Fate of As(III) and As(V) during Microbial Reduction of Arsenic-Bearing

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Fate of As(III) and As(V) during microbial reduction of arsenic-bearing ferrihydrite facilitated by activated carbon Song Wu, Guodong Fang, Dengjun Wang, Deb P. Jaisi, Peixin Cui, Rui Wang, Yujun Wang, Lu Wang, David M. Sherman, and Dongmei Zhou ACS Earth Space Chem., Just Accepted Manuscript • DOI: 10.1021/ acsearthspacechem.8b00058 • Publication Date (Web): 09 Jul 2018 Downloaded from http://pubs.acs.org on July 10, 2018

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ACS Earth and Space Chemistry

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Fate of As(III) and As(V) during microbial reduction of

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arsenic-bearing ferrihydrite facilitated by activated carbon

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Song Wu†, #, Guodong Fang†, Dengjun Wang‡, Deb P. Jaisi§, Peixin Cui†, Rui Wang†, #,

5

Yujun Wang*, †, Lu Wang∥, David M. Sherman 丄, Dongmei Zhou*, †

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†

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Science, Chinese Academy of Sciences, Nanjing 210008, P.R. China

9

‡

Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil

National Research Council Resident Research Associate at the U.S. Environmental

10

Protection Agency, Ada, OK 74820, USA

11

§

Department of Plant and Soil Sciences, University of Delaware, Newark 19716, USA

12

∥

13

Technology, Harbin 150090, China

14

丄

15

State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of

#

Department of Earth Sciences, University of Bristol, Bristol BS8 1RJ, UK

University of Chinese Academy of Sciences, Beijing 100049, P.R. China

16 17

*Corresponding authors: Phone: +86 25 86881180. Fax: +86 25 86881000. E-mail:

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[email protected] (Y.J. Wang), [email protected] (D.M. Zhou).

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ACS Paragon Plus Environment

ACS Earth and Space Chemistry 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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Abstract

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Microbial reduction of arsenic (As)-bearing Fe(III)-(oxyhydr)oxides is one of the

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major processes for the release of As in various environmental settings such as acid

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mine drainage, groundwater, and flooded paddy soil. Pyrogenic carbon has recently

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been reported to facilitate microbial extracellular reduction of Fe(III)-(oxyhydr)oxides.

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The aim of this study was to investigate the important hot topic regarding the fate and

25

transformation of As during activated carbon (AC) facilitated microbial reduction of

26

As-bearing ferrihydrite. Our results show that the rate and extent of Fe(III) reduction

27

in As-bearing ferrihydrite by Shewanella oneidensis MR-1 were accelerated by AC.

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The AC facilitated reduction caused the release of As(III) into the solution, whereas

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the preferential immobilization of As(V) on the solid phase. Furthermore, AC

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accelerated the precipitation of vivianite and siderite in sequence during microbial

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reduction processes. Both of the formed vivianite and siderite had an insignificant

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capacity for capturing As(III); however, As(V) was selectively immobilized by

33

vivianite compared to that of siderite. Taken together, our findings provide crucial

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insights into understanding the role of AC on the redox and immobilization of Fe and

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As in sub-oxic and anoxic environments and thus their environmental fate when

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pyrogenic carbons are employed for agronomic and environmental applications.

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Keywords: activated carbon, Fe reduction, arsenic, vivianite, siderite, extracellular

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electron transfer

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1. Introduction

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Arsenic (As) is a pervading environmental toxin that widely distributes in the

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natural environments such as in groundwater and paddy soils and is endangering

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human health throughout the world.1 Fe-(oxyhydr)oxides have commonly been

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identified as one of the key (geo)sorbents for As sequestration in soils and sediments.2,

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3

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inner-sphere adsorption complexes on Fe(III)-(oxyhydr)oxides including ferrihydrite,

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goethite, lepidocrocite, and hematite.4, 5 However, the capability of As sequestration

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by Fe(II)-(oxyhydr)oxides and mixed-valence Fe(II, III)-(oxyhydr)oxides varies

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markedly.6, 7 For example, As(III) is demonstrated to form weak outer-sphere complex

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on siderite,8 whereas As(V) partly replaces phosphorus in vivianite via substitution.9

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The formation, transformation, and fate of Fe-(oxyhydr)oxides are mainly driven by

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microbial activities.10 Hence, microbial reduction of Fe(III)-(oxyhydr)oxides and their

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associated contaminant (e.g., As) dissolution are highly interconnected to

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release/retention of As especially in groundwater and paddy soil environments.11, 12

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Microbial reduction of Fe(III)-(oxyhydr)oxides, owing to the poor solubility of Fe3+ in

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Fe(III)-(oxyhydr)oxides at circumneutral pH conditions, requires extracellular

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electron transfer processes, i.e., electron transfer via cell surface-localized c-type

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cytochromes, redox-active electron shuttles, and (or) electrically conductive pili.13 For

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instance, extracellular redox-active electron shuttles secreted by bacteria promote the

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microbial reduction of Fe(III)-(oxyhydr)oxides.14,

Arsenic occurs as As(III) and As(V), and both As(III) and As(V) can form strong

15

3


Besides, environmentally


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ubiquitous humic substances have been known as effective extracellular electron

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shuttles, facilitating microbial reduction of Fe(III)-(oxyhydr)oxides.16

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Pyrogenic carbon including soot, char, black carbon, activated carbon (AC), and 17

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biochar

is a powerful adsorbent for the sequestration of a series of organic and

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inorganic contaminants,18, 19 but with the exception of some oxyanions.20 In addition

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to the adsorption functionality, pyrogenic carbon has recently been reported to be

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redox active.21, 22 The surface redox-active quinone/hydroquinone groups in pyrogenic

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carbon

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the acceleration of microbial extracellular electron transfer processes. As

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aforementioned, the reduction of Fe(III)-(oxyhydr)oxides and its associated

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concomitant

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Fe(III)-(oxyhydr)oxides. For instance, anthraquinone-2,6-disulfonate and riboﬂavin

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are able to serve as electron shuttles to promote the reductive dissolution of As and

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Fe.27 However, the similar role of pyrogenic carbon in these redox processes remains

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less understood.28, 29 The major reason for this knowledge gap is likely related to its

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previously unconcerned redox characteristics.

23, 24

combined with its electrical conductivity 25, 26 are found to be crucial for

dissolution

affect

the

release

of

As

originally

bound

to

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Given that pyrogenic carbon is increasingly used for environmental remediation

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and acts as a soil conditioner,30, 31 research on its role in influencing the fate of As is

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increasingly important.32 Moreover, little effort has been devoted to understand the

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sequestration of As in the biogenic secondary minerals that are formed after the

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reduction of Fe(III)-(oxyhydr)oxides in the presence of electron shuttles. AC

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impregnated Fe-(oxyhydr)oxides has been found to be a reliable sorbent for effective

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As removal from wastewater and groundwater.33, 34 Furthermore, compared to biochar,

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the highly carbonized AC does not release a significant amount of dissolved organic

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carbon that plays an important role in the redox reactions.23, 24 Therefore, the main

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focus of this study was to identify the fate of As(III) and As(V) during the facilitated

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microbial reduction of As-bearing ferrihydrite by AC. The specific objectives were to:

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(i) determine the role of AC on microbial reduction of As(III)-bearing ferrihydrite

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(As(III)-FH), As(V)-bearing ferrihydrite (As(V)-FH), and pure ferrihydrite (FH) alone,

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(ii) evaluate the effect of FH reduction on As release/retention, and (iii) identify the

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As speciation and binding environment in the secondary biogenic minerals formed

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during microbial reduction processes.

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2. Materials and Methods

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2.1. Preparation of activated carbon, incubation of bacteria, and synthesis of

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minerals

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The AC was purchased from Sinopharm (AC-W, catalog no.7440-44-0), and was

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used in our previous studies.23, 35 The other two ACs were obtained by oxidizing

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AC-W powders in a concentrated HNO3 for 2 h or 4 h (designated as AC-W-N2 and

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AC-W-N4, respectively) at 90 °C. The resulting ACs were ball milled and then

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characterized by speciﬁc surface area analyzer, X-ray photoelectron spectroscopy, and

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Fourier transformed infrared measurements, as described previously.35 The diameter

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of more than 90% of the particles in each AC sample was less than 10 μm.23 The 5



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content of redox-active oxygen-containing functional groups (e.g., quinone/phenol) in

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AC increases with the treatment time by HNO3 and is crucial for promoting microbial

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reduction of FH.23 The as-prepared ACs were suspended in water to a final

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concentration of 20 g L-1, purged with N2 to remove dissolved oxygen, and then

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sealed and autoclaved at 120 °C for 20 min.

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Shewanella oneidensis MR-1, a well-known bacterium for Fe(III) reduction in

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various ferruginous minerals, soils, and sediments,36 was cultured aerobically for 18 h

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in the Luria-Bertani medium in an incubator (150 rpm, 28 °C). The bacterial cells

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were harvested by centrifugation (6,000×g for 6 min), washed with anoxic

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bicarbonate buffer (30 mM, pH 7.0), and then re-suspended in an anoxic bicarbonate

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buffer before use (~2 × 1011 cells mL-1).

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The FH minerals (As(III)-FH, As(V)-FH, and FH) were synthesized by adding

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different amounts and species of As. Briefly, the continuously-stirring Fe(NO3)3·9H2O

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(40.4 g L-1) solutions that contain 0, 1.94 g L-1 of NaAsO2, and 4.66 g L-1 of

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Na2HAsO4·7H2O were neutralized by 1 M of KOH solution to synthesize FH,

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As(III)-FH, and As(V)-FH, respectively.37 The Fe:As ratio was kept at 50:1 (w:w) for

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As(III)-FH and As(V)-FH minerals. The synthesized Fe(III)-(oxyhydr)oxide minerals

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were washed and then suspended in deionized water (normalized to 200 mM of

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Fe(III)) which was deoxygenated by N2 purging for 2 h, and then stored in sealed

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serum bottles.

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2.2. Activated carbon mediated microbial reduction of As-bearing ferrihydrite

6


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Batch experiments were performed in 100 mL serum bottles containing 40 mL of

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anoxic mineral medium (pH 7, 30 mM bicarbonate buffer, 0.6 g L-1 KH2PO4, 0.3 g L-1

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NH4Cl, 0.5 g L-1 MgSO4·7H2O, 0.1 g L-1 CaCl2·2H2O, 1 mL L-1 vitamin solution, 1

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mL L-1 trace element solution, and 1 mL L-1 selenate-tungstate solution).23 The 30

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mM sodium lactate was used as the electron donor and 2 mL of the As(III)-FH,

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As(V)-FH, and FH minerals served as the electron acceptors (at a final concentration

129

of 10 mM of Fe(III) in each experiment). A 2 mL of AC-W, AC-W-N2, or AC-W-N4

130

(at a final concentration of 1 g L-1) stock suspension prepared in anoxic water (or

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anoxic water alone for biotic control) was added as a potential electron shuttle for the

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three different types of FHs. A 1 mL of S. oneidensis MR-1 stock in the anoxic buffer

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(or anoxic buffer alone for control) was then syringed into the serum bottles to initiate

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the microbial reduction of Fe(III) in FHs. All treatments were performed in batch

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incubation (80 rpm, 28 °C) in quintuplicates. Subsamples were withdrawn at

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predetermined time intervals for the analyses of Fe and As. Briefly, a 0.1 mL of

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subsample was transferred into 1 mL of 1 M HCl to dissolve solid minerals for the

138

quantification of total Fe and Fe(II) contents.23 A ~0.1 mL filtrate of the culture

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suspension (filtrated through a 0.22 μm filter) was diluted in 1 mL of 1 M HCl or 10

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mM H3PO4 to quantify the dissolved Fe(II) or dissolved As(III) and As (V),

141

respectively. The H3PO4 solution was used to minimize the oxidation and

142

precipitation of As in iron rich samples.38 All these extraction and treatment

143

procedures were performed inside the anoxic glovebox (AW 400SG, Electrotek,

7



144

United Kingdom). Moreover, the effect of S. oneidensis MR-1 and AC on redox

145

transformation of As was also evaluated by batch incubation experiment (see Text S1,

146

Supporting Information (SI)).

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2.3. X-ray absorption (XAS) spectroscopy analysis

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The solid phase products cultured for 56 days were collected, washed, and

149

freeze-dried. The samples were then ground to fine powder, mounted in thin plastic

150

sample holders, and covered with Kapton tape in the anoxic glovebox. The siderite,

151

vivianite, and FH that sorbs or co-precipitates with As were synthesized and used as

152

the standard references for XAS analyses (Text S2, SI). The X-ray absorption near

153

edge structure (XANES) and extended X-ray absorption fine structure (EXAFS)

154

spectroscopy data at the As K-edge (11867 eV) for the bio-reduced solids and the As

155

standards were collected in fluorescence detection mode using a Lytle detector at

156

beam-line BL14W at the Shanghai Synchrotron Radiation Facility (SSRF). The X-ray

157

energy was calibrated with Au LIII-edge (11919 eV). The data were analyzed by

158

using the IFEFFIT program.39, 40

159

2.4. Analytical methods

160

The concentrations of Fe(II) and total Fe (pre-reduced by hydroxylamine

161

hydrochloride) were determined spectrophotometrically by the Ferrozine assay. The

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Fe(II) production follows an approximate linear rate during the early stage of the

163

reduction.41 The initial reduction rate was calculated by linear regression of the

164

steepest slopes of the FHs reduction curve at the initial stage.42 The concentrations of

8


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As(III) and total As(V) were measured by hydride generation atomic fluorescence

166

spectrometry (AFS-230E, Haiguang, China).43 X-ray diffraction (XRD, Ultima IV,

167

Rigaku, Japan) was employed to characterize mineralogical compositions of the solid

168

phase products at different time intervals (7, 20, and 56 days). Moreover, the solid

169

phase products collected at 7 and 56 days were fixed in formaldehyde and

170

glutaraldehyde and dehydrated using ethanol and removed water for scanning electron

171

microscope (SEM)-energy dispersive X-ray spectrometry (SEM-EDX) analyses

172

(S-4800, Hitachi, Japan).23

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3. Results and Discussion

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3.1. Activated carbon facilitated microbial reduction of As(III)-FH, As(V)-FH, and

175

FH minerals

176

The effect of AC on microbial reduction of Fe(III) in As(III)-FH, As(V)-FH, and

177

FH was first evaluated (Figure 1 and Figure S1, SI). The inoculation of S. oneidensis

178

MR-1 into the reaction medium at 0 day led to a continuous increase in ratio of

179

Fe(II)/Fetotal over time. Irrespective of the Fe(III)-(oxyhydr)oxide minerals (i.e.,

180

As(III)-FH, As(V)-FH, and FH) used, a similar trend of Fe(III) reduction was

181

observed, indicating that the presence of As(III) and As(V) had a negligible impact on

182

the rate and extent of Fe(III) reduction. Compared to the treatments in the absence of

183

AC, the presence of AC-W, AC-W-N2, and AC-W-N4 markedly promoted the

184

reduction of Fe(III) in As(III)-FH, As(V)-FH, and FH minerals. The initial rate of

185

Fe(III) reduction ranged between 0.38 and 1.73 mM day-1, which is comparable to 9



186

that of microbial reduction for other As-bearing FHs (in the range of 0.8 to 1.78 mM

187

day-1) reported previously.37 In addition to the reduction rate, the extent of FHs

188

reduction was greater in the presence vs. absence of AC. Specifically, the reduction

189

rates and extents were 0.38 and 0.39 mM day-1 and 70.5% and 77.0%, for As(III)-FH

190

and As(V)-FH, respectively, in the absence of AC. In comparison, the rate and extent

191

were up to 1.35 and 1.37 mM day-1 and 85.0% and 85.3%, respectively, in the

192

presence of AC-W (Figure S2, SI). The rate and extent were further elevated to

193

1.60-1.73 mM day-1 and 88.0-97.3% for the treatments that include AC-W-N2 and

194

AC-W-N4. The higher FHs reduction rate and extent in the presence of AC-W-N2 and

195

AC-W-N4 compared to those of AC-W may due to the higher content of quinone

196

groups in the AC, which has been discussed in detail in our recent study.23 Moreover,

197

the Fe(II)/Fetotal ratio varied insignificantly during the entire incubation period in the

198

abiotic control experiments (Figure 1C). These results are consistent with our recent

199

findings that the redox-active oxygen-containing functional groups in AC facilitate

200

microbial reduction of FH.23 The ACs serving as electron shuttles promote electron

201

transfer from microbial cells to FHs.23, 42

202

The promoted microbial reduction of As(III)-FH and As(V)-FH by ACs also

203

yielded the release of Fe2+ into the solution (Figure S3, SI). The concentration of Fe2+

204

increased slowly and then reached a maximum concentration of 1.22 and 0.51 mM on

205

day 56 for As(III)-FH and As(V)-FH, respectively, without the addition of ACs. In

206

contrast, for the treatments in the presence of AC-W, AC-W-N2, and AC-W-N4, the

10


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207

concentration of Fe2+ in the solution increased to 2.41-2.78 mM on day 9.5. Recent

208

findings suggest that the addition of biochar promotes the release of Fe2+ in soil and

209

sediment.28, 44 However, the concentration of Fe2+ obtained here was as low as 0.42

210

mM over the prolonged incubation time (56 days). This is likely due to the potential

211

formation of secondary mineral precipitations composed of Fe2+ and anion in the

212

solution.45 For the treatments without inoculation of S. oneidensis MR-1, the

213

concentration of Fe2+ in the solution was undetected (Figure S3C, SI). These results

214

collectively suggest that the accelerated microbial reduction of As(III)-FH and

215

As(V)-FH in the presence of ACs may promote the precipitation of secondary

216

minerals.

217

3.2. Aqueous chemistry of As during AC mediated microbial reduction of As(III)-FH

218

and As(V)-FH minerals

219

The reduction and concomitant dissolution of As(III)-FH and As(V)-FH may

220

induce the release and transformation of As(III) and As(V). Moreover, the capacity for

221

As sorption by AC is limited probably because of its surface negative charge property

222

at circumneutral pH conditions.46 Therefore, the effects of AC mediated microbial

223

reduction of As(III)-FH and As(V)-FH on As release were examined. As shown in

224

Figure 2A, the As in As(III)-FH was slowly released into the solution without AC. But

225

the addition of AC-W, AC-W-N2, and AC-W-N4 led to a fast release of As, and the

226

As concentration in the solution reached a plateau of 8.85-9.52 mg L-1 on around 9.5

227

days and then changed insignificantly during the later phases of the incubation

11



228

experiments. The As(III) accounted for the 100% of total As in the solution during the

229

whole incubation period when As(III)-FH was the starting mineral. Interestingly,

230

when As(V)-FH was the starting mineral, the As was first released to the solution,

231

then slowly removed from the solution without AC (Figure 2B). However, the

232

addition of AC-W, AC-W-N2, and AC-W-N4 led to the fast removal of the released

233

As. Moreover, the concentration of As(III) in the solution was lower than 0.11 mg L-1

234

for all the treatments during the entire incubation period when As(V)-FH was the

235

starting mineral. This may due to the fact that S. oneidensis MR-1 did not reduce

236

As(V).37

237

The effect of S. oneidensis MR-1 and AC on the redox transformation of

238

dissolved As(III) and As(V) was evaluated in this study. Both the As(V) reduction and

239

As(III) oxidation did not occur in the presence or absence of AC (Figure S4, SI). For

240

the treatments without inoculation of microbial cell, 0.56-0.89 mg L-1 of As(III) and

241

1.24-2.22 mg L-1 of As(V) were presented in the solution, and the As(III) and As(V)

242

concentration fluctuated within the ranges during the incubation period, when

243

As(III)-FH and As(V)-FH were the starting minerals, respectively (Figure S5, SI). The

244

addition of FHs was 10 h earlier than the initiation of batch incubation by the addition

245

of ACs. The As in FHs was exchanged by the co-existed anions in the medium once

246

the FH were added and led to the concentration of dissolved As was not increased in

247

Figure S5. The presence of ACs in these treatments did not impact the concentration

248

of As(III) or As(V) released in the solution (Figure S5, SI). Moreover, the dissolved

12


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249

total As concentration was not decreased with time in the presence of AC (Figure S4,

250

SI). These observations are due primarily to the low As sorption capacity by AC.46

251

The medium contained 4 mM of phosphorus, but dissolved Fe was undetectable in the

252

solution. The high ratio of dissolved phosphorus/Fe may result in the disassociation of

253

As(V) from FH.47 The release of As without inoculation of bacterial cell reflects the

254

competition between phosphorus and As(V) oxyanions for the sorption sites on FH.5

255

The reduction and concomitant dissolution of As(III)-FH led to the release of As(III),

256

whereas they caused slow release and then removal of As(V) for As(V)-FH. AC

257

promoted the release of As(III) but inhibited the release of As(V) instead. These

258

results signify that the bio-reduced solid was probably not capable of sorbing As(III),

259

but was likely to immobilize As(V). Hence, the mineralogical composition of the

260

bio-reduced solid and the content and speciation of As in the solid were characterized.

261

3.3. Secondary minerals formed during AC mediated microbial reduction of

262

As(III)-FH, As(V)-FH, and FH minerals

263

Magnetite, green rust, goethite, lepidocrocite, siderite, and vivianite are the

264

dominant

secondary

minerals

precipitated

during

265

Fe(III)-(oxyhydr)oxides.6, 48, 49 The composition of precipitated secondary minerals

266

depends on rate of Fe2+ production and co-existed ligand.50,

267

mineralogical compositions of the solid phase products on 7, 20, and 56 days during

268

microbial reduction of As(III)-FH, As(V)-FH, and FH (Figure 3, and Figure S6, SI)

269

were examined. The nature of the formed secondary minerals at different time

13


microbial

reduction

51

of

Hence, the


270

intervals was independent of the type of starting minerals, i.e., As(III)-FH, As(V)-FH,

271

and FH. Vivianite and siderite were the final secondary minerals precipitated in these

272

processes. For the treatments without the presence of AC, no secondary mineral was

273

found on 7 days, but vivianite started to precipitate on 20 days, and both vivianite and

274

siderite were formed at the end of the incubation (56 days). However, the formation

275

time of secondary minerals was shortened with the addition of AC-W-N4. Clear XRD

276

characteristic spectra of vivianite (PDF #83-2453) were observed on 7 days. Both

277

vivianite and siderite were formed on 20 days and the intensity of XRD spectra

278

increased gradually until 56 days, indicative of increased mass of these minerals. The

279

promoted Fe(III) reduction and the higher concentration of dissolved Fe2+ in the

280

presence of ACs compared to those in biotic control experiments led to the faster

281

precipitation of vivianite and siderite in sequence. In contrast, no secondary mineral

282

was detected in the abiotic control experiments (Figure 3C). The medium components

283

were designed to mimic the geochemical compositions of subsurface environments 37,

284

52

285

carbonate (30 mM). The formation of secondary minerals was consistent with their

286

solubility behaviors. The log Ksp of vivianite and siderite are -36 and -10.9,

287

respectively.53 Hence, the formation of vivianite and siderite was thermodynamically

288

favored. The presence of chloride, sulfate, and carbonate impedes the precipitation of

289

lepidocrocite and goethite,51 while the fast reduction rate of Fe(III) and the presence

290

of phosphorus may be the reason for the fact that no magnetite or green rust was

that include phosphorus (4.4 mM), chloride (7.0 mM), sulfate (2.0 mM), and

14


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291

formed.50 Vivianite was formed prior to siderite both in the presence and absence of

292

AC-W-N4. This is consistent with the thermodynamic calculations performed by

293

Zachara et al.41

294

To further verify the mineralogical characteristics of the formed precipitates, the

295

morphology of the bio-reduced solids on 7 and 56 days was examined using SEM

296

(Figure 4). Only amorphous solid occurred on 7 days of treatments without AC

297

(Figures 4A and E), but flake-like minerals were observed for the treatments in the

298

presence of AC-W-N4 when As(III)-FH and As(V)-FH were the starting minerals

299

(Figures 4B and F). Both flake-like and cube-shaped minerals were observed for all

300

the treatments on 56 days (Figures 4C, D, G, and H). Most notably, the types of

301

secondary minerals identified based on the morphological observations using SEM on

302

7 and 56 days were identical to those of mineralogical results obtained from XRD

303

analyses (Figure 3). These results substantiate that the flake-like mineral is vivianite

304

and the cubic-shaped mineral is siderite, which are the characteristic features of these

305

minerals reported elsewhere.23,

306

formation of flake-like vivianite and cube-shaped siderite in sequence, and this may

307

impact the fate of co-existed As.

308

3.4. Solid phase As chemistry during AC mediated microbial reduction of As(III)-FH

309

and As(V)-FH minerals

37

Our results indicate that AC accelerates the

310

The As content in the solid phase products was first characterized after

311

dissolving the solids in HCl (Table S1, SI). For the starting As(III)-FH and As(V)-FH

15



312

minerals, the As content was 7.99 and 8.66 mg g-1, respectively. In comparison, the As

313

content in the treatments in the presence of AC-W-N4 and absence of bacteria after 56

314

days of incubation was 3.00 and 3.13 mg g-1, respectively. These results substantiate

315

high concentration of As(III) and As(V) immobilized by As(III)-FH and As(V)-FH

316

minerals, consistent with previously reported findings.5 After microbial reduction of

317

As(III)-FH for 56 days in the presence and absence of AC-W-N4, the content of As on

318

the solid phase products was as low as 0.30 and 0.24 mg g-1, but was high (3.62 and

319

5.31 mg g-1) for the reduction of As(V)-FH (Table S1, SI).

320

The distribution of As in the secondary mineral precipitates (described above)

321

was further unraveled by SEM-EDX mapping. When As(III)-FH was the starting

322

mineral, no obvious accumulation of As occurred onto vivianite (blue arrow) and

323

siderite (red arrow) both in the presence and absence of AC-W-N4 (Figures 5A-H). In

324

contrast, when As(V)-FH was the starting mineral, significant accumulation of As

325

occurred onto vivianite (blue arrow), but no obvious accumulation of As was

326

observed onto siderite (red arrow) both in the presence and absence of AC-W-N4

327

(Figures 5I-P). The presence of AC-W-N4 did not significantly affect the distribution

328

of As, compared with that in the absence of AC. The results of SEM-EDX spectra for

329

the individual secondary minerals combined with the entire field of view also validate

330

the selective distribution of As onto the solid phase products (Figure S7, SI). When

331

As(III)-FH was the starting mineral in the presence of AC-W-N4, no obvious

332

accumulation of As was found onto siderite (Figures S7A1-A3, SI) or vivianite

16


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333

(Figures S7B1-B3, SI), as evidenced by the absence of As peaks in the corresponding

334

spectra. Intriguingly, when As(V)-FH was the starting mineral in the presence of

335

AC-W-N4, the elemental distribution and the corresponding spectrum analyses of

336

siderite show no obvious peaks for As (Figures S7C1-C3, SI), but significant

337

accumulation of As and an obvious As peak are shown due to the coupling of As with

338

vivianite (Figures S7D1-D3, SI). These results together clearly indicate that As(III)

339

was poorly bond to biogenic siderite and vivianite, whereas As(V) was probably

340

strongly bond to biogenic vivianite but poorly bond to biogenic siderite.

341

To verify this assumption, the vivianite and siderite were chemically synthesized

342

in-house to investigate their sorption/co-precipitation capacity for As (Text S2, SI).

343

The chemically synthesized vivianite is able to sorb and co-precipitate with As(V),

344

but not with As(III) (Table S1, SI). This result matches with the SEM-EDX mapping

345

results. The chemically synthesized siderite sorbs and co-precipitates with As(V) and

346

As(III) (Table S1, SI), which is consistent with the results reported in the literature.8

347

However, this result dis-match with the SEM-EDX mapping results. As

348

aforementioned, we can conclude that biogenic siderite is unable to immobilize

349

As(III), but we are not sure for that of As(V). Therefore, the redox state and binding

350

environment of As in the bio-reduced solids when As(V)-FH was the starting mineral

351

were further determined by using XAS. FH, siderite, and vivianite are the possible

352

minerals in the bio-reduced solids. The biogenic vivianite and siderite are possibly

353

able to immobilize As(V), while they are unable to immobilize As(III). FH is capable

17



354

of sorbing/co-precipitating with both As(V) and As(III). As shown in Figure S8, the

355

XANES spectra of siderite and FH that sorbs and co-precipitates with As(V) were

356

almost the same. Hence, the siderite, vivianite, and FH that interacts with As(V), and

357

the FH that sorbs with As(III) were chosen as the model compounds for the linear

358

combination fitting (Figure S9, SI).

359

The original As(V)-FH and the As(V)-FH cultured for 56 days in the presence of

360

AC-W-N4 but without adding microbe show the same XANES spectra (Figure S8, SI).

361

This result indicates that the binding environment of As was not changed in the

362

absence of microbe. Linear combination fitting of As K-edge XANES spectra was

363

analyzed for the bio-reduced solid (Figure 6). As(V) was mainly sorbed to vivianite,

364

while not significantly sorbed to siderite and FH. In combination with the SEM-EDX

365

mapping analyses, all these results suggest that the As(V) was sorbed to biogenic

366

vivianite, rather than the biogenic siderite. Moreover, 18% and 37% of the As(V) in

367

the original As(V)-FH was transformed to As(III) in the bio-reduced solid in the

368

presence and absence of AC-W-N4, respectively. However, S. oneidensis MR-1 was

369

unable to reduce As(V) both in the presence and absence of AC (Figure S4, SI), and

370

As(V) could not be reduced when it is sorbed onto Fe-(oxyhydr)oxides without the

371

presence of light or O2.5, 6, 8 Consequently, the reduction of As(V) may due to the

372

photo-reduction of solid phase products during XAS scan.9

373

The As in some of the solid phase products was slowly photo-oxidized or

374

photo-reduced during the XAS scan (data not shown), as have been reported

18


Page 18 of 39

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375

previously.9, 54 Moreover, the low concentration of As and the high concentration of

376

Fe in the solid phase products result in a poor signal-to-noise spectrum, which is

377

especially obvious at high k area. These reasons together lead to the low quality of

378

XAS data. Hence, the shell-by-shell analyses of the EXAFS spectra were not

379

performed and further discussed.

380

Biogenic or natural vivianite was capable of immobilizing As(V),9, 48 but not

381

As(III).55 This is consistent with the result obtained in this study. Jonson and Sherman

382

found that chemically synthesized siderite tends to form inner-sphere surface complex

383

with As(V) but only forms weak outer-sphere complex with As(III).8 However, no

384

As(V) was sorbed onto the biogenic siderite. Both the biogenic and chemically

385

synthetic vivianite are flake-like and well crystallized (Figure 4 and Figures S10B and

386

S11C). Biogenic siderite was cube-shaped and well crystallized (Figure 4), whereas

387

chemically synthesized siderite was sphere-shaped with a lower degree of crystallinity

388

(Figures S10 A and S11 A and B, SI). Hence, the difference of As(V) immobilization

389

capacity between biogenic and chemically synthesized siderite may due to the

390

difference in their morphology and crystallinity properties for the experimental

391

conditions examined in this study.5 In conclusion, for the biogenic secondary minerals

392

of vivianite and siderite, only vivianite sorbs/co-precipitates As(V).

393

3.5. Environmental implications

394

Pyrogenic carbon is both a promising agent for environmental remediation and a

395

prospective soil conditioner for multiple agronomic applications. Recent research has

19



396

elucidated its redox properties 21, 22 and corresponding environmental impact.23 In this

397

study, AC was found to facilitate microbial reduction of As-bearing FH. On one hand,

398

the presence of AC enhanced the rate of immobilizing As(V) in precipitated vivianite

399

in the bio-reduced solid. Vivianite often occurs in waterlogged soils and aquatic

400

sediments such as paddy field soils,56 sewage treatment plants,57 lake sediments,53 and

401

coastal surface sediments.58 Moreover, As(V) also occurs in reducing paddy soils due

402

to the contribution of anaerobic As(III) oxidation bacteria.59 Hence, further study

403

should focus on elucidation of the co-existence of As(V) and vivianite in those

404

reducing environment, particularly Fe plaque on rice roots. On the other hand, the

405

presence of AC may pose potential environmental risk due to the promotion of As(III)

406

release. This means that the As removal technology by adsorption of As onto

407

Fe-(oxyhydr)oxides incorporated AC

408

to the facilitated microbial reduction of Fe-(oxyhydr)oxides by AC once the

409

Fe(III)-reducing bacteria are colonized on the adsorbent. Except for AC, the effect of

410

other types of pyrogenic carbon, i.e. soot, char, black carbon, and biochar, on the fate

411

of Fe and As in subsurface environments has not been well-studied. In addition,

412

strategies for the modification of pyrogenic carbon should be explored to alleviate its

413

potential environmental risks, which may help improve the environmental and

414

agronomic application of pyrogenic carbon.

415

4. Conclusions

34

may cause secondary environmental risk due

20


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416

Herein, the effect of AC on fate and transformation of Fe and As in As-bearing

417

FH was studied. The presence of AC-W promotes the reduction of As(III)-FH,

418

As(V)-FH, and FH. Moreover, the HNO3-oxidized AC further enhances the rate of

419

FHs reduction. The facilitated microbial reduction of As(III)-FH by AC promotes the

420

release of As(III) into solution, but favors the removal of As(V) from solution for the

421

reduction As(V)-FH. Flake-like vivianite and cubic-shaped siderite were precipitated

422

in sequence, but the presence of AC promotes the precipitation of these secondary

423

minerals compared to the treatments without AC. The SEM-EDX mapping and XAS

424

analyses indicate that when As(III)-FH was the starting mineral, the precipitated

425

siderite and vivianite have poor capacity for As capture; but when As(V)-FH was the

426

starting mineral, As(V) was selectively accumulated onto vivianite rather than by

427

siderite. Our findings advance the current knowledge about the role of AC on the

428

redox and immobilization of Fe and As in sub-oxic and anoxic environments and thus

429

their environmental fate, in which pyrogenic carbons are used for agronomic and

430

environmental applications.

21



431

ASSOCIATED CONTENT

432

Supporting information

433

The contents of As in the solids, the reduction of ferrihydrite, the initial reduction rate

434

of ferrihydrite, the Fe2+ released into the solution, the effect of microbe and AC on As

435

transformation, the release of As in the absence of microbe, the XRD of the

436

bio-reduced solid, the SEM-EDX mapping, the XANES spectra, the XRD and SEM

437

of synthetic minerals.

438

AUTHOR INFORMATION

439

Corresponding author

440

*Phone: +86 25 86881180; fax: +86 25 86881180; e-mail: [email protected] (Y.J.

441

Wang), [email protected] (D.M. Zhou).

442

Notes

443

The authors declare no competing financial interest.

444

ACKNOWLEDGMENTS

445

The authors gratefully thank the support by the National Natural Science Foundation

446

of China (21537002, 41422105, and 41671478). The authors also acknowledge the

447

support of beamline 14W of Shanghai Synchrotron Radiation Facility, China.

448

22


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Figure 1 Shewanella oneidensis MR-1 (A, B) and abiotic (C) reduction of As(III)-bearing ferrihydrite and As(V)-bearing ferrihydrite in the presence and absence of AC-W, AC-W-N2, and AC-W-N4, respectively. Error bars represent the standard deviations from triplicate experiments.

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Figure 2 Aqueous total As concentration and percentage of As(III)/total As during activated carbons mediated microbial reduction of As(III)-bearing ferrihydrite (A). Aqueous total As and As(III) concentration during activated carbons mediated microbial reduction of As(V)-bearing ferrihydrite (B).

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Figure 3 X-ray diffractograms of the solid phases after microbial reduction of As(III)-bearing ferrihydrite (A) and As(V)-bearing ferrihydrite (B) for 7, 20, and 56 days in the presence and absence of AC-W-N4. (C) shows the X-ray diffractograms of the solid phases cultured for 56 days in the absence of microbe.

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ACS Earth and Space Chemistry 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46

Figure 4 Representative scanning electron microscope images of the solid phase minerals after microbial reduction of As(III)-bearing ferrihydrite (A-D) and As(V)-bearing ferrihydrite (E-H) for 7 (A, B, E, F) and 56 days (C, D, G, H) in the presence (B, D, F, H) and absence (A, C, E, G) of AC-W-N4.

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Figure 5 Representative scanning electron microscope images of the secondary minerals after microbial reduction of As(III)-bearing ferrihydrite (A, E) and As(V)-bearing ferrihydrite (I, M) for 56 days in the presence (E, M) and absence (A, I) of AC-W-N4, and their corresponding element distribution. Arsenic is shown in red (B, F, J, N), iron in blue (C, G, K, O), and phosphorus in green (D, H, L, P). Red and blue arrows indicate biogenic siderite and vivianite, respectively.

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Figure 6 As K-edge XANES (A), As k3-weighted EXAFS (B), and linear combination fitting result (C) of bio-reduced solid on day 56 in the absence (upper) and presence (lower) of AC-W-N4 when As(V)-bearing ferrihydrite was the starting mineral. As(V) sorbed vivianite, As(III) sorbed ferrihydrite, As(V) sorbed ferrihydrite, and As(V) sorbed siderite were model compounds spectra.

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Graphical abstract

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Fate of As(III) and As(V) during Microbial Reduction of Arsenic-Bearing

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