From energy to (soil organic) matter

In this concept paper, we propose a new view on soil organic matter (SOM) formation: microorganisms use most of the organics entering the soil as energy rather than as a source of carbon (C), while SOM accumulates as a residual by-product because the microbial energy investment in its decomposition exceeds the energy gain. During the initial stages of decomposition, the nominal oxidation state of C (NOSC) in remaining litter decreases, and the energy content increases. This reflects the rapid mineralization of available compounds with positive and neutral NOSC (carboxylic acids, sugars, some amino acids). Consequently, the NOSC of the remaining compounds drops to −0.3 units, and the oxidation rate decreases due to the residual relative accumulation of aromatic and aliphatic compounds (which are hydrolized later) and entombment of the necromass. Ultimately, incompletely decomposed plant residues will have 1%–2.5% more energy per C unit than the initial litter. The linear decrease in energy density of a broad range of organic substances by 106 kJ mol−1 C per NOSC unit upon oxidation is supported by experimental data on litter decomposition. Preferential recycling of energy-rich reduced (lipids, aromatics, certain amino acids, amino sugars) and the microbial degradation of oxidized compounds (carboxylic acids) also energetically enrich SOM. Despite the high energy content, the availability of energy stored in SOM is lower than in litter. This explains why SOM is not fully mineralized (thermodynamically unfavorable), especially in the absence of plant C to provide new energy (e.g., in bare soil). Energy from litter activates decomposers to mine nutrients stored in SOM (the main ecological function of priming effects) because the nutrient content in SOM is 2–5 times higher than that of litter. This results in only 0.4%–5% year−1 of litter-derived C being sequestered in SOM, whereas SOM stores 1%–10% year−1 of the total litter-derived energy. 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. © 2022 John Wiley & Sons Ltd.