Effect of drought on soil microbial metabolisms driving carbon allocation and volatile organic compound cycling in the tropical rainforest at Biosphere 2

Droughts are occurring with increased frequency and duration in tropical rainforests due to climate change, having a significant impact on soil C dynamics. The role of microbes as drivers of changing C flow, particularly in relation to volatile organic compound (VOC) cycling, remains largely unknown. Here, we aimed to characterize microbial responses to drought using an integrative, multiple ‘omics approach, and hypothesized that microbial communities will adapt by altering their C allocation strategies. Specifically, during pre-drought, primary metabolic pathways will be more active with microbes using C towards growth, whereas during drought, microbes will divert C to secondary metabolite (including VOC) production in response to stress. To test this, we conducted an ecosystem-wide 66-day drought experiment in the tropical rainforest biome at Biosphere 2, a glass- and steel-enclosed facility near Tucson, AZ. To track carbon allocation by microbes, we injected C1 or C2 position-specific 13C-pyruvate solution into a 25 cm2 region within a soil flux chamber collar (n=6 locations) and measured C isotope ratios of VOC and CO2 emissions. Soil was collected at 0, 6, and 48 hours after pyruvate addition to examine responses in soil metatranscriptomics, metagenomics, and metabolomics (1H nuclear magnetic resonance [NMR] and Fourier-transform ion cyclotron resonance [FTICR]). Our results indicated that 13CO2 (primarily emitted from C1-13C-pyruvate) fluxes decreased during drought, indicating diminished microbial activity. 13C-VOCs (primarily emitted from C2-13C-pyruvate) fluxes also differed between pre-drought and drought. Furthermore, drought-induced increases in activity of VOC-producing metabolic pathways, including acetate and acetone biosynthesis, were evident, as inferred from volatilome, metabolome, and metatranscriptome data. Overall, these results indicate that integration of multiple ‘omics datasets reveal specific impacts of drought on microbial activity affecting carbon flow in the tropical rainforest soil.