E. colipopulations in unpredictably fluctuating environments evolve to face novel stresses through enhanced efflux activity

Abstract

There is considerable understanding about how laboratory populations respond to predictable (constant or deteriorating-environment) selection for single environmental variables like temperature or pH. However, such insights may not apply when selection environments comprise multiple variables that fluctuate unpredictably, as is common in nature. To address this issue, we grew replicate laboratory populations of E. coli in nutrient broth whose pH and concentrations of salt (NaCl) and hydrogen peroxide (H 2 O 2 ) were randomly changed daily. After ~170 generations, the fitness of the selected populations had not increased in any of the three selection environments. However, these selected populations had significantly greater fitness in four novel environments which have no known fitness-correlation with tolerance to pH, NaCl or H 2 O 2 . Interestingly, contrary to expectations, hypermutators did not evolve. Instead, the selected populations evolved an increased ability for energy dependent efflux activity that might enable them to throw out toxins, including antibiotics, from the cell at a faster rate. This provides an alternate mechanism for how evolvability can evolve in bacteria and potentially lead to broadspectrum antibiotic resistance, even in the absence of prior antibiotic exposure. Given that environmental variability is increasing in nature, this might have serious consequences for public-health.

Environmental stability affects phenotypic evolution in a globally distributed marine picoplankton

“…It has not been tested empirically whether fluctuations modulate responses to further environmental changes in marine phytoplankton, although theory and experiments on other model organisms such as Escherichia coli suggests that it should (Ghalambor et al, 2007;Draghi and Whitlock, 2012;Chevin et al, 2013;Karve et al, 2014). This is particularly important, as even under optimistic scenarios, CO 2 levels in the ocean are going to increase long after the 2100 cutoff applied to most climate models (IPCC report, 2007).…”

Extent of adaptation is not limited by unpredictability of the environment in laboratory populations ofEscherichia coli

“…Experiments show that this is indeed the case when environment fluctuates unpredictably over short duration of selection [12]. However, when faced with unpredictable environments over longer duration, the overall mean fitness actually improves [13].…”

“…In other words, when an organism adapts to a temperature of say 40 ºC, then it is likely to do well under 39 ºC or 38ºC. However, when the environment fluctuates across qualitatively different parameters (say salt and pH [12,13], then the both the nature and the strength of selection can vary. This change is likely to affect the adaptation of organisms.…”

An interplay of population size and environmental heterogeneity explains why fitness costs are rare

“…We conducted growth measurements to obtain high-resolution growth curves for all the 60 independently evolving populations in all four distinct sole carbon sources (T, G, M, and S) at the end of the evolution experiment. We used the maximum growth rate (R) as the measure of fitness (Leiby & Marx 2014;Karve et al 2015;Chavhan et al 2019a, b) (see Methods for details). We identified the occurrence of significant costs of adaptation in our experimental populations as cases that showed adaptation to one environment and simultaneous maladaptation to another.…”

“…We used the maximum growth rate (R) as the measure of fitness. We computed R as the maximum slope of the growth curve over a dynamic window of ten OD (600 nm) readings (Leiby & Marx 2014;Karve et al 2015;Chavhan et al 2019a, b). As described in the Results section, for each of the four sole carbon sources (G, M, S, and T), we used single sample t-tests to compare the fitness of each of the ten evolutionary regimens to that of the ancestor.…”