Structural Diversity Controls Dissolved Organic Nitrogen Mineralization Driven by Dissimilatory Iron Reduction

Dissimilatory iron reduction (DIR) processes play a critical role in regulating the transformation of dissolved organic nitrogen (DON), yet the structural-dependent biogeochemical behaviors of DON from different sources remain poorly understood. Using a suite of complementary analytical techniques, we systematically compared the mineralization pathways and molecular transformations of nitrogen (N)-containing compounds in two representative dissolved organic matter (DOM): (1) dissolved black carbon (DBC) derived from pyrolysis (representing combustion-sourced DON from fire-affected ecosystem) and (2) leached dissolved organic carbon (LDOC) derived from compost (representing biogenic-sourced DON from undisturbed ecosystem), as sole electron donors during DIR. Batch experiments demonstrated that DBC produced three times more ferrous iron than LDOC and achieved a substantially higher mineralization ratios of N-containing compounds (41% versus 23% for LDOC), with ammonium being the sole detectable N mineralization product. Fourier-transform ion cyclotron resonance mass spectrometry (FT-ICR MS) combined with N near-edge X-ray adsorption fine structure (NEXAFS) analysis revealed that DBC degradation specifically targets polycyclic aromatic components rich in aromatic N, especially those in 5-membered rings (e.g., pyrrolic N), which account for nearly half of DON loss. In contrast, LDOC preferentially removes labile amide N from lignin-like components and enriches recalcitrant aromatic N from polycyclic aromatic components. The number of N-containing molecular formulas decreased by 51.6% in DBC but only by 10.2% in LDOC. Thermodynamic calculations confirm that aromatic N, particularly pyrrolic N, dominates the degraded DBC pool. These electron-rich Lewis basic structures form stable coordination complexes with iron that facilitate electron transfer and activate adjacent carbon bonds for oxidative ring-cleavage. The estimated electron flux derived from the degradation of pyrrolic N alone accounted for ~11% of the total ferrous iron produced in DBC, underscoring the critical role as a redox-active molecular "ignition points". In contrast, LDOC mineralization followed a conventional carbon-centered anaerobic pathway. This study elucidates the contrasting mineralization behaviors of biogenic-sourced and combustion-sourced DON driven by DIR, revealing fundamental structure-reactivity relationships that govern N biogeochemical cycling.