Molecular–Microbial Cascades Regulate Organic Phosphorus Mineralization in Lake Sediments

Organic phosphorus (Po) mineralization is a major internal source of soluble reactive phosphorus (SRP) in lakes, yet the molecular and microbial mechanisms governing this transformation remain poorly understood. Here, we aim to elucidate these mechanisms by integrating excitation-emission fluorescence spectroscopy, Fourier transform ion cyclotron resonance mass spectrometry (FT-ICR-MS), and metagenomics across two contrasting ecological niches in Taihu Lake, namely the Cyanophyta-dominated and macrophyte-dominated regions. We also supplement our results with the findings from a global meta-analysis. We found that fulvic-associated Po (Fu-Po) dominated sedimentary Po inventories, whereas Po extracted with NaHCO₃ (NaHCO₃-Po) and microbial biomass Po (biomass-Po) exhibited higher decomposition potential. Fluorescence indices indicated increasing lability with depth, and humic-like materials exhibited a higher tendency to be decomposed under anoxia, accompanied by the accumulation of fulvic-like fractions. FT-ICR-MS revealed proteins and lignins as key constituents of humic-associated Po and Fu-Po, supporting their bioavailability, while NaHCO₃-Po was enriched in compounds with lipid-like CHOSP formulas, suggesting greater lability. Metagenomics identified <i>phoD</i> as the most abundant phosphatase-encoding gene, with rare but highly connected <i>phoD</i>-harboring taxa emerging as potential keystone regulators alongside abundant functional groups. Across global lake sediments, alkaline phosphatase activity, Po content, and <i>phoD</i> abundance were found to covary positively, and structural equation modeling highlighted Fu-Po as a disproportionate indirect driver of SRP replenishment via <i>phoD</i>-mediated phosphatase activity. These findings reveal a mechanistic cascade linking molecular composition to <i>phoD</i>-mediated enzymatic potential in Po mineralization, identifying Po bioavailability, rather than inorganic phosphorus pools alone, as a critical driver for reducing internal loading. Targeting this pathway could modulate Po mineralization mechanisms in sediments worldwide, offering valuable insights into the management of lake eutrophication under accelerating nutrient pressures.