Redox-Active Oxygen-Containing Functional Groups in Activated

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Redox Active Oxygen-Containing Functional Groups in Activated Carbon Facilitate Microbial Reduction of Ferrihydrite Song Wu, Guodong Fang, Yu-Jun Wang, Yue Zheng, Chao Wang, Feng Zhao, Deb P. Jaisi, and Dongmei Zhou Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b01854 • Publication Date (Web): 07 Aug 2017 Downloaded from http://pubs.acs.org on August 7, 2017

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Environmental Science & Technology

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Redox Active Oxygen-Containing Functional Groups in Activated

2

Carbon Facilitate Microbial Reduction of Ferrihydrite

3 ∥

∥

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Song Wu†, , Guodong Fang†, Yujun Wang†, Yue Zheng§, , Chao Wang†, Feng

5

Zhao§, Deb P. Jaisi‡, 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

Key Laboratory of Urban Pollutant Conversion, Institute of Urban Environment,

10

Chinese Academy of Sciences, Xiamen 361021, P.R. China

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‡

12

∥

Department of Plant and Soil Sciences, University of Delaware, Newark 19716, USA University of Chinese Academy of Sciences, Beijing 100049, P.R. China

13 14

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

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[email protected].

ACS Paragon Plus Environment


16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39

Abstract Carbonaceous materials are commonly used in agronomic and environmental applications primarily as geosorbents but their redox properties that may affect biogeochemical reactions are rarely documented. Herein, the role of activated carbon (AC) mediating microbial reduction of ferrihydrite is studied. Our batch experiment results show that ACs facilitated the reduction of ferrihydrite by Shewanella oneidensis MR-1, but the pretreatment of ACs with HNO3 further increased the rate of reduction. The redox active oxygen-containing functional groups in ACs were found to be responsible for the enhancement of the microbial reduction of ferrihydrite. This conclusion was supported by the electrochemical evidence that showed the electron exchange capacity (EEC) of ACs was facilitated due to the presence of quinone/hydroquinone groups and strongly positive correlation with the contents of C=O groups. Moreover, the co-precipitation of vivianite and siderite was found in the products in the presence of ACs but siderite only was present in the absence of ACs. The proper identification of potential functional groups in ACs mediating electron transfer during microbial reduction of ferrihydrite provides insights into the mechanism of reaction and potential roles carbonaceous materials may play on biogeochemical redox processes and consequently the fate of contaminants in the environment.

Keywords: Activated carbon, Fe reduction, electron transfer mediator, electron exchange capacity, biogeochemical redox process

TOC Art

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41

Introduction

42

Biogeochemical redox reactions play an important role in the formation and

43

dissolution of minerals and consequently control the retention and release of trace

44

elements associated with these minerals 1. In the biogeochemical redox reaction, the

45

electron

46

extracellularly

47

cytochromes in bacterial cells to solid minerals in contact with cells, ii) endogenous

48

and exogenous redox active electron shuttles that facilitate electron transfer between

49

cells and solid minerals, and iii) conduction along the redox active pili to the solid

50

minerals

51

electron transfer pathway dominates that from the direct contact with cells 5-8.

transfer 2

between

microorganisms

and

minerals

generally

occurs

as i) direct transfer of electrons from cell-surface localized c-type

3, 4

. For some genus such as Shewanella, the electron shuttle mediated

52

Black carbon is the carbonaceous residue produced mainly by the incomplete

53

combustion of fossil fuel and biomass 9. Both the naturally occurring black carbon

54

and the engineered analogs to black carbon are carbonaceous material, including

55

biochar, soot, activated carbon (AC), graphite, carbon nanotubes, and graphene oxide

56

10-12

57

groups, the carbonaceous material offers a great potential for carbon sequestration,

58

fertility enhancement, and soil amelioration 13-15. Humic substances and black carbon

59

constitute a significant fraction of natural organic matter present in soil and sediments

60

16, 17

61

shuttles, and thus facilitate redox transformation 18-20. Compared to humic substances

62

that contain multiple redox active surface functional groups, carbonaceous materials

63

also contain few functional groups and are electrically conductive, which make them

64

comparable to humic substances with particular differences 21, 22. Thus the capacity of

. Due to highly porous structure, high alkalinity, and abundant surface functional

. Both particulate and dissolved forms of humic substances are known as electron



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65

carbonaceous materials on redox transformation is expected to be different from that

66

of humic substances.

67

Carbonaceous materials have been widely reported to catalyze the chemical

68

transformation of organic pollutants. For example, persistent free radicals in biochar,

69

electrical conductivity (EC) of black carbon, and sulfur-based intermediates on black

70

carbon are found to facilitate the electron transfer and related chemical reactions 23-26.

71

Based on these findings, the carbonaceous material could be envisioned to play an

72

important role on mediating biogeochemical redox reactions in soils and sediments. In

73

fact, many microbiological reactions including syntrophic methane production,

74

degradation of organic contaminants, and reduction of Fe(III) in minerals are found to

75

be accelerated in the presence of carbonaceous material

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transformation mediated by carbonaceous material has been fairly studied, the

77

mechanisms of carbonaceous material mediated microbial processes have rarely been

78

elucidated

79

have reported the roles of biochar in mediating the microbial reduction of iron oxide

80

22, 28

81

were not included. This brings a void in scientific information on the potential

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unintended roles that carbonaceous materials can play once they are applied in soils

83

for agronomic and environmental causes.

22, 27-32

. While the chemical

22, 28

. In the microbe-biochar-iron oxide system, two recent publications

, but the mechanistic details on the reaction and roles of surface functional groups

84

With biochar taking a new scientific interest, there has been a recent spike in

85

research efforts both in characterization as well as assessing the impacts of black

86

carbon on the environment. For example, the redox property and electron transfer

87

kinetics of carbonaceous materials are thoroughly characterized recently

88

findings provided a foundation to study the black carbon mediated microbiological

89

redox reaction and related precipitation/dissolution of minerals. Therefore, the overall


21, 33

. These

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objective of this research was to identify the composition of electron shuttling

91

compounds in ACs and to elucidate the mechanisms of electron transfer by these

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shuttles during microbial reduction of Fe(III) oxides. The specific objectives were to: i)

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determine the effect of AC on microbial reduction of ferrihydrite, ii) identify the key

94

characteristics of AC that are responsible for enhancing microbial reduction of

95

ferrihydrite. The ACs containing abundant surface functional groups were also treated

96

with HNO3 to enhance the content of oxygen-containing functional groups and several

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spectroscopic and electrochemical methods were employed to achieve these

98

objectives.

99 100

MATERIALS AND METHODS

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Preparation of HNO3 oxidized and hydroquinone modified activated carbon

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Three types of activated carbon stocks were purchased from commercial sources

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and are generically named as AC-X from XFNANO Materials Tech, China (catalog

104

no. XF026), AC-W from Sinopharm, China, and AC-S from Sigma-Aldrich, USA

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(catalog no. 242276). To change the surface functional groups, the ACs were reacted

106

with 66% HNO3 at 90 °C, and stirring for 2 or 4 h following a method described

107

previously 34. After the modification, a total of 9 different AC samples were generated.

108

These modified ACs are denoted as follows: AC-X (as received), AC-X-N2 (AC-X

109

modified for 2 h in HNO3), AC-X-N4 (AC-X modified for 4 h in HNO3). Similar

110

analogous nomenclature is used for other modified activated carbons: AC-W,

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AC-W-N2, AC-W-N4, AC-S, AC-S-N2, and AC-S-N4. The particle size distribution

112

of selected AC samples (AC-W, AC-W-N2, and AC-W-N4) were analyzed by using

113

laser diffraction method (Beckman Coulter, LS 13320, USA) 21. As shown in Fig. S1,

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more than 90% of the AC particles have a diameter less than 10 µm. The fitting result



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of C 1s photoelectron spectrum of the 9 AC samples was showed in Tab. S1 and

116

reported in our previous publication 34.

117

We modified ACs to verify the types of redox active functional groups present.

118

The detailed modification procedure is included in the Supporting Information (SI,

119

Text S1). Moreover, ferrihydrite, AC suspension, and AC leachate were prepared for

120

redox experiments (SI, Text S2). The details of microbial culture, and quantification

121

of cell numbers, and the electrochemical characterization of ACs are described in the

122

Supporting Information (SI, Texts S3 and S4).

123

Fe(III) reduction in ferrihydrite

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Batch experiments on the Fe(III) reduction in ferrihydrite were conducted in a 35

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100 mL serum bottle with 40 mL anoxic mineral medium (pH 7.0)

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mM ferrihydrite as an electron acceptor and 30 mM sodium lactate as an electron

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donor and 30 mM bicarbonate buffer. A 2 mL of the 50 g L-1 AC, AC leachate, or

128

anoxic water was added separately to the reaction medium. Then the medium was

129

amended with 1 mL of S. oneidensis MR-1 cells (~2 × 1011 cells mL-1) or 1 mL of

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anoxic water (for abiotic control experiment). A ~0.1 mL of the mineral-cell

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suspension was withdrawn at selected time intervals, and 1 mL of 1 M HCl was

132

spiked and reacted for 2 h to extract total Fe(III) and Fe(II) in the solid phase 28. The

133

soluble electron shuttles, flavin adenine dinucleotide (FAD), flavin mononucleotide

134

(FMN), and riboflavin (RF) were quantified using HPLC (SI, Text S5). The

135

morphology of the solid phase samples at 72 h and 288 h was analyzed under a

136

scanning electron microscope (S-4800, Hitachi, Japan, SI, Text S6). Other analytical

137

methods are described in the Supporting Information (SI, Text S7).

138 139


containing 30

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RESULTS AND DISCUSSION

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Enhancement of Fe(III) reduction in ferrihydrite in the presence of AC

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The AC mediated microbial reduction of Fe(III) in ferrihydrite was initiated by

143

inoculating S. oneidensis MR-1 cell at t = 16.5 h (shown by the arrows in Fig 1) after

144

16.5 h of equilibration of ACs-media suspension. Soon after the cells were added, the

145

Fe(II) content increased markedly but it remained almost the same in the experiments

146

without microbial cells. For example, at the end of batch culture at 243 h, the extent of

147

Fe(III) reduction achieved was 74.1%, 78.9%, and 73.7% for AC-X, AC-W, and

148

AC-S treatments, respectively, while the extent was limited to 38.6% for the biotic

149

control. Compared to the pristine ACs, the HNO3 treated ACs enhanced both the rate

150

and extent of Fe(III) reduction, with almost 100% Fe(III) reduced to Fe(II). The

151

maximum reduction rate of ferrihydrite ranged from 0.127 to 0.434 mM h-1 in the

152

presence of ACs, which is significantly higher than the biotic control (0.047 mM h-1,

153

Fig. S2, Table S1). These rates are comparable to past publications on microbial

154

reduction of iron oxide mediated by carbonaceous materials (reduction rates on the

155

ranges of 0.019 – 0.047 and 0.12 ~ 1.49 mM h-1, respectively 10, 28).

156

Biochar leachate has been reported to enhance the Fe(III) reduction in the

157

presence of microorganisms 22. Therefore, microbial reduction of ferrihydrite was also

158

performed in the presence of AC leachate to testify its role in the reduction. Our

159

results showed that the extent of Fe(III) reduction remained almost the same as that of

160

biotic (in the presence of S. oneidensis MR-1) or abiotic controls (Fig. S3 A-C). It

161

means that the addition of AC leachate enhanced neither the microbial nor the

162

chemical reduction of ferrihydrite. This, however, allowed us to confirm that AC

163

leachates cannot be accounted for enhancing ferrihydrite reduction. Such rather

164

unexpected result was reported in a past study, in which biochar was added to



28

165

stimulate microbial reduction of ferrihydrite

166

pyrolyzed at 250 oC and 500 oC 22, the ACs are often pyrolyzed and then activated and

167

have a low content of total organic carbon. As shown in Table S2, total organic

168

carbon content in the AC leachate was too low (about 1.5 mg L-1 of total organic

169

carbon versus 1080 mg C L-1 of sodium lactate in the culture media) to contribute

170

significantly to supply carbon for the microbial metabolism. However, other processes

171

such as stimulating microbial growth or by mediating the electron transfer from

172

microorganisms to mineral are likely mechanisms that ACs can enhance the microbial

173

reduction of Fe(III) in ferrihydrite. To investigate this further, we tested microbial

174

growth in the presence of AC in the media and the electrochemical property of ACs.

175

The results are discussed below.

. Compared to the biochars that are

176 177 178

Microbial growth during Fe(III) reduction in ferrihydrite The Fe(III) reduction is normally found to stimulate microbial growth depending 7, 36

179

on the composition of incubation media used

180

and rates of reductions with the addition of different ACs (AC-W, AC-W-N2,

181

AC-W-N4, or none), the relative abundance of 16S rRNA gene of S. oneidensis MR-1

182

was found to be fluctuated within a narrow range, between 0.95 and 1 (Fig. S4). Since

183

this fluctuation was within the range of error, the addition of ACs can be confirmed

184

not to stimulate the microbial growth. It further means that any change in reduction

185

among these treatments cannot be ascribed to the changes of microbial growth.

. Compared to the different extents

186

To reconfirm the gene abundance results, live/dead staining was performed as a

187

means to count cells directly. The live-dead count of cells during iron reduction

188

experiments showed a distinct difference between two sets of treatments, with and

189

without ACs (Figs. 2 and S5). For example, after incubation for 32 h, almost all


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bacterial cells were found to be alive (as the emitted fluorescence was green only

191

without any red i.e., dead). However, by 109 h of incubation dead cells dominated in

192

the treatment with ACs, but the extent of the dead cell was found to be relatively low

193

in the biotic control treatment. As shown in Fig. 1, at 124 h (107 h after spiking

194

microbial cell), 55 – 83 % of the ferrihydrite were reduced in the presence of ACs,

195

whereas the reduction was limited to 25% when ACs were not included. As expected,

196

the higher Fe(II) production resulted in the faster dissolution of ferrihydrite and

197

depletion of sodium lactate in the media. These lines of evidence suggest that the

198

presence of ACs accelerated the death of microorganisms compared to that biotic

199

control especially in longer experiments because of the limited supply of ferrihydrite

200

to sustain cell metabolism. Nonetheless, the microbial cells might be metabolically

201

active for redox reaction as in non-growth experiments 7.

202

Several electron shuttling compounds including FAD, FMN, and RF are 37, 38

203

synthesized by S. oneidensis MR-1 to promote extracellular electron transfer

204

Measurements of FAD, FMN, and RF compounds in S. oneidensis MR-1 incubation

205

experiments showed low concentrations of FMN and RF in the biotic control

206

treatment but FAD was hardly detected. None of FAD, FMN, and RF compounds

207

were detected in the treatments ACs (Fig. S6). This intriguing observation could

208

possibly result from the removal of FAD, FMN, and RF compounds due to adsorption

209

onto AC surfaces. The measured electron exchange capacities (EEC) for ACs was

210

3.35 – 16.05 mM e- L-1 (calculated from data presented in Table S1), which was

211

significantly higher than that of FMN and RF compounds (less than 0.1 µM L-1) in the

212

absence of ACs. Hence, the capacity of the adsorbed FMN and RF compounds

213

carrying electrons from cell to ACs and then from ACs to ferrihydrite should be

214

negligible. Based on the EEC values, it is safe to conclude that FAD, FMN, and RF


.


215

compounds have limited contribution to facilitate microbial reduction of ferrihydrite

216

in the presence of ACs because the electron mediating capacity of ACs is high (see

217

below).

218 219

Electrochemical property of the activated carbon

220

During the microbial reduction of ferrihydrite, electrons generated by oxidation

221

of organic carbon substrate (sodium lactate in this study) are eventually transferred to

222

ferrihydrite. This transfer of extracellular electrons could be enhanced by adding

223

electron shuttles 5. Apart from being electrically conductive, ACs possess multiple

224

redox-active surface functional groups. Thus, AC can mediated electron transfer in

225

two ways: i) acting as the electron reservoir that has dual electron donating capacity

226

(EDC) and electron accepting capacity (EAC), and ii) acting as the electron conduit

227

due to the conductive graphitic structure 21, 31.

228

FTIR was suitable to characterize surface functional groups of highly oxidized

229

carbons 39. It was firstly used to qualitatively identify the bands of oxygen-containing

230

functional groups (Fig. S7). These functional groups and corresponding IR bands

231

include -OH at 3435 cm-1, C=O‒C at 1715 cm-1, C=O at 1590 cm-1, and phenolic-OH

232

at 1165 cm-1. The contents of these four types of oxygen-containing functional groups

233

were found to be increased after the HNO3 oxidation of ACs, which are consistent

234

with our past findings 34.

235

For both quinone and carbonyl functional groups, the decomposition temperature

236

analyzed in a temperature-programmed desorption study spectrum and the peak

237

positions in the XPS spectrum were same 39. It may mean that the carbonyl/quinone

238

groups are present together 40 or interchangeable (i.e., two carbonyl groups invert into

239

one quinone group or vice versa)

41, 42

. Since the carbonyl/quinone groups on the


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41, 43, 44

240

carbonaceous materials are known to be redox active

241

analyses were employed to examine the redox property of ACs. Capacitance current

242

was observed in the AC-W samples, in which a pair of redox peaks were clearly

243

present, with the oxidation/reduction potential at approximately 0.1 V/-0.1 V (in the

244

traces of AC-W-N2 and AC-W-N4; Fig. 3A). Redox peaks in AC-S-N2 and AC-S-N4

245

were found to be similar to AC-W-N2 and AC-W-N4 (Fig. S8B). But there were no

246

redox peaks observed in cyclic voltammograms of AC-X-N2 and AC-X-N4 (Fig.

247

S8A). This may be due to the low electrical conductivity of these ACs after HNO3

248

oxidation. On the other hand, HNO3 oxidation has been found to alter the

249

carbon-oxygen functional groups of ACs

250

quantitative XPS analyses verified the increased content of C=O groups after HNO3

251

treatment of ACs (Fig. S7 and Table S1). Hence, the redox peaks in cyclic

252

voltammograms were ascribed to the high content of redox active oxygen-containing

253

groups such as quinone/hydroquinone species in ACs 47.

, cyclic voltammetric

45, 46

. Both the qualitative FTIR spectra and

254

To further verify the presence of quinone/hydroquinone groups in ACs, their

255

content on AC surfaces was altered by chemical bonding and physical adsorption of

256

hydroquinone and by thermo-chemical pyrolysis. When the ACs underwent chemical

257

bonding and physical adsorption with hydroquinone, the oxidation peak at 0.1 V was

258

enhanced in the cyclic voltammograms (Figs. S9 and S10A). However, when the ACs

259

underwent thermo-chemical pyrolysis, the oxidation peak at 0.1 V diminished (Fig.

260

S10B). The intensity of the bands at 1590 and 1165 cm-1 in the FTIR spectra of the

261

chemical bonding and physical adsorption treated ACs were much higher than that of

262

pyrolysis treated ACs (Fig. S11). This was consistent with the cyclic voltammetry

263

results. These results together verified that the treatment of ACs with HNO3 elevated

264

the content of surface quinone/hydroquinone species of ACs.



265

Quinone/ hydroquinone

groups are well-known electron shuttles and

266

significantly enhance both the rate and extent of Fe(III) reduction 7. This is because

267

quinone/ hydroquinone reversibly accept/donate electrons. In the chronoamperometric

268

experiment, the working electrode was able to mimic the redox potential of electron

269

donor/acceptor in the natural environment by poising at a certain potential. Hence,

270

chronoamperometric experiments can provide a reliable measure to quantify the EDC

271

and EAC of ACs

272

oxidation/reduction current (Fig. S12). For the measurement of EAC, the reduction

273

current decreased to a stable background current quickly. However, for the

274

measurement of EDC, the decrease of the oxidation current to a stable background

275

required much more time (Fig. S12). The sluggishness of oxidation current in the

276

EDC measurement might have caused by the slow kinetics of electron transfer from

277

ACs to 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt

278

(ABTS) 21, 48. The electron donating/electron accepting moieties of black carbon were

279

found to be oxidized/reduced in the presence of O2/borohydride, respectively 21. The

280

measured EDC of the ACs varied from 0.19 – 0.80 mM e- (g AC)-1 before HNO3

281

oxidation to around 0.29 – 0.90 mM e- (g AC)-1 after the treatment. However, the

282

EACs of the ACs increased significantly from 0.54 –1.77 mM e- (g AC)-1 before

283

HNO3 treatment to 3.62 ₋ 6.09 mM e- (g AC)-1 after the treatment (Fig. 3B). This

284

means that the HNO3 oxidation mainly elevated the content of electron accepting

285

moieties of ACs. Furthermore, the EECs of the three types of ACs were found to be

286

increased with the HNO3 treatment. These results are consistent with the FTIR and

287

cyclic voltammetry results (Figs. 3A, S7, and S8). The EEC values of AC-X, AC-W,

288

and AC-S (1.34 – 2.27 mM e- (g AC)-1) were comparable to that of biochar (0.14 –

289

2.28 mM e- (g char)-1), whereas the EEC of the HNO3 oxidized ACs (3.91 – 6.42 mM

43

. In fact, the addition of ACs led to an increase of


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e- (g AC)-1) were much higher than that of biochar 21. These results suggest that the

291

treatment with HNO3 would be an effective way to manipulate the redox property of

292

carbonaceous materials.

293

The electrical conductivity (EC) of the three types of ACs (namely AC-W, AC-X,

294

and AC-S) was found to be decreased with the increase in the time of HNO3 treatment

295

(Fig. 3B, Table S1). This result is comparable to that of multi-walled carbon

296

nanotubes and carbon felt that were treated by HNO3

297

materials depends on the charring temperature31, 51. Among three types of ACs tested

298

in this study, AC-S was found to have the highest EC, while AC-X had the lowest EC.

299

Moreover, the EC of AC-X decreased drastically from 0.0179 to 0.0007 S cm-1 after

300

the HNO3 treatment. These results together indicated that HNO3 treatment elevated

301

the content of redox active oxygen-containing functional groups of ACs, which might

302

play a major role in enhancing the microbial reduction of Fe(III) in ferrihydrite.

49, 50

. The EC of carbonaceous

303 304 305

Proposed mechanism of AC facilitating microbial reduction of ferrihydrite Biochar is an efficient redox agent and is capable of donating and accepting 10

306

electrons

307

particularly quinone/hydroquinone groups, of ACs were responsible for the

308

enhancement of microbial reduction of ferrihydrite. The vast span of physicochemical

309

properties of activated carbon materials helps us elucidate key factors that control the

310

electron tranfer capacity of activated carbons.

. The aforementioned results demonstrated that the characteristics,

311

The AC characteristics were individually tested for their relationship with the

312

maximum reduction rate of ferrihydrite (kmax, Figs. 4, S13, and S14). In fact, EEC,

313

content of C-defects, and C=O content were positively correlated with kmax, with

314

correlation coefficients (R2) of 0.612 (p < 0.01), 0.591 (p < 0.01), and 0.521 (p < 0.05),



Page 14 of 34

315

respectively. In contrast, the content of C-OH was negatively correlated with kmax,

316

with R2 of 0.871 (p < 0.001). This was aroused by that both the original C-OH and the

317

newly generated C-OH were tended to be oxidized when the ACs were treated by

318

HNO3. Moreover, the specific surface area, volume of micro-pores, and volume of

319

meso-pores were negatively correlated with kmax (Fig. S14). This result indicated that

320

the content of pores in ACs could inhibit ferrihydrite reduction. The likely reason

321

could be that the redox sites in small pores are less available to cells and ferrihydrite

322

particles. The correlations among EEC and contents of C-defects, C=O, and C-OH

323

with kmax indicated that the contents of C-defects, C=O, and C-OH may be responsible

324

for the measured EEC. Therefore, contents of C-defects, C-OH, and C=O were

325

individually tested for their relationship with EEC (Fig. 5).

326

The increase of the content of redox active oxygen-containing functional groups

327

and the decrease of EC during the pretreatment of ACs with HNO3 provide

328

information useful to discern the contributions of newly formed redox active

329

oxygen-containing functional groups to the enhancement of the microbial reduction of

330

ferrihydrite. It is well known that both the redox active moieties and the EC of biochar

331

contribute to the microbial reduction of organic contamiants

332

between EC and kmax was found in Fig. S13A. Herein the positive correlation between

333

EEC and kmax while the no correlation between EC and kmax suggested that the redox

334

property of ACs rather than the EC itself was responsible for the enhancement of

335

microbial reduction of ferrihydrite. The results showed that C-defects was positively

336

correlated with the kmax but had no correlation with EEC (Figs. S13B and 5A), which

337

deserves further research.

31

. But no correlation

338

The C-OH functional group is redox active and known for electron donating

339

capacity 21, 43, 52. The electron donating C-OH and the electron accepting C=O groups


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340

forms an electrochemical redox couple 43, 52. The oxidation of ACs by HNO3 led to the

341

significant increase of electron accepting C=O group, whereas the electron donating

342

C-OH group remained rather constant (0.19 – 0.80 versus 0.29 – 0.90 mM e- (g AC)-1).

343

Hence, although C-OH group is redox active it was not correlated with EEC (Fig. 5B).

344

To the other hand, positive correlation between the content of C=O and EEC (R2 =

345

0.934, p < 0.0001) implied that the redox active C=O group was a significant

346

contributor for the measured EEC. Together, these results suggested that redox active

347

oxygen-containing functional groups (i.e. quinone/hydroquinone) of activated carbon

348

played a crucial role in facilitating electron transfer during microbial reduction of

349

ferrihydrite.

350 351 352

Effect of ACs on the formation of secondary minerals The reduction of iron-bearing minerals not only affects the dissolution and 3, 53

353

subsequent speciation of Fe, but also promotes the precipitation of new minerals

354

A SEM analysis showed the presence of a flake-like secondary mineral in AC-W-N4

355

after 72 h of incubation (Fig. 6B), whereas the majorly of ferrihydrite reamin largely

356

unchanged without the presence of AC (Fig. 6A). This indicated that the addition of

357

AC-W-N4 likely accelerated the formation of secondary minerals. Bacterial cells were

358

still found to be intact until 72 h incubation. With the prolonged incubation, both

359

cube-shaped and stacks of flaky secondary minerals were formed in the presence of

360

AC-W-N4 (Fig. 6D and inset in Fig. 6D), whereas only cube-shaped secondary

361

mineral was formed in the absence of ACs (Fig. 6C). These findings together provide

362

strong evidence that ACs also stimulated the formation of secondary minerals during

363

microbial reduction of ferrihydrite.


.


364

XRD analysis was performed to further identify the composition of secondary

365

minerals (Fig. S15 - 17). Vivianite was formed in the presence of AC-W-N4, whereas

366

no mineral was detected in the absence of ACs until 72 h of incubation (Fig. S16).

367

However, continued incubation until 288 h showed the formation of siderite in the

368

absence of ACs (Fig. S15 A-C), whereas both vivianite and siderite were formed.

369

Therefore, the cubic and flake-like crystallites in the SEM images are most likely

370

siderite and vivianite, respectively. Precipitation of these two minerals during

371

microbial reduction of Fe(III) in ferrihydrite is reported in previous studies 54, 55.

372

No secondary mineral, however, was formed in the absence of bacteria for the

373

entire length of incubation (Fig. S15 D). When 30 mM of Fe2+ was added to the

374

culture media, both vivianite and siderite were formed in the absence of AC, but no

375

mineral was formed in the presence of AC-W-N4 (Fig. S17). This was verified by the

376

SEM results that both cubic (siderite) and flake-like (vivianite) crystallites were

377

present in the absence of AC-W-N4 (Fig. S18 A), whereas only nano-sized small

378

particles were observed in the presence of AC (Fig. S18 B and C). In conclusion,

379

when bacteria and AC-W-N4 were present, the formation of secondary mineral was

380

promoted, but the only presence of AC-W-N4 inhibited the formation of mineral.

381

Therefore, the effect of AC on the biological and abiotic formation of ferrous minerals

382

needs to be fully studied. The mineralogical and SEM results together provided strong

383

evidence that the addition of ACs during microbial reduction of ferrihydrite

384

accelerated the formation of secondary minerals and the composition of minerals

385

varied with the presence of ACs as well.

386 387

Environmental implications


Page 16 of 34

Page 17 of 34


388

Here we demonstrated that AC enhanced the microbial reduction of ferrihydrite,

389

with the maximum reduction rate of ferrihydrite increased by 1.7 – 8.2 times. The

390

nature of secondary minerals was found to depend primarily on the Fe(III) reduction

391

rate and the content of biogenic Fe(II)

392

ferrihydrite in the presence of ACs altered the type and rate of secondary mineral

393

formation. The dissolution and precipitation of iron-bearing minerals often determine

394

the fate of hazardous metal contaminants 57-60. Moreover, the capacity of iron-bearing

395

minerals sequestrating heavy metals varies both with physical properties and chemical

396

composition 55, 61. For example arsenic (As) selectively to vivianite rather than siderite

397

has been found to bind As with vivianite when both are present as secondary minerals

398

55

399

area, their impact on toxic metal sequestration is disproportionate to other minerals.

400

Therefore, careful analysis is needed to identify the composition of ferrous minerals

401

formed during AC facilitated microbial reduction of ferrihydrite. Furthermore, the

402

elucidation of the speciation and fate of hazardous metal contaminants concomitant

403

with the AC mediated processes is also very urgent.

56

. The promotion of microbial reduction of

. Given that these secondary minerals are nano-sized are often have larger surface

404

Electron transfer in chemical and biological reactions dominates the geochemical

405

and biochemical transformations in the living beings and in natural environment 18, 62,

406

63

407

terrestrial and marine environments

408

electron mediating capacity of various carbonaceous materials helps to assess their

409

roles in biogeochemical redox processes in surface and shallow subsurface

410

environments. The finding of this study suggested that ACs are redox active and plays

411

roles both as electron accepting and donating reactions. The EEC of ACs are

412

comparable to that of humic substances (1.34 ~ 6.42 mM e- (g AC)-1 versus 2 ~ 5 mM

. Carbonaceous materials are ubiquitous in water, soils, and sediments in both 64

. Thus the understanding generated from



413

e- (g HS)-1)

62

414

oxygen-containing functional groups, i.e. quinone/hydroquinone moieties. Thus the

415

electron transfer properties of ACs could be taken analogous to humic substances in

416

considering the roles of ACs on biogeochemical redox processes and in particular the

417

environmental behavior and fate of organic contaminants and redox sensitive metal

418

oxides 65, 66. This provides further insights into the effect of carbonaceous materials on

419

the fate and transformation of contaminants during microbial reduction of

420

iron-bearing minerals and contributes to the agronomic and environmental impacts of

421

these biomass-derived carbonaceous materials.

and increase with the elevated content of redox active

422


Page 18 of 34

Page 19 of 34


423

ASSOCIATED CONTENT

424

Supporting information

425

Characteristics of ACs (diameter, FTIR, cyclic voltammetry, and EDC/EAC), initial

426

reduction rate of ferrihydrite, the effect of AC leachate on microbial reduction of

427

ferrihydrite, the total organic carbon content, the summary of model parameters, the

428

epifluorescence microscopy data, soluble electron shuttles in the culture suspension,

429

and XRD and SEM results. This material is available free of charge via the Internet at

430

http://pubs.acs.org.

431

AUTHOR INFORMATION

432

Corresponding author

433

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

434

Zhou).

435

Notes

436

The authors declare no competing financial interest.

437

ACKNOWLEDGEMENTS

438

We gratefully acknowledge the support by the National Natural Science Foundation

439

of China (21537002, 41422105, 41671478), and the National Key Scientific

440

Instrument and Equipment Development Project (No. 2013YQ17058508). We thank

441

Beijia Yuan from Nanjing Foreign Language School for help on epifluorescence

442

microscopy experiment. We also thank anonymous reviewers and associate editor Dr.

443

Thomas Hofstetter for their invaluable comments and suggestions to improve the

444

scientific quality of this paper.

445



Page 20 of 34

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651 652

Figure 1 Extent of Fe(III) reduction in ferrihydrite mediated by AC-X, AC-X-N2, and AC-X-N4 (A), AC-W, AC-W-N2, and AC-W-N4 (B),

653

and AC-S, AC-S-N2, and AC-S-N4 (C) in the presence and absence of a facultative bacterium, S. oneidensis MR-1. Please note biotic and

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abiotic controls refer to ferrihydrite reduction in the presence and absence of S. oneidensis MR-1, respectively.

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Figure 2 The live/dead cell counts using epifluorescence microscopy (note that the

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live cells emit green fluorescence and dead cells red fluorescence) in the culture

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suspensions during microbial reduction of ferrihydrite in the absence (biotic control)

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and presence of AC-W-N4 at three different times (32 h, 109 h, and 210 h). The white

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bar in each image represents 10 µm in length.

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Figure 3 Cyclic voltammetry of three types of ACs: AC-W, AC-W-N2, and

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AC-W-N4 (A). The electron donating capacity (EDC), electron accepting capacity

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(EAC), and electrical conductivity (EC) of the activated carbons (B). The electron

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exchange capacity (EEC) was calculated as the sum of EDC and EAC.

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Figure 4 Correlation between chemical and redox properties: A) electron exchange

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capacity (EEC), B) the content of C-OH, and C) the content of C=O of ACs with

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maximum reduction rate of ferrihydrite (kmax).

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Figure 5 Correlation of contents of C-defects (A), C-OH functional group (B), and

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C=O functional group (C) in ACs with the electron exchange capacity (EEC).

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Figure 6 Scanning electron microscopy (SEM) images of residual ferrihydrite and

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newly formed minerals after microbial reduction for 72 h (A and B) and 288 h (C and

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D) in the presence (B and D) and absence (A and C) of AC-W-N4. The inset in (D)

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shows layering and step-wise growth of the newly formed mineral. The flake and

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cubic shaped minerals are vivianite and siderite, respectively.


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Redox-Active Oxygen-Containing Functional Groups in Activated

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