Plant Roots Exert Stronger Co-Structuring Effects than Soils on the Litter Microbial Community Following the Succession of Fagus lucida Forests

Clarifying the responses of microbial communities in distinct microhabitats like roots, the soil, and litter layers to secondary succession is critical for predicting the effects of global climate change on ecosystem functions. We investigated the microbial activities, compositions, and networks in these microhabitats of Fagus lucida forests ranging from 40 to 200 years. The results showed that soil physicochemical properties decreased with forest succession, except for NH4+-N and available phosphorus, which decreased at the early stage. All vector angles of extracellular enzyme stoichiometry that were greater than 45° indicated that phosphorus was the key limiting element for microorganisms. The microbial community shifted from r- to K-strategists with forest succession, displaying the replacement of most bacterial phyla by Proteobacteria and Acidobacteriota, and an increase in the Acidobacteriota: Proteobacteria ratio, especially in the soil and litter layers. Soil properties, particularly NH4+-N and pH, significantly affected the bacterial diversity and structure. Moreover, the bacterial network complexity increased with succession, particularly in the litter layer, and the topological properties of bacterial networks showed a stronger influence on microbial activities compared with those of fungal networks. The richness of keystone taxa in the litter layer was higher than in the soil layer and roots. However, the fungal community dominated by symbiotrophs showed lower sensitivity to soil nutrient changes and greater resilience to forest succession, displaying stable diversity and decreased network complexity, particularly in the roots. Ectomycorrhizal fungi (e.g., Russula) dominated the fungal guilds, and their abundance increased with forest succession, accompanied by a decrease in pathogenic fungi. Plant roots with significantly higher phosphatase activities played a stronger role than soils in structuring the litter microbial community, as reflected by similar carbon- and nitrogen-acquiring enzyme activities, microbial compositions, a greater share of taxa, and closer community distance. Our results revealed the increasingly important role of plant roots with forest succession in structuring the microbial community and nutrient cycling in the soil and litter layers.