our study reveals the physical basis of osmoresponse, yielding far-reaching implications for microbial physiology.