The thermodynamic efficiency of soil microbial communities subject to long-term stress is lower than those under conventional input regimes

Isothermal microcalorimetry measures the thermal flows occurring in systems with very high precision and may be used to quantify carbon (C) assimilation and resource-use efficiencies in soils. We determined the thermodynamic efficiency of soil microbial communities located in soils which had received contrasting long-term management regimes (53 y) with respect to organic matter and nitrogen (N) inputs, viz. farmyard manure, sewage sludge, straw and calcium nitrate, calcium nitrate only, or ammonium sulphate. Two thermodynamic efficiency indices were considered: (i) total thermodynamic efficiency of soil microbial communities (ηeff), i.e. general heat production released following substrate addition, per unit heat energy input to the soil system, and (ii) a specific thermodynamic efficiency index of energy retained in the soil system (ηsoil). The latter index provides quantitative data on how much C is assimilated and energy retained in the soil system. Further, we derived a ‘substrate-induced heat production’ (SIHP) index, which adjusts for size of the microbial biomass. Optimised concentrations of water or glucose plus water were added to the soil samples and resultant thermal signatures and C mineralisation were determined over a 48-h incubation period at 25 °C. The thermal signatures were further related to the microbial community profiles of the soils. The phenotypic structural and functional diversity profiles of the microbial communities in soils were assessed by phospholipid fatty acid and multi-substrate induced respiration methods at the start of the experiment, confirming significant differences between all five treatments in community composition and functional capabilities. Both the total and specific thermodynamic efficiency indices of the soil microbial communities exposed to long-term stress by heavy metal toxicity (sewage sludge) and low pH ((NH4)2SO4) were significantly smaller in magnitude than those under the three conventional (i.e. Ca(NO3)2, Straw + Ca(NO3)2, farmyard manure) input regimes (P < 0.05). The SIHP index however, was highest in the treatments receiving long-term inorganic inputs, indicating more heat production per unit biomass, than that found in all three organic input regimes. These differences in efficiencies were reflected in both the phenotypic and functional profiles of the communities. These indices may provide quantification of C assimilation and resource-use efficiency under different land-use and management scenarios, and potentially allow evaluation of the role of soils in governing the terrestrial C balance by studying the fate and regulation of C in soil systems.