A distinct growth physiology enhances bacterial growth under rapid nutrient fluctuations

Abstract

It has been long known that bacteria coordinate their physiology with environmental nutrient, yet our current understanding offers little intuition for how bacteria respond to the second-to-minute scale fluctuations in nutrient concentration characteristic of many microbial habitats. To investigate the effects of rapid nutrient fluctuations on bacterial growth, we coupled custom microfluidics with single-cell microscopy to quantify the growth rate of E. coli experiencing 30 s to 60 min nutrient fluctuations. Compared to steady environments of equal average concentration, fluctuating environments reduced growth rate by up to 50%. However, measured reductions in growth rate were only 38% of the growth loss predicted from single nutrient shifts - an enhancement produced by the distinct growth response of cells grown in environments that fluctuate rather than shift once. We report an unexpected physiology adapted for growth in nutrient fluctuations and implicate nutrient timescale as a critical environmental parameter beyond nutrient concentration and source.

Environmental fluctuations and their effects on microbial communities, populations and individuals

“…low nutrient) (Nguyen et al . 2020 ). Quantifications of single-cell growth rate from each environment, which used the same high and low nutrient concentrations, revealed distinct growth rate dynamics between cells grown in fluctuating vs. steady environments.…”

“…E. coli physiologically adapted to minute-scale nutrient fluctuations exhibited a greater average growth rate than predicted based on the growth rate dynamics of steady-state-adapted cells exposed to single shifts in nutrient concentration (Nguyen et al . 2020 ). The molecular underpinnings of this physiology remain to be elucidated, though it appears that fluctuation-adapted cells suspend transitions between steady-states in favor of prioritizing higher immediate growth rates.…”

“…When nutrient fluctuated between 30 s to 60 min timescales, the average growth rate of individual E. coli cells was observed to decrease with increasing nutrient timescales (Nguyen et al . 2020 ). For nutrient fluctuations much slower than 60 min, growth rate was predicted to increase with increasing nutrient timescale.…”

“…Environmental fluctuations can determine single-cell growth rates (Nguyen et al . 2020 ), the fixation of an allele in a population (Lin and Kussell 2016 ) and a community's metabolic output (DeAngelis et al . 2010 ) based on the relative timescale between environmental fluctuations and microbial response.…”

“…At the single-cell level, growing microbes are classically understood to alter their physiology toward the physiological steady state associated with their immediate environmental conditions, yet new work demonstrates that cells instead have fluctuation-adapted physiologies distinct from those characterized in steady environments (Nguyen et al . 2020 ).…”