Frequency- and Amplitude-Dependent Microbial Population Dynamics during Cycles of Feast and Famine

In nature microbial populations are subject to fluctuating nutrient levels. Nutrient fluctuations are important for evolutionary and ecological dynamics in microbial communities since they impact growth rates, population sizes, and biofilm formation. Here we use automated continuous-culture devices and high-throughput imaging to show that when populations of Escherichia coli are subjected to cycles of nutrient excess (feasts) and scarcity (famine) their abundance dynamics during famines depend on the frequency and amplitude of feasts. We show that frequency and amplitude dependent dynamics in planktonic populations arise from nutrient and history dependent rates of aggregation and dispersal. A phenomenological model recapitulates our experimental observations. Our results show that the statistical properties of environmental fluctuations have substantial impacts on spatial structure in bacterial populations driving large changes in abundance dynamics.

Figure 1

E. coli abundance dynamics in fluctuating nutrient conditions. (a) Example epifluorescence image showing single cells (blue) and aggregates (red) detected by image processing. (b) Number of planktonic cells (blue points) and cell aggregates (red line) detected per image by automated measurement, with aggregate abundances smoothed by a 1 h rolling average. Dashed vertical lines indicate regions of time where a washout event occurred (1 h duration). Black lines indicate spline estimates of planktonic population abundances. (c) Instantaneous growth rate for planktonic population estimated from the spline fits shown in (b). Green dots indicate maximum growth rate during recovery.

Figure 2

Frequency and amplitude dependent abundance dynamics. (a) Maximum growth rates of planktonic populations observed during recovery from a washout event for washouts that occurred every 72 h (black), 48 h (green), and 24 h (blue) with durations varying from 1 h ($1/10$ dilution, left), 1.5 h ($1/30$ dilution, middle), and 2 h ($1/100$ dilution, right). For each condition three independent replicates are shown. Legend in left panel applies to all panels in (a). (b) Example per-image abundances of planktonic populations ($N$) and aggregates ($A$) for systems experiencing washouts every 24 h with amplitudes of 1 (left), 1.5 (middle), and 2 (right) h, respectively. Each abundance time series is smoothed with a 1 h rolling average.

Figure 3

Simulated abundance dynamics. Numerical integration of a model describing planktonic ($N$) and aggregated or adherent ($A$) population dynamics (see main text for details). Panels are identical to Fig. 2. (a) Maximum growth rate of planktonic populations computed during recovery from a washout event for washouts that occurred every 72 h (black), 48 h (green), and 24 h (blue) with durations varying from 1 h ($1/10$ dilution, left), 1.5 h ($1/30$ dilution, middle), and 2 h ($1/100$ dilution, right). (b) Simulated abundance dynamics of planktonic populations ($N$) and aggregates ($A$) for systems experiencing washouts every 24 h with amplitudes of 1 (left), 1.5 (middle), and 2 (right) h, respectively.