New insights on carbon use efficiency using calorespirometry – a bioenergetics-based model

Soil organic carbon (SOC) represents both a source of energy (catabolism) and a building material for biosynthesis (anabolism) for microorganisms. Microbial carbon use efficiency (CUE) – the ratio of C used for biosynthesis over C consumed – measures the partitioning between anabolic and catabolic processes. While most work on CUE has been based on C mass flows, the role of SOC energy content, microbial energy demand, and general energy flows on CUE have been rarely considered. Thus, a bioenergetics perspective on CUE could provide new insights on how microorganisms utilize C substrates and ultimately allow C to be stabilized in soils.

The microbial growth reactions are generally associated with a negative enthalpy change, which results in heat dissipation from the system. This heat can be measured using an isothermal calorimeter, which is often coupled with respiration measurements. This coupled system allows studying energy and C exchanges, and calculating their ratio referred to as the calorespirometric ratio (CR). Here, we formulate a coupled mass and energy balance model for microbial growth and provide a generalized relationship between CUE and CR. In the model, we consider two types of organic C in soils, the added substrate (i.e., glucose) and the native SOC. Furthermore, we assume that glucose is taken up via aerobic (AE) and two fermentation metabolic pathways – glucose to ethanol (F1) and glucose to lactic acid (F2); for simplicity, only aerobic growth on the native SOC was adopted. We use this model as a framework to generalize previous formulations and generate hypotheses on the expected variations in CR as a function of substrate type, metabolic pathways, and microbial properties (specifically CUE). In turn, the same equations can be used to estimate CUE from measured CR.

Our results show that in a non-growing system, CR depends only on the rates of different metabolic pathways (AE, F1, and F2). While in growing systems, CR is a function of rates as well as growth yields for these metabolic pathways. Under purely aerobic conditions, our model predicts that CUE increases with increasing CR when the degree of reduction of the substrate is higher than that of the microbial biomass. Similarly, CUE decreases with increasing CR when the degree of reduction of substrate is lower than that of the biomass. In the case of combined metabolism – aerobic and fermentation simultaneously – CUE is not only a function of CR and the degree of reduction of substrates but also the rates and growth yields of all metabolic pathways involved. To summarize, in this contribution we illustrate how calorespirometry can become an efficient tool to evaluate CUE and the role of different metabolic pathways in soil systems.