Long-term NPK fertilization enhances microbial carbon use efficiency in Andosols by alleviating P limitation and shifting microbial strategies

Abstract

Microbial carbon use efficiency (CUE) is an essential indicator of soil organic carbon (SOC) dynamics. The high yield (Y)-resource acquisition (A)-stress tolerance (S) life strategy framework was used to assess microbial adaptation and its impact on CUE in response to soil environment and nutrient availability. Topsoil (0–15 cm) was collected from a 36-year experimental field of Andosol in Japan with six fertilizer treatments: no application, inorganic PK, NK, NPK, compost, and NPK with compost (NPKCM) to elucidate the effects of nutrient availability and environmental changes caused by fertilization on CUE. Soil chemical properties, microbial biomass and community structure, and extracellular enzyme activities (EEAs) were measured. Microbial nutrient limitation and CUE were assessed using enzyme stoichiometry (CUEst), and structural equation modeling (SEM) tested the conjecture that microbial nutrient limitation, mainly P-limitation, reduces CUEst through changes in bacterial community structures and EEAs. Results showed higher CUEst in NPK-treated soils (NPK: 0.37, NPKCM: 0.32) compared to P-deficient soils (Ctrl: 0.19, NK: 0.22). Increased P availability and reduced DOC:AP and IN:AP ratios in NPK-treated soils favored a shift of dominant bacterial strategies from A-strategists (including Alphaproteobacteria, Vicinamibacterales, and AD3) to Y-strategists (including Bacteroidota, Verrucomicrobiota, Blastocatellales, Bryobacterales, and Ktedonobacterales). SEM revealed that increased soil C and P availability alleviated microbial P limitation, enhancing CUEst directly and via reducing C-acquiring EEAs and altering microbial strategies. Overall, NPK fertilization may be an optimal strategy for enhancing SOC sequestration by improving microbial CUE in Andosols, emphasizing the trade-off between nutrient acquisition and energy conservation.