Abstract
Iron (Fe) oxides exist in a spectrum of structures in the environment, with ferrihydrite widely considered the most bioavailable phase. Yet, ferrihydrite is unstable and rapidly transforms to more crystalline Fe(III) oxides (e.g., goethite, hematite), which are poorly reduced by model dissimilatory Fe(III)-reducing microorganisms. This begs the question, what processes and microbial groups are responsible for reduction of crystalline Fe(III) oxides within sedimentary environments? Further, how do changes in Fe mineralogy shape oxide-hosted microbial populations? To address these questions, we conducted a large-scale cultivation effort using various Fe(III) oxides (ferrihydrite, goethite, hematite) and carbon substrates (glucose, lactate, acetate) along a dilution gradient to enrich for microbial populations capable of reducing Fe oxides spanning a wide range of crystallinities and reduction potentials. While carbon source was the most important variable shaping community composition within Fe(III)-reducing enrichments, both Fe oxide type and sediment dilution also had a substantial influence. For instance, with acetate as the carbon source, only ferrihydrite enrichments displayed a significant amount of Fe(III) reduction and the well-known dissimilatory metal reducer Geobacter sp. was the dominant organism enriched. In contrast, when glucose and lactate were provided, all three Fe oxides were reduced and reduction coincided with the presence of fermentative (e.g., Enterobacter spp.) and sulfate-reducing bacteria (e.g., Desulfovibrio spp.). Thus, changes in Fe oxide structure and resource availability may shift Fe(III)-reducing communities between dominantly metal-respiring to fermenting and/or sulfate-reducing organisms which are capable of reducing more recalcitrant Fe phases. These findings highlight the need for further targeted investigations into the composition and activity of speciation-directed metal-reducing populations within natural environments.
Highlights
Iron (Fe)oxide minerals are potent repositories of nutrients and metal(loid)s
Within both goethite and hematite enrichments, the amount of Fe(II) produced showed a strong dependence on sediment dilution, with most reduction occurring in the 10−3 dilution culture when lactate and glucose were provided as carbon sources (Figure 1)
Differences in community structure as a function of carbon source and sediment dilution dictated the amount of Fe(III) reduced and whether more recalcitrant Fe phases were available for reduction
Summary
Iron (Fe) (hydr)oxide minerals are potent repositories of nutrients (e.g., phosphate) and metal(loid)s (e.g., arsenic). Release of these elements into the aqueous milieu may occur upon dissolution of the Fe (hydr)oxides mediated by a number of abiotic and biotic processes. The biotic mechanisms of Fe(III) reduction within soils and sediments are primarily attributed to either an indirect consequence of fermentation or microbial respiration, in which organisms couple the oxidation of carbon or molecular hydrogen to the reduction of Fe(III) for energy conservation (dissimilatory reduction). Microbial Fe(III) reduction accounts for a up to 50% of carbon oxidation in non-sulfidogenic sediments (Canfield et al, 1993; Thamdrup, 2000)
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