Multi-omics reveals niche partitioning of nitrogen and phosphorus cycling between free-living and particle-attached fractions across an N:P gradient in eutrophic Lake Taihu.

Cyanobacterial blooms in hyper-eutrophic lakes are managed through nitrogen-to-phosphorus (N:P) control, yet single-axis nutrient reduction has often been insufficient to achieve sustained bloom suppression in shallow systems such as Lake Taihu, China. We hypothesised that the missing management dimension is spatial: free-living (FL, 0.22-3 µm) and particle-attached (PA, >3 µm) fractions may deploy distinct nutrient-acquisition machineries under the same bulk N:P. Native Lake Taihu assemblages were cultured at four N:P molar ratios (5, 16, 23, 40; TN fixed at 2.0 mg N L⁻¹; TP adjusted to 0.886, 0.277, 0.192, and 0.111 mg P L⁻¹, respectively) for 28 days, then sequentially filtered and analysed by 16S amplicon sequencing, shotgun metagenomics and 15-T Fourier-transform ion cyclotron resonance mass spectrometry (FT-ICR-MS) of dissolved organic matter (24 paired-fraction biomass samples + 8 DOM samples). Three key findings emerged. First, FL and PA carry the genetic potential for chemically distinct phosphorus-acquisition strategies (hereafter termed the P-currency split): FL is enriched in the high-affinity inorganic-Pi transporter genes pstSCAB (dominated by Synechococcus), whereas PA carries the genetic potential to mobilise organic P via phoD and ugpQ (dominated by Bacteroidota); the PstS + Ppk1 dual-wheel hypothesis was not supported under fraction-resolved testing. Second, PA harbours the genetic potential for a consistent nitrogen-cycle hotspot across all N:P levels, with nifH enriched 1.8-5.0-fold in PA and 87% attributable to the heterotroph Porphyrobacter. Third, Synechococcus shows an apparent stoichiometric niche-shift from FL dominance at N:P = 23 (43.8%) to PA dominance at N:P = 40 (54.1%). Together, the joint N:P × fraction model explained 95.8% of community variance (Mantel r = 0.963 within PA). These findings identify the phoD-anchored Bacteroidota guild and PA-aggregate disruption as candidate fraction-resolved management levers that complement conventional nutrient reduction in shallow eutrophic lakes.