From energy to soil organic matter

Abstract

We developed a new concept of soil organic matter (SOM) formation and microbial utilization of organic carbon (C) and energy: microorganisms use most of the organics entering the soil as energy rather than as a C source, while SOM accumulates as a residual by-product because the microbial energy investment in its decomposition exceeds the energy gain. So, the energy use efficiency (EUE) is at least as important as the carbon use efficiency (CUE). The microbial EUE depends on the nominal oxidation state of carbon (NOSC) of organic compounds, which is the exact proxy of energy content: The energy content per C atom (enthalpy of combustion) increases by 108 kJ mol−1 C per one NOSC unit. The NOSC in litter remaining by decomposition decreases, and the energy content increases. Consequently, the NOSC of the remaining compounds drops to −0.3 units, and the oxidation decreases due to the residual accumulation of aromatic and aliphatic compounds, and entombment of the necromass. Preferential recycling of energy-rich reduced (lipids, aromatics, certain amino acids, amino sugars) and the microbial degradation of oxidized compounds (carboxylic acids) enrich energy content in remaining SOM. This explains why SOM is not fully mineralized (thermodynamically unfavorable). Energy from litter activates decomposers to mine nutrients stored in SOM (the main function of priming effects) because the nutrient content in SOM is 2–5 times higher than that of litter. Thus, the energy captured by photosynthesis is the main reason why microorganisms utilize organic matter, whereby SOM is merely a residual by-product of nutrient storage and a mediator of energy fluxes. For the first time we assessed the NOSC of microbial biomass in soil (−0.52) and calculated the corresponding energy content of −510 kJ mol−1 C, whereas bacteria contain less energy per unit of C than fungi. We linked CUE and EUE considering the NOSC of microbial biomass and element compositions of substrates utilized by microorganisms. The microbial EUE is always lower than CUE. This is one of the reasons why microbial growth is more limited by energy than by C. Based on the comparison of processes of C and energy utilization for cell growth and maintenance, we concluded that the two main mechanisms behind lower EUE versus CUE are: (i) microbial recycling: C can be microbially recycled, whereas energy is always utilized only once, and (ii) chemical reduction of organic and inorganic compounds: Energy is used for reduction, which is ongoing without C utilization. Gunina A, Kuzyakov Y 2022. From energy to (soil organic) matter. Global Change Biology 28 (7), 2169-2182Wang C, Kuzyakov Y 2023. Energy use efficiency of soil microorganisms: Driven by carbon recycling and reduction. Global Change Biology 29, 6170-6187