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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Redox Active Oxygen-Containing Functional Groups in Activated

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Carbon Facilitate Microbial Reduction of Ferrihydrite

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

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Zhao§, Deb P. Jaisi‡, Dongmei Zhou*, †

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

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§

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

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

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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

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

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[email protected].

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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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Introduction

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Biogeochemical redox reactions play an important role in the formation and

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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

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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

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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

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

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of humic substances.

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Carbonaceous materials have been widely reported to catalyze the chemical

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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.

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

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

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fact, many microbiological reactions including syntrophic methane production,

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

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be accelerated in the presence of carbonaceous material

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transformation mediated by carbonaceous material has been fairly studied, the

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mechanisms of carbonaceous material mediated microbial processes have rarely been

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elucidated

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

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22, 28

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

82

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

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

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

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kinetics of carbonaceous materials are thoroughly characterized recently

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findings provided a foundation to study the black carbon mediated microbiological

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

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. These

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

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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

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characteristics of AC that are responsible for enhancing microbial reduction of

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

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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

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objectives.

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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

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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

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

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

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

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

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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

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

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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

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reported in our previous publication 34.

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

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

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

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

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

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Supporting Information (SI, Texts S3 and S4).

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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

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

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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

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

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

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

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

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

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

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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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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leachates cannot be accounted for enhancing ferrihydrite reduction. Such rather

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

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stimulate microbial reduction of ferrihydrite

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

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

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

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

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

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

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

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

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

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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

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on the composition of incubation media used

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

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

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

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

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

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

. Compared to the different extents

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

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

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

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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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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compounds have limited contribution to facilitate microbial reduction of ferrihydrite

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

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below).

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Electrochemical property of the activated carbon

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During the microbial reduction of ferrihydrite, electrons generated by oxidation

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

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

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

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

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

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

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due to the conductive graphitic structure 21, 31.

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FTIR was suitable to characterize surface functional groups of highly oxidized

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

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

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

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

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

234

with our past findings 34.

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For both quinone and carbonyl functional groups, the decomposition temperature

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

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

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

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one quinone group or vice versa)

41, 42

. Since the carbonyl/quinone groups on the

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carbonaceous materials are known to be redox active

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

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

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

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

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

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

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

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

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carbon-oxygen functional groups of ACs

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

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

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

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groups such as quinone/hydroquinone species in ACs 47.

, cyclic voltammetric

45, 46

. Both the qualitative FTIR spectra and

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

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

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

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

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

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

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

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

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

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

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the content of surface quinone/hydroquinone species of ACs.

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Quinone/ hydroquinone

groups are well-known electron shuttles and

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

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

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

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

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chronoamperometric experiments can provide a reliable measure to quantify the EDC

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and EAC of ACs

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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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

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

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carbonaceous materials.

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

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

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

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nanotubes and carbon felt that were treated by HNO3

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

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

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

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

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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

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

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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),

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

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

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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

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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

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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

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

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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

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

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

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contribute to the microbial reduction of organic contamiants

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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

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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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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.

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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

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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

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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

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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

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(64) Michael I. Bird, J. G. W., Gustavo Saiz, Christopher M.Wurster, and Anna

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McBeath. The pyrogenic carbon cycle. Annu. Rev. Earth. Pl. Sc. 2015, 43 (1),

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273-298.

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(65) Yang, Z.; Kappler, A.; Jiang, J. Reducing capacities and distribution of

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redox-active functional groups in low molecular weight fractions of humic acids.

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Environ. Sci. Technol. 2016, 50 (22), 12105-12113.

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(66) Tan, W. B.; Xi, B. D.; Wang, G. A.; Jiang, J.; He, X. S.; Mao, X. H.; Gao, R. T.;

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Huang, C. H.; Zhang, H.; Li, D.; Jia, Y. F.; Yuan, Y.; Zhao, X. Y. Increased

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electron-accepting and decreased electron-donating capacities of soil humic

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substances in response to increasing temperature. Environ. Sci. Technol. 2017, 51 (6),

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3176-3186.

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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),

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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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