Rapid Decomposition of Gallic Acid in Anaerobic Conditions Mediated by Bacteria-Iron Mineral Interactions

It is widely held that polyphenols accumulate in soil due to limited phenol oxidase activity, thereby inhibiting resident microbes and promoting carbon stabilization. Contradicting this paradigm, we demonstrate that bioreduced Fe(II) from iron minerals may be enriched under anaerobic conditions, which accelerates phenol decomposition. Using gallic acid (GA) as a model, the biodegradation rate was 1.6-2.2 times higher under anaerobic conditions (k = 0.021-0.26 h^-1) compared to aerobic environments in bacteria (Bacillus megaterium, Lactoccus Lactis, or Shewanella putrefaciens) cocultured with iron oxides. Carbon mass balance and LC-MS analysis revealed that bacterial reduction of Fe(III) to Fe(II) shifted the GA transformation pathway from oxidative polymerization toward depolymerization, Fe(II)-complexation, and enhanced mineralization, increasing CO₂ release by approximately 3-fold. These changes were positively correlated with the Fe(II)/Fe(III) ratio. Electrochemical analysis confirmed that pseudocapacitance arising from Fe(II)/Fe(III) cycling at the mineral-biofilm interface reduced charge transfer resistance (e.g., from 16.58 to 6.93 Ω·cm^-2 for Fe₂O₃ system), accelerating GA mineralization. In contrast, aerobic conditions promoted Fe(III)-mediated phenol polymerization. Soil validation showed that the anaerobic GA degradation rate constant (k = 0.12 h^-1) and cumulative CO₂ production were 2 times and 1.5 times higher than under aerobic conditions, respectively. These findings challenge the classic view of polyphenol-driven carbon sequestration in saturated soils, highlighting the critical role of anaerobic microbe-mineral coupled iron redox cycling in regulating soil carbon turnover under changing redox conditions.