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Biochar-Facilitated Microbial Reduction of Hematite Shengnan Xu, Dinesh Adhikari, Rixiang Huang, Hua Zhang, Yuanzhi Tang, Eric E. Roden, and Yu Yang Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.5b05517 • Publication Date (Web): 02 Feb 2016 Downloaded from http://pubs.acs.org on February 2, 2016
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Environmental Science & Technology
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Biochar-Facilitated Microbial Reduction of Hematite
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Shengnan Xu1#, Dinesh Adhikari1, Rixiang Huang3, Hua Zhang1,2, Yuanzhi Tang3, Eric Roden4, Yu
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Yang1*
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1 Department of Civil and Environmental Engineering, University of Nevada, Reno, NV, 89557, USA;
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2 College of Environmental Science and Engineering, Guilin University of Technology, Guilin, Guangxi,
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541004, China;
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3 School of Earth and Atmospheric Sciences, Georgia Institute of Technology, 311 Ferst Drive, Atlanta,
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GA, 30332-0340, USA;
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4 Department of Geoscience, University of Wisconsin-Madison, 1215W. Dayton St., Madison,
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Wisconsin, 53706, USA.
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Current Address: Department of Civil and Environmental Engineering, University of Alberta,
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Edmonton, AB T6G 2R3, Canada
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*Corresponding Author: MS 258, 1664 N. Virginia Street, Reno, NV, 89523; Phone: 775-682-6609;
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Email:
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ABSTRACT
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As an important component of soil organic matter (SOM), the transformation of pyrogenic carbon plays a
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critical role in the biogeochemical cycles of carbon and other redox-active elements such as iron (Fe).
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Herein, we studied the influences of wheat straw-derived biochars on the microbial reduction of 100 mM
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of hematite by the dissimilatory metal reducing bacteria Shewanella oneidensis MR-1 under anoxic
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conditions. The long-term microbial reduction extent and initial reduction rate of hematite were
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accelerated by more than 2-fold in the presence of 10 mg L-1 of biochar. Soluble leachate from 10 mg L-1
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biochar enhanced Fe(III) reduction to a similar degree. Microbially pre-reduced biochar leachate
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abiotically reduced hematite, consistent with the apparent electron shuttling capacity of biochar leachate.
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Electron paramagnetic resonance (EPR) analysis suggested that biochar leachate-associated semi-quinone
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functional groups was likely involved in the redox reactions. In addition to electron shuttling effects,
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biochar particles sorbed 0.5-1.5 mM of biogenic Fe(II) and thereby increased the long-term extent of
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hematite reduction 1.4-1.7 fold. Our results suggest that Fe redox cycling may be strongly impacted by
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pyrogenic carbon in soils with relatively high content of indigenous pyrogenic carbon or substantial
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application of biochar.
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INTRODUCTION
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biogeochemical cycles of carbon and redox-active elements, such as iron (Fe).1-3 Under anoxic conditions,
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dissimilatory Fe(III)-reducing microorganisms are able to utilize humic substances as electron acceptors
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to oxidize organic compounds and gain energy for metabolic activities.4 As an electron shuttle, reduced
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humic substances can further transport electrons to poorly soluble Fe(III) (oxyhydr)oxides to facilitate
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their reduction.5 Quinone moieties in NOM have been shown to be the main functional group in
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mediating the electron transport between bacteria and Fe(III) oxides.6-8
Natural organic matter (NOM)-mediated microbial redox reactions are important for the
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Existing studies on the NOM-facilitated redox reactions have focused on aqueous phase and to a
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lesser extent solid-phase humic substances.9,10 In contrast, the impact of pyrogenic carbon on the
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reduction of Fe has received limited attention, despite the fact that pyrogenic carbon contains much more
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aromatic carbon and also likely a higher quinone content compared to humic substances.11-13 Pyrogenic
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carbon-mainly generated from incomplete combustion of biomass-contributes to 5-36% of total organic
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carbon in soils.14,15 Aromatic functional groups account for up to 90% of the carbon in pyrogenic organic
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matter, and substantial quinone contents have been detected in various pyrogenic carbons.16 This unique
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structural feature suggests that pyrogenic carbon may have the capability to facilitate electron transport
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during redox reactions. Previous studies have shown that biochar can facilitate the reductive degradation
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of toxic organic compounds.17-19 However, limited knowledge is available for the role of pyrogenic
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carbon in the redox reactions for Fe.20
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In this study, we investigated the role of biochars in the reduction of hematite by the dissimilatory
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Fe(III)-reducing bacterium (DIRB) Shewanella oneidensis MR-1. Biochar was used as a representative
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pyrogenic carbon, because it is widely present in soils and there are increasing interests in the application
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of biochar as agricultural soil amendments.21 The central goal of this work is to compare hematite
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reduction by S. oneidensis MR-1 in the presence and absence of biochars, and to elucidate the influences
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of physicochemical properties of biochar, especially the content of semi-quinone radicals. Our focus on
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the reduction of crystalline Fe(III) oxide differs from a recent study about the biochar-promoted reduction
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of synthetic ferrihydrite.22 Unlike poorly crystalline Fe(III) (oxyhydr)oxide ferrihydrite, crystalline Fe(III)
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oxide phases such as hematite do not typically undergo major recrystallization during microbial
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reduction,22, 23 which often plays a critical role in governing the long-term extent of amorphous Fe(III)
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oxide reduction.24 Rather, accumulation of aqueous Fe(II) and their sorption on the Fe(III) oxide and
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DIRB surfaces limit the long-term extent of reduction,25,
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ligands that complex with Fe(II) can increase the extent of Fe reduction by delaying/retarding Fe(II)
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sorption on the mineral and cell surfaces.27 The fact that biochar can bind a significant amount of Fe(II)
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and other divalent cations,28 raises the possibility that biochar could influence the rates of crystalline
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Fe(III) oxide reduction through both electron shuttling and Fe(II) binding effects, and is tested in this
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study.
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therefore both aqueous- and solid-phase
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MATERIALS AND METHODS
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Materials.
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Biochars were produced by pyrolyzing wheat straws at two different heat treatment temperatures
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(HTTs) (250 and 500 °C), and each of the two biochars were further fractionated into two size fractions
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(0.25-0.5 mm and
