A superoxide-driven pathway in the manganese cycle: Biogenic oxidation of Mn(II) by Pseudomonas sp. QJX-1 under glyphosate exposure

Biogenic manganese oxides (BMOs) are commonly found in groundwater and are widely used to remove a wide range of micropollutants. However, the impacts and mechanisms by which micropollutants affect biological Mn(II) oxidation remain unclear. In this study, glyphosate was found to significantly enhance biogenic Mn(II) oxidation by Pseudomonas sp. QJX-1 through the production of superoxide anion radicals (·O 2 − ). Glyphosate induced oxidative stress and impaired the electron transport chain (ETC) in QJX-1, particularly disrupting gene expression in complexes I, III, and IV. This disruption caused electrons to leak from the impaired electron transport chain, electrons interacted with molecular oxygen to form ·O 2 − . This was confirmed by the fact that ·O 2 − production increased by 69.49% with glyphosate compared to without glyphosate, and the addition of ·O 2 − scavengers completely suppressed Mn(II) oxidation. Moreover, glyphosate redirected electrons from the ADP to ATP conversion process toward ·O 2 − generation. NADH, the substrate of Complex I, acted as an electron donor driving ·O 2 − production, the addition of NADH significantly increased both ·O 2 − concentration and Mn(II) oxidation rate. These findings comprehensively elucidate the molecular mechanism of biogenic Mn(II) oxidation under glyphosate stress and provid valuable insights into the global Mn cycle in the environment. • QJX-1 produced extracellular ·O 2 − to indirectly oxidize Mn(II). • Glyphosate redirected electrons from the conversion of ADP to ATP toward the generation of ·O 2 − . • Glyphosate impaired the ETC in QJX-1, resulting in electron leakage. • The expression of genes related to complexes I, III, and IV was disrupted, causing electrons to leak from the ETC and interact with O 2 to form ·O 2 − .