Thermophilic traits correlate with slow growth in permafrost soils

Abstract Permafrost soil is characterized by prolonged freezing conditions. Thermophilic microbes have been discovered in various permanently cold environments, including permafrost, where they can persist for extended periods. The reason for this apparent mismatch between microbial adaptations and environmental conditions is unclear. Here, we test the hypothesis that thermophilic traits provide selective advantage to extremely slow-growing microbes, even in cold temperatures. We used a computational approach to predict optimal growth rates and several measures of thermophilicity in metagenome-assembled genomes (MAGs) from permafrost and active layer soils in diverse cold regions. We find that in permafrost, where available energy is always low, measures of thermophilicity correlate positively with minimum doubling time, indicating that slow growers in permafrost have more thermophilic traits. This trend is reversed in microbes in active layer soil, in which seasonal thawing, temperature changes, and episodic rain events allow periodic fast growth. Similar trends were observed in the relationship between optimal growth rates and the optimal temperature of nucleoside diphosphate kinase (NDPK), an enzyme whose temperature optimum is known to be correlated to optimal growth temperatures of the host organism. Thermophilic traits within slow growers appear to be environmentally rather than phylogenetically constrained, and thermophilic slow growers share few horizontal gene transfers with other permafrost microbes. These findings suggest that the presence of thermophilic traits in slow-growers appears to be an adaptation to extreme slow growth in a persistently low-energy environment. Importance Permanently cold environments, including permafrost soils, contain an active microbial community, which appears to include thermophilic, or heat-loving, microorganisms. This appears to be a paradox – how (and why) do microbes adapted to high temperatures live in permanently cold environments? We provide a potential answer: that the well-understood adaptations which allow microorganisms to survive high temperatures are similar to the poorly understood adaptations that allow microbes to persist over long timescales in very low-energy environments, including permafrost and the Earth’s deep subsurface. The latter environments represent 88% of the all biomass of bacteria and archaea on Earth, but the adaptations of deep subsurface microorganisms are poorly understood. This work is a step towards understanding how microorganisms persist in two different, challenging environments.