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Abstract

The reactivity of iron(III)-(oxyhydr)oxides toward microbial iron(III)-reduction is dependent on mineral reactive surface area and solubility, properties that can be altered by redox cycling. Because carbon (C) stability and nutrient availability can be influenced by redox dynamics, there is a need to evaluate the mechanisms that govern iron(III)-(oxyhydr)oxide transformations and strategies of microbial iron(III)-reducers to access these phases under fluctuating redox conditions in soils. To do this, we characterized the native iron phases in soils from the Bisley Watershed, Luquillo Critical Zone Observatory (LCZO), PR using selective chemical extractions, X-ray diffraction and 57Fe-Mssbauer spectroscopy. We then conducted laboratory experiments where we exposed the soils to redox cycles with variable iron(II)-oxidation rates and measured changes in the solution and solid phase iron speciation as well as sequenced mRNA extracted from native iron(III)-reducing bacteria. The native iron composition in the LCZO soil comprised goethite and lepidocrocite, with higher solid phase iron(II) correlated with higher lepidocrocite abundance and citrate-ascorbate extractable (low crystallinity) iron. 57Iron-Mssbauer spectra at 140 Kelvin (K) show that iron-(oxyhydr)oxides underwent either an increase or a decrease in crystal order due to rate of iron(II)-oxidation over multiple redox cycles in laboratory incubations. Soil RNA isolated following multiple redox cycles was subsequently depleted of rRNA and enriched for mRNA by linear amplification. De novo assembly of millions of paired-end Illumina reads was used to further examine the importance of several putative c-type cytochrome, pilin, exopolysaccharide, chemotaxis, TCA cycle and carbon degradation transcripts that were collectively binned to iron(III)-reducer genomes of Anaeromyxobacter, Geobacter and Desulfovibrio. We also enriched 57iron in soil incubations to track iron(III)-(oxyhydr)oxide formation. We found that rapid oxidation of enriched iron(II) generates short-range-ordered (i.e. low crystallinity) iron phases that are more readily solubilized by iron(III)-reducing microorganisms than the bulk native soil iron phases at the onset of iron(III)-reduction. Some 57iron-enriched solid iron(III) that is not reduced becomes incorporated into longer-range-order phases (i.e. higher crystallinity) during iron(III)-reduction. A portion of iron(II) formed in the solid phase during iron(III)-reduction displays weak magnetic order in the Mssbauer spectra collected at 4.5 K, perhaps arising from the formation of nano-magnetite or, more generally, iron(II) adsorbed/incorporated at the surface of short-range-ordered iron(III)-(oxyhydr)oxides. These processes regarding mineral-microbial interactions are expected to be linked to ecosystem-level nutrient cycling, carbon stability and global greenhouse gas emissions in highly-active, humid, tropical forest soils.

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