Iron-organic matter complexes accelerate microbial iron cycling in an iron-rich fen

The accessibility of iron (Fe) species for microbial processes is dependent on solubility and redox state, which are influenced by complexation with dissolved organic matter (DOM) and water-extractable organic matter (WEOM). We evaluated the complexation of these pools of organic matter to soluble Fe(II) and Fe(III) in the slightly acidic Schlöppnerbrunnen fen and subsequent effects on Fe(II) oxidation and Fe(III) reduction. We found the majority of soluble Fe(II) and Fe(III) is complexed to DOM. High-resolution mass spectrometry identified potential complexing partners in peat-derived water extracts (PWE), including compound classes known to function as ligands or electron shuttles, like tannins and sulfur-containing compounds. Furthermore, we observed clear differences in the stability of Fe(II)- and Fe(III)-DOM, with more labile complexes dominating the upper, oxic layers (0-10 cm) and more stable complexes in lower, anoxic layers (15-30 cm). Metal isotope-coded profiling identified a single potential chemical formula (C₄₂H₅₇O₁₃N₉Fe₂) associated with a stable Fe-DOM complex. Fe(III) reduction and Fe(II) oxidation incubations with Geobacter sulfurreducens PCA and Shewanella oneidensis MR-1 or Sideroxydans CL-21, respectively, were used to determine the influence of Fe-DOM complexes on Fe cycling rates. The addition of PWE led to a 2.3-fold increase in Fe(III) reduction rates and 0.5-fold increase in Fe(II) oxidation rates, indicating Fe-DOM complexes greatly influence microbial Fe cycling by potentially serving as electron shuttles. Molecular analyses revealed Fe(III)-reducing and Fe(II)-oxidizing bacteria co-exist across all depths, in approximately equal proportions (representing 0.1-1.0% of the total microbial community), despite observed changes in redox potential. The activity of Fe(III)-reducing bacteria might explain the presence of the detected Fe(II) stabilized via complexation with DOM even under oxic conditions in upper peat layers. Therefore, these Fe(II)-DOM complexes can be recycled by microaerophilic Fe(II)-oxidizers. Taken together, these results suggest Fe-DOM complexation in the fen accelerates microbial-mediated redox processes across the entire redox continuum.