Microbial and abiotic interactions driven higher microbial anabolism on organic carbon accumulation during 2000 years of paddy soil development in the Yangtze River Delta, China

Paddy soil as a major component of cropland, plays an important role in the global carbon (C) cycle and favors carbon sequestration especially in southern China. Soil microorganisms are central to the conversion of organic matter into SOC, yet the mechanisms underlying the paddy management at long time scales remain largely unknown, including microbial enzyme and functional potential kinetics, microbial growth and turnover. Here, using observations from a 2000-year-old paddy chronosequence since reclamation from tidal wetland at two different soil depths (0-20 cm and 20-50 cm) in the Yangtze River Delta, China, we show how paddy soil C sequestration is driven by the relationship between short-term responses in microbial physiology and long-term changes in biogeochemical soil properties. The samples were analyzed for nutrient pools, microbial biomass and growth, microbial activity and community composition, functional gene abundances, as well as microbially mediated nitrogen (N) cycling rate to determine how these microbial functionalities and processes affect microbial carbon use efficiency (CUE), an important indicator for microbial C sequestration. Across multiple time-scales ranging from decades to millennia, SOC in topsoil was increased by 65% during the first 50 years and reached the steady-state condition until 700-year, then was largely accumulated by 169% and 125% in 1000- and 2000-year, respectively, while C loss appeared in subsoil after 700 years of paddy cultivation. For topsoil and subsoil, microbial CUE reached to the highest values in 1000- and 700-year (0.46 and 0.36, respectively, while only 0.20 in the tidal wetland), along with microbial growth which both increased 5.2- and 3.3-fold in 1000-year, respectively. We found the similar increasing trends between microbial CUE and soil C:P and N:P ratios, the reduction of N limitation and functional potentials including N- and P-cycling, C degradation, C-fixation (acsA gene), microbial community homogenization and microbial biomass across soil chronosequence in topsoil. Moreover, the structural equation model revealed that with longer paddy management, the decline in soil pH had positive effects on microbial functional potentials and microbial biomass carbon. The enhanced functional potentials directly positively affected microbial growth, and thereby on microbial biomass carbon. Finally, the prolonged paddy cultivation increased SOC content via its direct positive effect and indirect positive influence on microbial biomass carbon. We conclude that longer paddy management captures the cumulative microbial anabolism on SOC sequestration in the plough layer, with the shifts in abiotic and biotic conditions towards increased nutrient availability and homogenous microbial community with higher functional potentials.