Article pubs.acs.org/est
Effects of Bound Phosphate on the Bioreduction of Lepidocrocite (γFeOOH) and Maghemite (γ-Fe2O3) and Formation of Secondary Minerals Edward J. O’Loughlin,*,† Maxim I. Boyanov,† Theodore M. Flynn,† Christopher A. Gorski,‡,§ Scott M. Hofmann,† Michael L. McCormick,∥ Michelle M. Scherer,‡ and Kenneth M. Kemner† †
Biosciences Division, Argonne National Laboratory, Argonne, Illinois 60439-4843, United States Department of Civil and Environmental Engineering, University of Iowa, Iowa City, Iowa 52242-1527, United States § Department of Civil and Environmental Engineering, The Pennsylvania State University, University Park, Pennsylvania 16802-7304, United States ∥ Department of Biology, Hamilton College, Clinton, New York 13323, United States ‡
S Supporting Information *
ABSTRACT: Natural FeIII oxides typically contain a range of trace elements including P. Although solution phase and adsorbed P (as phosphate) have been shown to impact the bioreduction of FeIII oxides and the formation of “biogenic” secondary minerals, little is known about the potential effects of occluded/incorporated phosphate. We have examined the bioreduction of FeIII oxides (lepidocrocite (γ-FeOOH) and maghemite (γ-Fe2O3)) containing 0−3 mass% P as “bound” (a term we use to include both adsorbed and occluded/ incorporated) phosphate. Kinetic dissolution studies showed congruent release of Fe and P, suggesting that the phosphate in these materials was incorporated within the particles; however, 53% or 86% of the total phosphate associated with the lepidocrocites containing 0.7 or 3 mass% P, respectively, was extracted with 0.1 M NaOH and can be considered to be adsorbed, both to exterior surfaces and within micropores. In the absence of phosphate, lepidocrocite was rapidly reduced to magnetite by Shewanella putrefaciens CN32, and over time the magnetite was partially transformed to ferrous hydroxy carbonate (FHC). The presence of 0.2−0.7 mass% P significantly inhibited the initial reduction of lepidocrocite but ultimately resulted in greater FeII production and the formation of carbonate green rust. The bioreduction of maghemite with and without bound phosphate resulted in solid-state conversion to magnetite, with subsequent formation of FHC. We also examined the potential redox cycling of green rust under alternating FeIII-reducing and oxic conditions. Oxidation of biogenic green rust by O2 resulted in conversion to ferric green rust, which was readily reduced back to green rust by S. putrefaciens CN32. These results indicate the potential for cycling of green rust between reduced and oxidized forms under redox dynamics similar to those encountered in environments that alternate between iron-reducing and oxic conditions, and they are consistent with the identification of green rust in soils/ sediments with seasonal redox cycling.
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containing structural FeII (e.g., magnetite, siderite, green rust, vivianite, ferrous hydroxy carbonate (FHC; also known as the mineral chukanovite)).2−5 The presence of dissolved and adsorbed phosphate has been shown to have significant effects on the rate and extent of the bioreduction of FeIII oxides and the formation of “biogenic” secondary mineralization products, particularly green rust (a mixed FeII/FeIII, layered double hydroxide).2,4−8 The FeII:FeIII ratio in green rusts typically
INTRODUCTION
The reduction of FeIII oxides by FeIII-reducing microorganisms is a major component of the biogeochemical cycling of Fe and can play an important role in the biogeochemical cycling of C in aquatic and terrestrial environments. Indeed, the occurrence of FeII in suboxic and anoxic environments is commonly attributed to the action of dissimilatory FeIII-reducing bacteria (DIRB) and archaea, phylogenetically diverse microorganisms that can obtain energy by coupling the oxidation of organic compounds or H2 to reduction of FeIII to FeII.1 The bioreduction of FeIII can yield a suite of FeII species including soluble FeII complexes, FeII complexes with the surfaces of organic and inorganic solid phases, and a host of mineral phases © 2013 American Chemical Society
Received: Revised: Accepted: Published: 9157
February 7, 2013 June 15, 2013 July 1, 2013 August 2, 2013 dx.doi.org/10.1021/es400627j | Environ. Sci. Technol. 2013, 47, 9157−9166
Environmental Science & Technology
Article
Table 1. Selected Properties of the Lepidocrocites and Maghemites Used in This Study and the Secondary Mineralization Products Resulting from Their Bioreduction identification of secondary mineralization productsd surface area m2 g−1
1 M HCl dissolution FeIII releasea mmol h−1
10 mM ascorbic acid dissolution FeII releaseb μmol h−1
total FeII productionc during bioreduction mmol d−1
% P by mass
molar ratio P:Fe
lepidocrocite L1
0e
0
73.1 ± 0.76
1.06 ± 0.04
14.7 ± 0.6
2.11 ± 0.09
maghemite M1
0e
0
98.2 ± 0.37
2.01 ± 0.05
15.8 ± 0.6
8.14 ± 2.48
lepidocrocite L2 (Bayferrox 943) maghemite M2 (Bayferrox 943 derived) lepidocrocite L3
0.18 ± 0.007
0.0045
17.6 ± 0.23
0.95 ± 0.02
6.5 ± 0.5
0.45 ± 0.03
0.21 ± 0.005
0.0057
79.8 ± 0.86
0.91 ± 0.02
16.2 ± 0.8
11.26 ± 2.77
Mag, FHC (minor)
Mag, FHC
Mag, FHC
0.27 ± 0.009
0.0074
36.9 ± 0.39
1.45 ± 0.02
10.0 ± 1.0
0.32 ± 0.01
GR, FHC
lepidocrocite L4
0.69 ± 0.012
0.0208
106 ± 1.16
10.17 ± 2.40
69.9 ± 3.4
0.30 ± 0.02
lepidocrocite L5
3.00 ± 0.014
0.1026
282 ± 3.23
93.18 ± 8.25
147.1 ± 9.9
0.70 ± 0.12
GR, FHC (minor) GR, FHC (minor) GR, Vivi (minor), FHC (minor)
GR, FHC GR, FHC GR, Viv
system
pXRD Magf, FHCg (minor) Mag, FHC (minor) GRh, FHC (minor)
Mössbauer
SEM
Mag, FHC
Mag, FHC Mag, FHC GR, FHC
Mag, FHC FHC, GR
GR, FHC GR, FHC, Viv
a
Dissolution rates were calculated by linear regression of the data during the period of linear FeIII release (see Figure S17). bDissolution rates were calculated by linear regression of the data during the period of linear FeII release (see Figure S18). cFeII production rates were calculated by linear regression using least-squares regression of the data during the period of maximum sustained FeII production (see Figure 3). dCharacterization at ∼1 year after inoculation. Additional information on pXRD, Mössbauer, and SEM imaging results is provided in SI. e
