<p>The terrestrial subsurface hosts one of Earth’s largest biomes, with groundwater systems representing major habitats for microbial life. In these environments, microbes persist under energy scarcity caused by the absence of photosynthesis, physical isolation and slow geochemical turnover, but the ecological principles underpinning their survival are poorly understood. Here we propose a framework of ‘microbial frugality’ to describe how evolutionary and physiological traits enable life to persist near the energetic minimum in groundwater. Key traits include low replication rates, genome streamlining, metabolic versatility and dependencies, and a standby metabolism that primes cells for rapid response to transient nutrient inputs. Central to this lifestyle is the necromass pump, the continual recycling of microbial biomass that creates an internally generated carbon reservoir sustaining long-term activity. Together, these traits collectively enable persistence across groundwater ecosystems and mirror principles known from the marine deep biosphere, suggesting convergent solutions to extreme oligotrophy. The efficiency, interdependence and necromass recycling associated with microbial frugality highlight the unique role of groundwater microbes in global biogeochemical cycles.</p>