Bacterial adaptation to changing conditions – an eco-physiological case study with the gut bacterium Escherichia coli

To thrive, microbial organisms must successfully cope with the changing conditions they regularly encounter. The response to changing conditions typically requires the synthesis of new enzymes - for example a specific transporter to utilize a newly available nutrient source. But protein synthesis is resource demanding and novel protein synthesis by ribosomes is a fundamental constraint which limits growth even in  nutrient replete conditions. Cells must thus devise effective regulation strategies which control the synthesis of different proteins --  in relation to the environmental conditions they encounter and what physiology demands to promote survivival and growth. To better understand these regulation strategies and their eco-physiological origin, we have investigated the response of Escherichia coli to changes in available nutrient sources, connecting transient gene-expression and proteome composition to growth phenotypes. By combing experiments and theory we show how competition between genes for the limited protein synthesis capacity constrains growth during the transition. Despite this constraint, cells substantially express genes that are not required in the conditions they encountered, trapping them in states where precursor levels are low and the genes needed to replenish the precursors are outcompeted. These observations might explain why bacteria frequently show long phases of growth arrest when conditions change. Contrary to common modeling assumptions, our findings also highlight that microbial cells do not attempt to optimize growth under changing environments but rather exhibit very specific response strategies which likely evolved to promote fitness in the specific native environment cells typically encounter.