Drainage regulation enhanced the spatial heterogeneity of C, N, P, and S cycling genes and their microbial hosts along a cascade damming river

Understanding how seasonal hydrological regulations by cascade reservoirs affect biogeochemical processes is crucial for sustainable river management. This study used metagenomic sequencing and genome binning to explore the spatial dynamics of carbon, nitrogen, phosphorus, and sulfur (C, N, P, and S) cycling genes and their microbial hosts in a cascade-damming river, along with the associated regulatory mechanisms. The results revealed that multi-element biogeochemical cycling genes displayed significant seasonal variations, with pronounced spatial heterogeneity in the spring drainage period relative to the autumn storage period. Specifically, spring cascade-regulated reaches exhibited elevated gene abundances for carbon fixation and nitrification, alongside diminished potentials for carbon degradation and denitrification compared to natural river reaches, thereby corroborating the gene differentiation. The reduced residual of VPA (0.086 versus 0.742) and the elevated explanatory percentages of RDA (57.6% versus 31.4%) during spring suggested that hydrogeochemical variables explained greater variance in the cycling of C, N, P, and S in spring than in autumn, with hydrological regulations identified as the primary driver by PLS-PM. Spring drainage regulated the spatial heterogeneity of C, N, P, and S cycling through enhancing the longitudinal gradients of physicochemical parameters and nutrients. Conversely, autumn storage weakened longitudinal connectivity and flattened hydrogeochemical gradients. Raup-Crick null-model analysis revealed a higher contribution of stochastic processes in autumn than in spring (31.7% vs. 28.3%; p < 0.05). The metagenome-assembled genome further showed that hydrological regulations promoted the community's shift from the coexistence of diverse lineages during the drainage period to the dominance of a few core taxa during the storage period, reducing host turnover and intensifying functional homogenization in autumn. The findings necessitate season-specific management to mitigate spring eutrophication risks through optimal discharge and nutrient control and to preserve autumn functional complementarity through dynamic impoundment and water-level regulation.