Microbial Reduction of Crystalline Iron(III) Oxides:  Influence of Oxide Surface Area and Potential for Cell Growth

Abstract

Quantitative aspects of microbial crystalline iron(III) oxide reduction were examined using a dissimilatory iron(III) oxide-reducing bacterium (Shewanella alga strain BrY). The initial rate and long-term extent of reduction of a range of synthetic iron(III) oxides were linearly correlated with oxide surface area. Oxide reduction rates reached an asymptote at cell concentrations in excess of ≈1 × 109/m2 of oxide surface. Experiments with microbially reduced goethite that had been washed with pH 5 sodium acetate to remove adsorbed Fe(II) suggested that formation of a Fe(II) surface phase (adsorbed or precipitated) limited the extent of iron(III) oxide reduction. These results demonstrated explicitly that the rate and extent of microbial iron(III) oxide reduction is controlled by the surface area and site concentration of the solid phase. Strain BrY grew in media with synthetic goethite as the sole electron acceptor. The quantity of cells produced per micromole of goethite reduced (2.5 × 106) was comparable to that determined previously for growth of BrY and other dissimilatory Fe(III)-reducing bacteria coupled to amorphous iron(III) oxide reduction. BrY reduced a substantial fraction (8−18%) of the crystalline iron(III) oxide content of a variety of soil and subsurface materials, and several cultures containing these materials were transferred repeatedly with continued active Fe(III) reduction. These findings indicate that Fe(III)-reducing bacteria may be able to survive and produce significant quantities of Fe(II) in anaerobic soil and subsurface environments where crystalline iron(III) oxides (e.g., goethite) are the dominant forms of Fe(III) available for microbial reduction. Results suggest that the potential for cell growth and Fe(II) generation will be determined by the iron(III) oxide surface site concentration in the soil or sediment matrix.

Fe(III) Oxide Reactivity Toward Biological versus Chemical Reduction

“…The results of the experiments shown in Figure 1A confirm the general linear dependence of initial bacterial Fe(III) oxide reduction rate on oxide surface area documented in previous experiments with a smaller suite of synthetic oxides (7). The consistent linear correlation between oxide reduction rate and surface area across a wide range of FeRB cell densities ( Figure 2A) indicates that limitations on reduction rate posed by reductant abundance were not responsible for linearization of an otherwise logarithmic rate vs surface area relationship.…”

Dissimilatory bacterial reduction of Al-substituted goethite in subsurface sediments

“…Although not well studied, natural crystalline Fe(III) oxides, including both goethite and hematite, appear more reducible than those synthesized in the laboratory (Roden and Zachara, 1996;Zachara et al, 1998). The reasons for this observation have not been confirmed but isomorphous substitution of Fe(III) by other metals (e.g., Al(III)), and larger crystallite disorder, surface roughness, and surface area of natural Fe(III) oxides may be important.…”

“…Amorphous and crystalline Fe(III) oxides are utilized as electron acceptors by dissimilatory Fe-reducing bacteria (DIRB) (Lovley and Phillips, 1986;Arnold et al, 1986;Roden and Zachara, 1996;Fredrickson et al, 1998;Zachara et al, 1998). S. alga and other facultative Shewanella strains can grow, albeit slowly, using ferrihydrite and goethite as sole electron acceptors (Roden and Zachara, 1996).…”

“…S. alga and other facultative Shewanella strains can grow, albeit slowly, using ferrihydrite and goethite as sole electron acceptors (Roden and Zachara, 1996). Synthetic goethite is resistant to bacterial reduction and, in general, is incompletely reduced in presence of excess electron donor and large cell populations (e.g., Ͼ10 8 cells/mL).…”

“…Synthetic goethite is resistant to bacterial reduction and, in general, is incompletely reduced in presence of excess electron donor and large cell populations (e.g., Ͼ10 8 cells/mL). Low solubility, saturation of the residual oxide and bacterial surfaces with biogenic Fe(II), free energy availability, and complex physiologic factors apparently control the rate and extent of reduction (Roden and Zachara, 1996;Urrutia et al, 1998;Zachara et al, 1998;Liu et al, 2001). Aqueous and solid-phase ligands that withdraw biogenic Fe(II) from the oxide and bacterial surfaces tend to increase the extent of goethite reduction (Urrutia et al, 1998(Urrutia et al, , 1999, presumably by reducing the surface saturation of Fe(II).…”