Mineralogical, Physical and Geochemical Factors that Drive Microbial Reduction of Iron Oxides and Diagenesis under Broad Environmental Conditions

Iron reduction by dissimilatory iron-reducing bacteria (DIRB), coupled with the oxidation of organic compounds or H2, causes formation of post-depositional (diagenetic) Fe(II)-containing minerals. Previous studies on the composition, distribution and precipitation rates of secondary minerals during microbial iron reduction have primarily focused on ferrihydrite reduction by Shewanella spp. However, comparatively little is known about these processes by a variety of other DIRB and the effect of specific environmental factors on Fe(II)-bearing mineral diagenesis. Here we examine how environmental conditions influence the reduction of ferric iron minerals by Orenia metallireducens strain Z6, a DIRB from the phylum Firmicutes. This includes the effects of: (1) pH at 6.5-8.5; (2) temperature at 22-50 °C; (3) salinity at 2-20% NaCl; (4) solution chemistry of phosphate and sulfate; (5) electron shuttles (e.g., anthraquinone-2,6-disulfonate (AQDS)); and (6) iron oxides, including ferrihydrite, lepidocrocite, goethite, hematite, and magnetite. For a total of 19 culturing conditions, we measured ferrous iron produced over time using the ferrozine assay and formation of secondary minerals using scanning electron microscopy with energy-dispersive X-ray spectroscopy (SEM-EDS), X-Ray Diffraction (XRD), and extended X-ray absorption fine structure spectroscopy (Fe-edge XANES and EXAFS). Results show that both the rate and extent of DIRB reduction of ferrihydrite and lepidocrocite vastly exceeded those of the more crystalline minerals. The microscopic and spectroscopic analyses indicate diversity in the composition and relative abundance of Fe(II)-containing minerals such as green rust, siderite, magnetite and/or vivianite under the different experimental conditions. However, the secondary mineralization products cannot be attributed to either the extent or kinetics of Fe(II) generation. Instead, the composition of these digenetic minerals resulted from the intricate interplay of precipitation dynamics, adsorption of Fe(II), and subsequent transformation (dissolution and reprecipitation). This study establishes the first mechanistic understanding of biomineralization of Fe(II) bearing minerals during microbial iron reduction under a broad range of environmental conditions.