Physiological architecture and evolutionary origins of cellular adaptability

Area of Science:

• Cellular biology
• Evolutionary biology
• Systems biology

Background:

• Cellular adaptability is crucial but its mechanisms across different scales remain unclear.
• Understanding how cells adapt to complex environments requires integrating single-cell physiology, population dynamics, and evolutionary processes.

Purpose of the Study:

• To investigate the relationship between single-cell physiology, population responses, and evolutionary timescales in cellular adaptability.
• To explore how long-term selection for osmotolerance affects the hierarchy of cellular adaptation in budding yeast.

Main Methods:

• Single-cell transcriptional profiling of budding yeast across 20 complex environments.
• Long-term experimental evolution (>3,000 generations) under osmotic stress.
• Analysis of transcriptional responses, stress integration, translational coordination, and fitness.

Main Results:

• Ancestral yeast populations exhibited a reproducible hierarchy of transcriptional responses to environmental cues, originating from contingent regulation of translation initiation.
• Evolution under osmotic stress increased osmotolerance and reordered this hierarchy, deprioritizing osmotic stress as a primary adaptation axis.
• The evolved strain showed impaired stress response integration, defective translational coordination, and reduced fitness in non-selected conditions.

Conclusions:

• Cellular adaptability is not static but an evolved architecture shaped by selection history.
• Long-term adaptation can lead to trade-offs, compromising general stress response and fitness in diverse environments.
• The study reveals the mechanistic basis of adaptation hierarchies and their plasticity during evolution.