Lower microbial carbon use efficiency reduces cellulose-derived carbon retention in soils amended with compost versus mineral fertilizers

Cellulose decomposition is a key process in soil carbon (C) cycling due to the high abundance of cellulose in plant biomass. Microbial functional groups that sequester C from cellulose, and the accumulation of cellulose C in soil aggregates, remains debated. We hypothesized that cellulose derived 13C would be more efficiently converted into soil organic C by microorganisms, and retained in soil subjected to long-term application of compost. In this study, soil sampled from a long-term (27 years) field experiment with application of compost (Compost), NPK fertilizers (NPK) and without fertilizers (control), was incubated with 13C-cellulose for 120 days. The cellulose 13C content, microbial community structure (lipid biomarkers) and microbial 13C use efficiency (CUE) were measured. The incorporation of 13C into large macroaggregates (>2000 μm), small macroaggregates (250–2000 μm), microaggregates (53–250 μm), and silt + clay fraction (<53 μm) was analyzed to elucidate cellulose 13C sequestration process in aggregates. In contrast to our initial hypothesis, 13C remaining in soil after 120 days of incubation was maximal in unfertilized soil (25%) and minimal in Compost soil (17%). Compost soil had higher abundance of fungi and especially fast-growing bacteria (Gram-negative (G–) bacteria) than NPK and control soils. This accelerated decomposition and lowered CUE of 13C, therefore reducing the amount of 13C remaining in the Compost soil. In contrast, in the other soils, the lower fungal abundance reduced cellulose decomposition, which in turn contributed to growth of Gram-positive (G+) bacteria characterized by larger CUE than G– bacteria. This increased the ratio of G+/G– bacteria, resulting in larger CUE and more 13C remaining in NPK and control soils. Cellulose-derived 13C content decreased in small macroaggregates and microaggregates for all three soils, and in silt + clay fraction for the Compost soil; meanwhile, cellulose-derived 13C content increased in the silt + clay fraction for NPK and control soils from day 14 onwards. The ratios of 13C content in small macroaggregates and microaggregates to that in silt + clay fraction were higher in NPK and unfertilized soils than in Compost soil during the incubation. This indicated that less 13C was redistributed from large aggregates to silt + clay fraction in Compost soil. Overall, cellulose was more rapidly decomposed and incorporated into aggregates in organic C-rich soil, but their transformation efficiency into soil organic C was lower than in organic C-poor soil.