Microbial metagenomic responses to long-term warming vary in different soil aggregates

Abstract:

Physical protection of soil organic matter mediates soil carbon loss to the atmosphere over climate warming, a process driven by microbial activity. Nearly three decades of soil warming in a temperate forest has reduced soil C and microbial biomass, more so in macroaggregates (250-2000 µm) than in microaggregates (<250 µm) due to less physical protection. However, the responses of microbial strategies to long-term warming in different aggregates are still unclear. We hypothesized that long-term warming increases genes associated with microbial maintenance and stress tolerance, and the warming effect is stronger in macroaggregates than in microaggregates owing to greater substrate limitation. Mineral soils were sampled from the control and heated plots at Harvard Forest (MA, USA), isolated into macroaggregates and microaggregates, and metagenome DNA was sequenced by the Joint Genome Institute (JGI). We found that warming increased the relative abundance of genes associated with maintenance (i.e., carbohydrate transport) and stress tolerance (i.e., cell motility, defense mechanisms, signal transduction) in microaggregates but not in macroaggregates, suggesting that microbes likely reduced resource investment to growth after long-term warming. Genes associated with maintenance and stress tolerance were more abundant in macroaggregates than in microaggregates, possibly associated with greater substrate limitation. Long-term warming altered microbial metagenomic composition in across aggregates. Metagenomic composition was different between macroaggregates and microaggregates, but this difference was smaller in the heated than control soils, suggesting chronic warming selected microbes with more similar traits among aggregates. Our findings suggest that after long-term warming, microbial communities increase their resource investment in maintenance and stress tolerance more in soil compartments that have stronger physical protection.