The evolution of Fe(II)-oxidizing microorganisms has been closely linked to the evolution of Earth's iron biogeochemical cycle and redox history. However, its impact on the coupled biogeochemical cycling of iron and phosphorus, particularly the distribution of iron-bound phosphate (PFe) in water columns, remains largely unexplored. This study elucidates the distinct Fe(II) oxidation mechanisms of the anoxygenic Rhodobacter ferrooxidans SW2 and the oxygenic Synechococcus sp. PCC 7002, along with the properties, transformation processes, and phosphate interactions of their biogenic iron (oxyhydr)oxides. SW2-mediated Fe(II) oxidation via iron oxidase drove sequential transformation from ferrihydrite to green rust and then to goethite. The resulting cell-mineral aggregates had a large hydrodynamic diameter (Dh, up to 26 μm), a high Fe/C ratio (∼2.5), and a rapid sedimentation rate (up to 57.7 m/day), efficiently transporting PFe to deep-sea sediments. In contrast, PCC 7002 indirectly oxidized Fe(II) via oxygen production, forming poorly crystalline iron (oxyhydr)oxides stabilized by extracellular polymeric substances. The resultant small aggregates (Dh = ∼6.9 μm), with a slower sedimentation rate (∼3.9 m/day), exhibited high phosphorus retention and were susceptible to dissimilatory iron reduction, facilitating PFe recycling in surface waters. These findings suggest that biogenic iron (oxyhydr)oxides from anoxygenic iron oxidizers act as carriers, transporting phosphorus to deep sediments, whereas those from oxygenic cyanobacteria function as phosphorus traps in surface waters. This study provides new insights into how the evolution of Fe(II)-oxidizing microorganisms reshapes PFe cycling and distribution in water columns, emphasizing the need to integrate microbiological and geochemical perspectives in understanding Earth's biogeochemical cycles.

Fe(II)-catalyzed ferrihydrite (Fh) transformation is a critical process in biogeochemical cycling and contributes to paleoenvironmental reconstruction, yet the underlying mechanisms by which organic matter modulates these transformations remain poorly understood. This study elucidates how four common carboxylic ligands (acetate, oxalate, malonate and citrate), representing mono-, di- and tri-carboxylic types, regulate each step of Fe(II)-catalyzed Fh transformation, ultimately shaping transformation kinetics, and product phases. Batch transformation experiments under anoxic conditions at pH 7.0 were conducted to monitor Fe(II) speciation and intermediate labile Fe(III) (Fe(III)labile) accumulation over time, and the temporal evolution of mineral phases, morphologies, and particle sizes was investigated using powder X-ray diffraction, Fourier transform infrared spectroscopy, and transmission electron microscopy. By decoupling individual reaction step, we revealed the distinct effects of these ligands on Fe(II) adsorption on Fh, Fe(II)-Fh interfacial electron transfer (IET), and the repolymerization of Fe(III)labile into secondary minerals. The mono-carboxylic ligand acetate exhibits minimal influence on these reaction steps within the studied concentration range (0.4–2 mM). Di-carboxylic ligands (malonate and oxalate, 0.2–1 mM) reduce Fe(II) adsorption, with stronger inhibition at higher concentrations, while citrate uniquely enhances Fe(II) adsorption by forming ternary surface complexes. These results indicate that the multi-carboxylic ligands, in contrast to mono-carboxylic acetate with negligible effect, exhibit dual, concentration-dependent effects on Fe(II)-catalyzed Fh transformation: at low concentrations, they primarily enhance the electron-donating capacity of surface-associated Fe(II), thereby accelerating Fe(III)labile accumulation through promoted Fe(II)-Fh IET. As ligand concentration increases, their inhibition of Fe(III)labile repolymerization becomes dominant, markedly suppressing the consumption and nucleation of Fe(III)labile. Moreover, these inhibitory effects are more pronounced for ligands with more carboxyl groups. Notably, the strong linear correlation between effective (uncomplexed) Fe(III)labile concentrations and secondary mineral formation rates demonstrates that carboxylic ligands primarily regulate Fh transformation by modulating the availability of Fe(III)labile for nucleation, with the concept of “effective” Fe(III)labile, as refined in this study, offering a more precise mechanistic and quantitative descriptor of the reactive Fe(III) pool that remains available for nucleation despite partial complexation by carboxylic ligands. Although both are dicarboxylic ligands, malonate and oxalate differentially direct Fh transformation by altering the surface free energy and nucleation barriers of lepidocrocite and goethite through distinct adsorption structures, thus shaping their morphologies, particle sizes, and relative proportions. This study offers new mechanistic insight into how carboxylic ligands regulate Fe(II)-catalyzed Fh transformation, enhancing understanding of iron mineral-organic matter interactions and their implications for iron cycling and mineral evolution in natural environments.

Sulphate-reducing microorganisms, or SRMs, are crucial to organic decomposition, the sulphur cycle, and the formation of pyrite. Despite their low energy-yielding metabolism and intense competition with other microorganisms, their ability to thrive in natural habitats often lacking sufficient substrates remains an enigma. This study delves into how Desulfovibrio desulfuricans G20, a representative SRM, utilizes photoelectrons from extracellular sphalerite (ZnS), a semiconducting mineral that often coexists with SRMs, for its metabolism and energy production. Batch experiments with sphalerite reveal that the initial rate and extent of sulphate reduction by G20 increased by 3.6 and 3.2 times respectively under light conditions compared to darkness, when lactate was not added. Analyses of microbial photoelectrochemical, transcriptomic, and metabolomic data suggest that in the absence of lactate, G20 extracts photoelectrons from extracellular sphalerite through cytochromes, nanowires, and electron shuttles. Genes encoding movement and biofilm formation are upregulated, suggesting that G20 might sense redox potential gradients and migrate towards sphalerite to acquire photoelectrons. This process enhances the intracellular electron transfer activity, sulphur metabolism, and ATP production of G20, which becomes dominant under conditions of carbon starvation and extends cell viability in such environments. This mechanism could be a vital strategy for SRMs to survive in energy-limited environments and contribute to sulphur cycling.

Biotransformation of ferrihydrite (Fh) by dissimilatory iron-reducing bacteria (DIRB) into various secondary minerals assemblages widely occurs in anaerobic environments. While respiration-driven supply rates of Fe(II) have been proposed as a primary factor controlling kinetics and mineral products of this process, the specific mechanism by which DIRB respiration rates regulate Fh biotransformation remains elusive. Here, to minimize the complex effects of microbial cells, we conducted Fh transformation using 1 mM biogenic Fe(II) (BioFe(II)), added at different rates to mimic diverse respiration-driven supply rates of Fe(II) by DIRB. For comparison, transformation experiments with FeSO4 alone and FeSO4 plus citrate (CitFe(II)) added at the corresponding supply rates were performed to decouple the specific effects of Fe(II) addition rates and extracellular polymeric substances (EPS) associated with BioFe(II). Decreasing FeSO4 supply rates favored the transformation of Fh to lepidocrocite (Lp) over to Gt and the subsequent transformation of Lp to magnetite (Mt), altering the transformation pathway from Fh → Lp/Gt → Gt to Fh → Lp/Gt → Mt/Gt. These results underscore the significant effect of aqueous Fe(II) supply rates on the competition of olation and oxolation of labile Fe(III) intermediates into different secondary minerals. In the experiments with BioFe(II) and CitFe(II), although EPS or citrate slightly increased Fe(II) adsorption and Fe(III)labile generation, the increase in sorbed Fe(II) was minimal compared to the variations in aqueous Fe(II) concentrations caused by the different Fe(II) supply rates. At the same Fe(II) supply rates, EPS or citrate notably inhibited the transformation of Fh to Gt and the further conversion of Lp, altering the pathway from Fh → Mt/Gt/Lp to primarily Fh → Lp. These effects became more pronounced with the decrease of BioFe(II) and CitFe(II) supply rates. Our findings provide new insights into how DIRB respiration rates control kinetics, pathways, and mineral products of Fh transformation, which is crucial for elucidating the relevant biogeochemical cycling of nutrients and (im)mobilization of contaminants.