Environmental history can counteract nutrient quality in shaping the evolution of bacterial growth rates

Despite sharing nearly identical enzymes, strains of the same microbial species display wide variability of growth rates when growing on the same nutrients. Here, we show that such growth rate variability can emerge as a consequence of evolutionary adaptation to different patterns of environmental fluctuations. We develop a mathematical model combining cellular proteome allocation with eco-evolutionary dynamics in fluctuating environments. We find that different patterns of environmental fluctuations select for distinct growth profiles. Slow-growing strains repeatedly outcompete fast-growers when evolved in rapidly changing environments. In a range of environments with asymmetric nutrient availability, evolution reproducibly leads to the robust diversification of two coexisting strains. We develop a theoretical framework based on adaptive dynamics which quantitatively predicts these evolutionary outcomes and explains them in terms of the growth-lag tradeoff that all cells face. Finally, we show that the model can reproduce several patterns in growth-rate data from closely-related strains. Our results highlight that bacterial growth rates can rapidly adapt to their recent environmental history by proteome allocation alone, in ways that often oppose expectations based on nutrient quality.