Influence of pO2 on Iron Redox Cycling and Anaerobic Organic

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Environmental Processes

Influence of pO2 on Iron Redox Cycling and Anaerobic Organic Carbon Mineralization in a Humid Tropical Forest Soil Chunmei Chen, Christof Meile, Jared Lee Wilmoth, Diego Barcellos, and Aaron Thompson Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b01368 • Publication Date (Web): 12 Jun 2018 Downloaded from http://pubs.acs.org on June 12, 2018

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Environmental Science & Technology

To Environ. Sci. & Technol.

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Influence of pO2 on Iron redox cycling and Anaerobic Organic Carbon Mineralization in a

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Humid Tropical Forest Soil

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Chunmei Chen1, Christof Meile2, Jared Wilmoth1, Diego Barcellos1, and Aaron Thompson1*

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University of Georgia, Crop and Soil Sciences, Athens, Georgia 30602, United States 2

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University of Georgia, Marine Sciences, Athens, Georgia 30602, United States

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Corresponding author

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*

Aaron Thompson, [email protected], (01) 706-410-1293

ACS Paragon Plus Environment


Abstract

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Ferrous iron (FeII) oxidation is an important pathway for generating reactive FeIII phases

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in soils, which can affect organic carbon (OC) persistence/decomposition. We explored how pO2

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concentration influences FeII oxidation rates and FeIII mineral composition, and how this impacts

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the subsequent FeIII reduction and anaerobic OC mineralization following a transition from oxic

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to anoxic conditions. We conducted batch soil slurry experiments within a humid tropical forest

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soil amended with isotopically-labeled 57FeII. The slurries were oxidized with either 21% or 1%

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pO2 for 9 d and then incubated for 20-d under anoxic conditions. Exposure to 21% pO2 led to

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faster FeII oxidation rates and greater partitioning of the amended 57Fe into low-crystallinity FeIII-

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(oxyhydr)oxides (based on Mössbauer analysis) than exposure to 1% pO2. During the subsequent

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anoxic period, low-crystallinity FeIII-(oxyhydr)oxides were preferentially reduced relative to

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more crystalline forms with higher net rates of anoxic FeII and CO2 production—which were

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well correlated—following exposure to 21% pO2 than to 1% pO2. This study illustrates that in

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redox-dynamic systems, the magnitude of O2 fluctuations can influence the coupled iron and

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organic carbon cycling in soils and more broadly, that reaction rates during periods of anoxia

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depend on the characteristics of prior oxidation events.

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TOC Art

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Introduction

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Iron (Fe) is an abundant redox-active element in soils 1-3, and conversions between FeII

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and FeIII can be mediated by both microbial and abiotic processes 4. Fe redox cycling is coupled

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to multiple biogeochemical cycles 5, 6. In natural environments, FeII can be oxidized via biotic or

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abiotic mechanisms coupled to O2 or NO3- 4, 7, 8, which contributes to the formation of FeIII

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(oxyhydr)oxides (hereafter referred to as FeIII oxides) of varying size, crystallinity, and purity in

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soils and sediments 3, 9-14. At circumneutral pH, abiotic oxidation dominates at high O2 levels,

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while abiotic and biotic oxidation may occur at comparable rates at low O2 levels.15, 16 The FeII

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oxidation and resultant precipitation of FeIII oxides in environments transitioning from anoxic to

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oxic conditions is a key process for retaining organic matter (OM), nutrients and contaminants 5,

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17-19

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the capacity to adsorb and/or incorporate a variety of constituents19-21. However, when O2

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becomes depleted in soils and sediments, FeIII oxides serve as important electron acceptors for

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microbial respiration 22-24, leading to the dissolution and transformation of solid phases and the

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release of sorbed and incorporated constituents 25-28. In addition, microbial FeIII reduction plays a

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central role in anaerobic OM mineralization in soils and sediments 23, 29-30. Microbial Fe

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reduction rates are influenced by the crystallinity of FeIII oxides 31-33, with short-range-ordered

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(SRO) phases (e.g., ferrihydrite, nano-goethite) favored over more crystalline forms 34, 35.

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Repeated reductive dissolution and transformation of and precipitation of FeIII oxide minerals

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can influence the crystallinity of those phases.3, 11, 36, 37Such redox cycling can be caused by

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periodic rainfall events or fluctuating water tables, which lead to temporal variations in soil O2

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concentrations.38-42 Thus, it has been suggested that in tropical humid forest soils subject to such

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conditions and rich in SRO FeIII oxides, microbial FeIII reduction may account for up to 44% of

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anaerobic organic carbon (OC) mineralization.22

. This is due to the physico-chemical properties of freshly formed FeIII oxides, which have



The influence of different patterns of O2 fluctuations (magnitude, duration and frequency)

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on Fe redox cycling and associated OC cycling is only beginning to be understood1, 11, 36, 43, 44.

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Ginn et al.1 showed that repetitive oscillations can lead to an overall increase in Fe reduction

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rates, which appears to be tied to the repeated formation (and dissolution) of rapidly reducible

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FeIII phases. During oxic periods, O2 concentrations are expected to control the oxidation rates of

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aqueous FeII 7 and influence the mineral composition of the resulting FeIII oxides 9, 45, 46. In a

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synthetic system of pure goethite, γ-Al2O3 and Suwannee River fulvic acid, Chen and Thompson

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exposed to low O2 conditions than when exposed to high O2. The degree to which O2 impacts the

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characteristics of FeIII precipitates depends on the type of mineral surface and OM present 47.

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However, the availability of the recently precipitated FeIII phases formed at varying O2 levels

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toward microbial reduction has not been directly evaluated in any system (synthetic or natural)

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that approximates soil or sediments by containing a mixture of aluminosilicates, Fe/Al oxides or

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other mineral phases and a variety of organic compounds 48, 49. Considering the range of

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naturally occurring environments such as wetlands and humid tropical forest that exhibit O2

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variations of 0-21% at the time scale of days to weeks driven by rainfall or changes in the water

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table38, 41, 50-52, a comprehensive understanding of the impacts of O2 concentration on the coupled

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structural and reactivity of FeIII-precipitates formed by FeII oxidation in soils and their impacts

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on C cycling is needed.

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have shown that FeII is oxidized at slower rates and results in more crystalline FeIII solids when

In this study, we hypothesized that in redox-fluctuating soils, higher O2 levels will lead to

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faster FeII oxidation rates and lower crystallinity FeIII solids, as well as greater subsequent

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microbial FeIII reduction and anaerobic OC mineralization following a transition from oxic to

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anoxic conditions. To test this, we amended isotopically-labeled 57FeII to soil slurries, oxidized


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soil slurries with continous 21% and 1% O2 respectively, and then re-exposed soil slurries to

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anoxic (N2-headspace) environment to promote Fe reduction. We tracked aqueous- and solid

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phase-FeII and 57Fe throughout the experiment, measured CO2 production during the anoxic

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period, and documented the solid-phase speciation of the spiked 57Fe using 57Fe Mössbauer

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spectroscopy. Materials and Methods

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Field site and soil characteristics Soil was collected from an upland valley site in the Bisley Research Watersheds of the

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Luquillo Experimental Forest, Puerto Rico, a NSF Long-term Ecological Research and Critical

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Zone Observatory (CZO) site. Soils are classified as Ultisols formed from volcanic parent

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material with quartz diorite intrusions53, 54. The abundant rainfall and warm temperatures,

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coupled with the high biological activity typical of humid tropical forests, lead to temporal

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fluctuations in bulk soil O2 concentrations, which vary from 0% to 21% over timescales of hours

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to weeks 38, 41. This can stimulate fluctuating FeII concentrations on similar timescales

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comprising gross Fe reduction and oxidation 55. We collected the upper 10 cm of the soil from

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the lower valley portion of Bisley Research Watershed site described elsewhere 1, 56, 57. Soils

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were placed in polypropylene ziplock bags, transported at field temperature to the University of

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Georgia and air-dried at 20 °C followed by dry sieving (< 2 mm) and homogenizing. The total

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soil Fe concentration, measured by ICP-MS following Li-metaborate fusion58 (Acme Labs,

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Vancouver, BC Canada), was 1152 mmol kg-1 soil. Total OC content measured via a Carlo Erba

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Elemental Analyzer was 4.8% (4000 mmol kg-1 soil). The concentration of short-range-ordered

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(SRO) FeIII-oxides (an index of the FeIII potentially reducible by microbes) was ~148 mmol Fe

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kg-1 soil (based on an ascorbic acid/citrate extraction with air-dried soil) 48. XRD revealed quartz



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(SiO2) as the major soil mineral, and a kaolinite group phase, a 2:1 layered aluminosilicate

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(likely chlorite), and goethite present in the soil clay fraction (< 2 mm).48

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Fe Oxidation and Reduction Experiments

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In soils, moisture and microbial activity largely control bulk pO2. While bulk soil pO2

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typically decreases from 21% up to 1% with soil moisture above field capacity52, 55, 59, 60, O2-

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limited (18 MO-cm) that was deoxygenated by sparging with N2 gas for 2 h and

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exposed to the glovebox atmosphere (95%/5% N2/H2 mix) for 48 h.

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All sampling was performed in the anoxic glove box. During oxic conditions, samples

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were moved temporarily (< 5 min) into the anoxic glove box for sampling. We monitored FeII

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and Fe isotopic compositions in both the aqueous (dissolved) phase and 0.5 M HCl-extract of

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soil slurry (See SI section 2 for detailed sampling). FeII in the aqueous sub-samples and the HCl-

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extracts was analyzed using a modified ferrozine protocol 1, 3, 44, in which the ammonium acetate

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buffer solution with pH 8.2 was used to accommodate the higher acid content. We selected HCl

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over organic-acid extractions because HCl has been shown to not introduce any isotopic

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fractionation of Fe during solubilization63, 64 and preserves FeII from oxidation during the

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analysis. The 0.5 M HCl extraction includes dissolved FeII in the aqueous phase, desorbs the

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majority of sorbed FeII and may also dissolve a portion of FeII in minerals such as siderite and

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magnetite1, 44, 65-67, although siderite formation is unlikely given the acidic pH (6) and a low

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carbonate concentration in our samples. We did not detect magnetite in our Mössbuaer analysis

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and therefore we assume the difference between HCl-extractable FeII and aqueous (dissolved)

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FeII can be attributed to sorbed FeII.

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Aqueous and HCl-extractable Fe isotope compositions were measured by inductively Coupled Plasma Mass Spectrometry (ICP-MS, Perkin Elmer, Elan 9000). Samples analyzed by



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ICP-MS were measured in an optimized DRC mode using reactive NH3 gas to minimize

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potential interferences from Ar, O, and H containing complexes that could convolute the mass-

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to-charge signal of Fe isotopes. The accuracy of this method was tested with Fe isotopic

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reference material IRMM-014. Repetitive measurements of isotopic fractions in IRMM-014

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were stable (4.56±0.11%, 93.12±0.22%, 2.02±0.12%, and 0.29±0.02% for f54Fe, f56Fe, f57Fe and

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f58Fe, respectively, n = 90). Total CO2 production was measured during the anoxic period. Reactors were crimp-

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capped with gas-tight lids inside the N2 chamber. Headspace gas was sampled immediately after

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capping and after 1 d for sampling during days 10-26 and after capping for 3 d during days 27-30

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(the last time point) to measured CO2 concentrations on a gas chromatograph with a thermal

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conductivity detector (Shimadzu, Columbia, MD, USA). The averaged CO2 production rate

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during the sampling periods was calculated on a soil mass (oven dry equivalent) basis as the

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difference of initial and final headspace CO2 mass concentration.

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57

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Fe Mössbauer Analysis Use of 57Fe isotopes allows us to track the amended 57Fe using Mössbauer spectroscopy,

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which detects only 57Fe atoms and not other Fe isotopes. To quantify the partitioning of the

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amended 57Fe via Mössbauer spectroscopy, we established a FeII-amended treatment with natural

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Fe isotope abundance prepared in the same exact way as the 57FeII-addition treatment described

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above, except that the FeII-bearing stock solution contained standard FeCl2·4H2O at natural

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isotopic abundance (~2.1% of 57Fe). The Mössbauer spectra of the amended 57Fe was then

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calculated as the difference between the spectra from the 57FeII-enriched treatment minus the

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baseline spectra obtained when adding FeII with natural isotopic abundance, after taking into

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account the different total 57Fe concentrations in the 57FeII-enriched treatment and the treatment


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adding FeII with natural isotopic abundance (see SI section 3 for further details). Therefore, the

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resulting Mössbauer spectra of the amended 57Fe excluded the spectral signal from the native soil

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Fe atoms. To prevent FeII oxidation, solid samples for 57Fe Mössbauer analysis were collected in

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the anoxic glove box following centrifugation at 20,000 g for 10 min, preserved between two

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layers of O2-impermeable Kapton tape (this step took 0.9) of FeII concentration over time during the anoxic period (SI

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Figure S3). Quantitatively, HCl-extractable FeII production rate ranged from 4.8– 7.2 mmol kg-1

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d-1, with dissolved and sorbed FeII being produced at rates of 1.2–2.2 and 4.0–5.3 mmol kg-1 d-1,

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respectively (SI Table S1). 57FeII-amended soils displayed greater HCl-extractable FeII

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production and thus higher FeIII reduction rates (5.7 – 7.2 mmol kg-1 d-1) than the control

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treatments containing only soil (~ 4.8 mmol kg-1 d-1) (SI Table S1). Oxidation of the control

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treatment (initially oxic soil with no FeII addition) with 21% and 1% O2 showed no difference in

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FeII production (and therefore FeIII reduction) during the subsequent anoxic period. In contrast,

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oxidation of 57FeII -amended soils with 21% O2 resulted in a greater FeIII reduction rate following

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a transition from oxic to anoxic period, compared to oxidation with 1% O2.

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Fe dynamics during the oxic-anoxic cycle The dissolved 57Fe/total Fe (FeT) ratio in the aqueous phase dropped from an initial value

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of 0.97 to 0.55 (first data point in Figure 2c) over the initial anoxic 1-day equilibration,

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indicating that a large proportion of the amended 57Fe underwent rapid atom exchange with

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native Fe in the soil prior to the oxidation event. Over the first day of oxidation with 21% or 1%

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O2, 57Fe fell below detection in the aqueous phase (Figure 2a) and remained undetectable until


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the subsequent anoxic period when the aqueous 57Fe/FeT ratio increased up to ~0.4, presumably

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due to reductive dissolution of 57FeIII formed either via oxidation/ precipitation of 57FeII or

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reductive dissolution of 57FeIII formed via atom exchange between 57FeII and native soil FeIII.

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Relative to oxidation with 1% O2, oxidation with 21% O2 resulted in greater solubilization of

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57

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higher FeII production rate. However, the aqueous 57Fe/FeT ratio during the anoxic period was

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similar for both of the 57Fe-amended soil treatments (21% and 1% O2, Figure 2c).

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CO2 production during the anoxic period

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Fluxes of CO2 during the 20-d anoxic period varied over time, but showed similar temporal

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trends across all treatments (Figure 3a). CO2 production peaked at day 16 (after 6 days of anoxic

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incubation) and declined afterwards. Generally, more CO2 was produced during the anoxic

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incubation from the 57FeII-amended soils than from the soil-only treatments (Figure 3a and 3b).

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While oxidation of the control (soil-only) treatment with 21 and 1 % O2 showed no differences in

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anoxic CO2 production, oxidation of the 57FeII-amended soils with 21% O2 led to more anoxic

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CO2 production than oxidation with 1%-O2 (Figure 3a and 3b). However, higher CO2 production

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was only evident between day 16 and 26, and from day 26 to 30 the 21%- and 1%-O2 oxidation

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treatments exhibited no differences in anoxic CO2 production in the 57FeII-amended soils (Figure

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3a). Overall, the cumulative anoxic CO2 production—which had a similar trend as FeII

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production across all the treatments—decreased in the order: 57FeII-amended soil with oxidation

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at 21% O2 > 57FeII-amended soil with oxidation at 1% O2 > the soil-only control treatments. The

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total CO2 production during the 20-d anoxic period accounted for 4.1-6.2% of total OC in the

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studied soil. In addition, rates of CO2 production were strongly correlated with FeII production

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under anoxic conditions (R2 = 0.94, P < 0.0001), with a ratio of produced FeII to CO2 of 5. This

Fe and total FeII during the subsequent anoxic cycle (Figure 2a and 2b), consistent with a



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is slightly higher than the stoichiometric ratio (~4) assuming microbial FeIII reduction is coupled

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to anaerobic mineralization of OC with a nominal oxidation state (NOSC) of zero30. It is possible

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that Fe-reducing microbes utilized OC with negative NOSC values68 or some FeII was generated

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by fermentative organisms that carry out incomplete C mineralization. Solid-phase partitioning

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of the added 57FeII following the initial 1-day anoxic period Collection of Mössbauer spectra at 140K, 77K, 12K, and 5K allows us to characterize the

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crystallinity-continuum of the FeIII-oxide solid phases in the sample. As temperature is reduced,

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portions of the FeIII-oxide populations are resolved as they magnetically order into a sextet

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(Figure 4 and SI Figure S2-4), with the more crystalline portions of the population ordering at

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higher temperatures10. In the initial unreacted soil sample, the spectral area assigned to the full

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FeIII-oxide sextets was 30.7%, 44.0%, 58.6%, 65.4% at 140K, 77K, 12K, and 5K, respectively

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(SI Figure S5 and Table S2). At 5K, we resolved the following Fe components in the initial

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unreacted soil: ~38% SRO- (e.g., nano-)goethite, ~27% ferrihydrite, ~14% most-disordered FeIII

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oxides (remain unordered at 5K), ~15% clay/OM-FeIII, as well as minor clay- FeII and ilmenite

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(

Influence of pO2 on Iron Redox Cycling and Anaerobic Organic

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