Trade-offs, trade-ups, and high mutational parallelism underlie microbial adaptation during extreme cycles of feast and famine

• Published in: Current biology Vol. 34; no. 7; pp. 1403 - 1413.e5
• Main Authors: Behringer, Megan G., Ho, Wei-Chin, Miller, Samuel F., Worthan, Sarah B., Cen, Zeer, Stikeleather, Ryan, Lynch, Michael
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 08.04.2024
• Subjects: adaptation; Adaptation, Physiological - genetics; biofilm; Escherichia coli; evolution; experimental evolution; famine; fluctuating environment; global regulator; motility; Mutation; mutational order; osmolarity; species; starvation; toxins; wastes; starvation; mutational order; global regulator; experimental evolution; Escherichia coli; fluctuating environment; biofilm; adaptation; motility
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2024.02.040

Microbes are evolutionarily robust organisms capable of rapid adaptation to complex stress, which enables them to colonize harsh environments. In nature, microbes are regularly challenged by starvation, which is a particularly complex stress because resource limitation often co-occurs with changes in pH, osmolarity, and toxin accumulation created by metabolic waste. Often overlooked are the additional complications introduced by eventual resource replenishment, as successful microbes must withstand rapid environmental shifts before swiftly capitalizing on replenished resources to avoid invasion by competing species. To understand how microbes navigate trade-offs between growth and survival, ultimately adapting to thrive in environments with extreme fluctuations, we experimentally evolved 16 Escherichia coli populations for 900 days in repeated feast/famine conditions with cycles of 100-day starvation before resource replenishment. Using longitudinal population-genomic analysis, we found that evolution in response to extreme feast/famine is characterized by narrow adaptive trajectories with high mutational parallelism and notable mutational order. Genetic reconstructions reveal that early mutations result in trade-offs for biofilm and motility but trade-ups for growth and survival, as these mutations conferred positively correlated advantages during both short-term and long-term culture. Our results demonstrate how microbes can navigate the adaptive landscapes of regularly fluctuating conditions and ultimately follow mutational trajectories that confer benefits across diverse environments. •Evolutionary outcomes differ based on duration and amplitude of feast and famine•Extreme feast/famine cycles confine adaptation and results in mutational order•Mutations in transcription regulators break trade-offs between growth and survival Cells frequently navigate both the rigors of starvation and resource variability. By experimentally evolving Escherichia coli populations in repeated extreme feast/famine cycles, Behringer and Ho et al. identify adaptive mutations breaking the evolutionary tension between survival and fast growth, a widely acknowledged paradigm in the literature.