Phyla-wide metabolic capabilities mute positive response to direct and indirect impacts of warming throughout the soil profile

Nicholas C. Dove, Biosciences, Oak Ridge National Laboratory, Margaret Torn, Lawrence Berkeley National Laboratory, Stephen C. Hart, Sierra Nevada Research Institute, University of California, Merced, CA and Neslihan Taş, Climate & Ecosystems Division, Lawrence Berkeley National Laboratory, Berkeley, CA

Background/Question/Methods
Increasing global temperatures are predicted to stimulate soil microbial respiration. However, the direct (i.e., enzyme and growth kinetics) and indirect (i.e., nutrient-mediated) impacts of warming on soil microbes, nevertheless, remain unclear. This is particularly true for subsoil microbes, which are relatively understudied. Here, with collected soils (0 to 80 cm in depth) from an ongoing in situ deep mineral-soil warming experiment (+4 °C above ambient) after 4.5 y of warming, we use DNA sequencing, reconstruction of microbial genomes (metagenome assembled genomes [MAGs]), estimated in situ MAG growth rates, and carbon use efficiency (CUE) via metabolic flux analysis to analyze microbial community composition, metabolism, and physiology. We couple these analyses with a series of process measurements from laboratory incubations with different C and nutrient amendments to investigate relative resource limitations. We hypothesize that: 1) warming-induced soil-C depletion results in increased C limitation and decreased nutrient limitation for the microbial communities in the whole soil profile; 2) resource limitations shift microbial community composition, physiology, and metabolism towards more oligotrophic traits (e.g., higher microbial CUE, increase in genes encoding for enzyme degrading complex C compounds); and 3) these changes to the microbial community are strongest in the subsoils where resource demand is greatest.
Results/Conclusions
We show that 4.5 y of whole-profile soil warming in a temperate mixed forest results in altered microbial community composition and metabolism in surface soils, partly due to C limitation. However, microbial communities in the subsoil responded differently to warming than in the surface. Throughout the soil profile—but to a greater extent in the subsoil— physiologic and genomic measurements show that phylogenetically different microbes could utilize complex organic compounds, which, contrary to our hypothesis, dampened the effect of altered resource availability induced by warming. We find subsoil microbes had 20% lower carbon use efficiencies and 47% lower growth rates compared to surface soils, which could constrain microbial community turnover. Collectively, our results show that elevated subsoil microbial respiration may continue without microbial community turnover and adaptation in the near-term. If these conditions persist, delayed temperature acclimation at depth could boost CO2 emissions from subsoil horizons.