The coupling of carbon and energy fluxes reveals anaerobiosis in an aerobic soil incubation with a Bacillota-dominated community

Abstract

Soil microorganisms rely on coupled fluxes of carbon and energy to fuel their maintenance, to switch from dormancy to activity and to grow under dynamically changing conditions in microhabitats. To identify the principles underlying this coupling, we measured heat and CO2 release from soil after glucose addition along with estimates of microbial biomass and community composition. The results revealed bi-directional deviations of the ratio of heat to CO2 release (Calorespirometric Ratio, CR) that are inconsistent with theoretical predictions for aerobic respiration, which is commonly assumed to be the major metabolic pathway in incubation experiments. Moreover, the microbial community was dominated by members of the Bacillota, whose relative abundance increased from 4 percent to 65 percent in 18 h. To interpret these findings, we developed a dynamic model of carbon and energy fluxes during the microbial growth on glucose. The model simulates aerobic respiration as well as anaerobic fermentation pathways to lactate, acetate and propionate depending on the time-varying availability of O2. Simulations captured the observed temporal CR pattern and suggested a gradual depletion of O2 and a shift to anaerobic pathways as the main driver. This interpretation is consistent with the dominance of Bacillota, many members of which are well adapted to anaerobic conditions. Our results highlight the potential of the joint analysis of matter and energy fluxes in combined experimental and modeling approaches and indicate the presence of facultative anaerobiosis under common experimental conditions, which could confer a competitive advantage to certain microbial taxa during growth on labile substrate.