Nanomaterials for facilitating microbial extracellular electron transfer: Recent progress and challenges

Accepted Manuscript Nanomaterials for facilitating microbial extracellular electron transfer: Recent progress and challenges

Peng Zhang, Jia Liu, Youpeng Qu, Da Li, Weihua He, Yujie Feng PII: DOI: Reference:

S1567-5394(18)30082-3 doi:10.1016/j.bioelechem.2018.05.005 BIOJEC 7162

To appear in:

Bioelectrochemistry

Received date: Revised date: Accepted date:

12 March 2018 3 May 2018 3 May 2018

Please cite this article as: Peng Zhang, Jia Liu, Youpeng Qu, Da Li, Weihua He, Yujie Feng , Nanomaterials for facilitating microbial extracellular electron transfer: Recent progress and challenges. The address for the corresponding author was captured as affiliation for all authors. Please check if appropriate. Biojec(2017), doi:10.1016/j.bioelechem.2018.05.005

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ACCEPTED MANUSCRIPT Submitted to: Bioelectrochemistry

Nanomaterials for facilitating microbial extracellular electron transfer: recent progress and challenges

State Key Laboratory of Urban Water Resource and Environment, School of Environment,

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a

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Peng Zhanga, Jia Liua**, Youpeng Qub, Da Lia, Weihua Hea, Yujie Fenga*

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Harbin Institute of Technology. No 73 Huanghe Road, Nangang District, Harbin 150090,

b

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China

School of Life Science and Technology, Harbin Institute of Technology. No. 2 Yikuang Street,

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Nangang District, Harbin 150080, China

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*Corresponding Author:

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E-mail: [email protected]; phone: (+86) 451-86287017;

**Co-Corresponding Author: E-mail: [email protected]

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Fax: (+86) 451-86287017

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ACCEPTED MANUSCRIPT Abstract Nanomaterials for facilitating the microbial extracellular electron transfer (EET) process have drawn increasing attention due to their specific physical, chemical and electrical properties. This review summarizes the research advances of nanomaterials for accelerating

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the EET process. Nanostructured materials, including oligomer, carbon nanotube (CNT),

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graphene, metal, metal oxides, and polymer, exhibit numerous admirable properties such as

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large surface area, high electrical conductivity, and excellent catalytic activity. In this review, depending on the exact site where the nanomaterials work, the nanomaterials are classified

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into four groups: inside-membrane, interface, inside-biofilm and interspecies. Synthesis of the

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nanomaterials, EET enhancement performance, and corresponding enhancement mechanisms are also discussed. In spite of the challenges, nanomaterials will be extremely promising for

Nanomaterials;

Extracellular

electron

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Keywords:

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promoting the EET process application in the future.

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Inside-membrane; Inside-biofilm;

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transfer;

Interface;

Interspecie;

ACCEPTED MANUSCRIPT 1. Introduction Electrochemically active bacteria can transfer electrons to extracellular electron acceptors, including electrode, metal oxides and other bacteria [1, 2]. Different extracellular electron transfer (EET) strategies are utilized by the bacteria: (1) direct electron transfer (DET)

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by c–type cytochromes associated with the outer membrane or conductive pili; (2) mediated

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electron transfer (MET) through either exogenous or endogenous electron mediator [3]. Many

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factors affect the performance of EET process, including electron donors, catalyst, pH, oxygen and electrode materials [4-11]. Practical strategies for promoting EET process have

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been widely explored, including the choice of proper electron acceptor materials[12, 13].

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Many kinds of materials, including carbon [14-19], stainless steel [20], metal [21-23] and so on, have been used as the material to collect the electricity generated by the microorganism.

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For higher electricity generation, the material properties, including easy microbial

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colonization and attachment, stable physical and chemical properties and efficient electron transfer ability from the microorganism to electron acceptor surface, were favored in the

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material selection and design [24].The modification for electron acceptors with additional

EET rate.

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functional materials have been widely used to improve their performance in enhancing the

The modification of the EET process at nano-scale enables an efficient electron transfer from bacteria to the electron acceptor surface [25-27]. Some kind of oligomer and metals can facilitate the transmembrane electron transfer by inserting into the cell membrane, which is the first barrier for EET. Carbon nanotube (CNT), graphene, polymer, and metal oxide/metal have been used to accelerate the EET rate on the interface between bacteria and an electron 3

ACCEPTED MANUSCRIPT acceptor. Carbon and iron oxide nanomaterials can be effectively embedded into the biofilm and facilitate the long-range electron transfer along the biofilm. Despite enhancing the EET process from bacteria to electrode, nanomaterials can also accelerate the interspecies electron

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transfer (IET) process by constructing an artificial bridge between symbiotic bacteria.

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Schematic 1. The different nanomaterial modification site during the EET process. Inside-membrane modification: the nanomaterial could be inserted or insitu fabricated in the periplasm and facilitate the electron transfer through the membrane proteins; Interface modification: nanomaterials could be decorated on the interface between electron acceptor and bacteria, which promoted the bacterial attachment and interface electron transfer rate; Inside-biofilm modification: trans-biofilm electron transfer tunnels were built inside the biofilm to accelerate the electron transfer; Interspecies modification: electron transfer between two bacteria could be accelerated by interspecies nanomaterial conduit.

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In this review, the research of the nanomaterials modification for facilitating EET process has been summarized and these nanomaterials are classified, depending on the exact site where they interact with EET process, into four modification groups: inside-membrane, interface, inside-biofilm and interspecies (Schematic 1). The EET enhancement effect, corresponding mechanism, and advantages/disadvantages of different modifications at the different site are discussed here.

2. Inside-membrane modification 4

ACCEPTED MANUSCRIPT The cell envelope has a cytoplasmic membrane that is the primary barrier separating the internal molecules from the external environment [28, 29]. However, the structural components of the cell envelope such as lipid bilayer and peptidoglycan are electrically nonconductive and physically impermeable to solids. To overcome the physical and electrical

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obstacles of the cell envelope, bacteria have developed specialized mechanisms [30] through

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the corresponding membrane proteins such as c-type cytochromes [28] for EET process. The

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EET rate by intercalating into the cell envelope.

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nanomaterials of metals and oligomer with appropriate scale were reported to accelerate the

Schematic 2. Hypothesized pathways for the EET chain in the presence of Pd and oligomer in gram-negative bacteria. The oligomers can insert into the membrane and may increase the conductivity and permeability of the lipid bilayer; the Pb nanoparticles could be in-situ fabricated in the periplasm and facilitate the electron transfer through the membrane proteins. 2.1 Pd nanoparticles 5

ACCEPTED MANUSCRIPT The effect of the membrane-bound biosynthetic Pd nanoparticles on the EET process of the metal-reducing bacterium Desulfovibrio desulfuricans was studied [7]. In the cyclic voltammetry (CV) test, higher currents with lactate oxidation were observed for the cells with Pd nanoparticles than Pd-free cells and this result confirmed that the EET process was

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enhanced by the Pd nanomaterial. As shown in Schematic 2, the Pd nanoparticles might

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dominate spatially between the positions of cytochromes and accelerate the electron transfer

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along the natural enzymatic EET pathway due to the high conductive capacity of Pd particle. The advantage of the biologically derived nanomaterials is that they can possess high

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achieved by designed nanomaterials easily.

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recognition of redox proteins and intercalate into membrane adequately, which cannot be

2.2 Oligomer

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Oligomer is broadly described by a D-π-D structure, where D is an electron-donating

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group and π refers to a π-delocalized linker. One example is the molecule 1,4-bis(4′-(N,N-bis(6′′-(N,N,N-trimethylammonium)hexyl)amino)-styryl) benzene tetraiodide

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(DSBN+), which incorporates charged groups and increase the solubility in polar organic

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solvents and water. Oligomer with pendant groups was demonstrated to be effective for reducing charge injection barriers at some material interfaces [31]. On the basis of the molecular dimensions of DSBN+, it might be inserted into lipid bilayer membranes of bacteria in an ordered orientation and mediate the microbial transmembrane electron transfer process. In a previous study, a longer water-soluble analogue of DSBN+, namely 4,4′-bis(4′-(N,N-bis(6′′-(N,N,N-trimethy-lammonium)hexyl)amino)-styryl)stilbene tetraiodide 6

ACCEPTED MANUSCRIPT (DSSN+), was synthesized and successfully incorporated into lipid bilayer membrane in an orientation such that the hydrophobic long molecular axis was perpendicular to the plane of the cell membrane and the polar pendant group terminals were positioned at the outer surfaces (Schematic 2) [32]. The CV experiment results showed that the transmembrane electron

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transport was significantly improved with DSSN+ addition and the electricity generation

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performance of yeast microbial fuel cell was improved by nearly 10-fold. In a similar study,

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the addition of DSSN+ led to 2 to 8 times higher current generation from a microbial community present in wastewater and these communities are more effective at consuming

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organic contaminants [33]. Meanwhile, the enhanced EET performance with the DSSN+

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addition was also observed in the cathode system, indicating that DSSN+ could also influence the microbe-electrode interaction of electron injection into the cell. In a recent study from this

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research team, a series of oligomers with different conjugation length and ionic pendant group

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were designed and synthesized and they were all successfully incorporated into Escherichia coli cells, with significantly higher electricity generation than the control [34]. The effect of

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DSSN+ on EET was also tested in a pure culture of S. oneidensis MR-1 system, the most

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studied model electrode respiring bacteria [35]. The S. oneidensis MR-1 with DSSN+ exhibited a 2.2-fold increase in the extracellular electron output. The CV results revealed that the DSSN+ addition sustainably increased cytochrome-based DET process. However, another finding suggested that membrane permeabilization is the dominant mechanism for the enhancement of extracellular bioactivity in S. oneidensis by DSSN+ [36]. Thus, the specific mechanisms for enhancing current generation by the oligomer addition, including increased membrane permeability, enhanced bacteria attachment and faster electron transfer, should be 7

ACCEPTED MANUSCRIPT pinpointed in the future [29].

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3. Interface Modification

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Schematic 3. Different kinds of interface modification with nanomaterials. Polymer, CNT, graphene and metal/metal oxide can be decorated on anode surface seperately; meanwhile, these nanometerials can be used in combination. Interface properties between bacteria and an electron acceptor, which determine the local

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density of electroactive bacteria and the efficiency of electron transfer, are crucial to EET

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process. Many attempts have been dedicated to improving the electron transfer rate at bacteria/electrode interface such as utilization of mediators e.g. neutral red, quinone and thionine [37]. However, the exogenous mediators are expensive, toxic and have operating losses, which limited their practical application. With the rapid development of nanoscience and nanotechnology, the interface modification with nanomaterials has become an important option for consideration. On the one hand, nanomaterials decoration can form porous structures with the large surface area and promote bacterial adhesion and biofilm formation; 8

ACCEPTED MANUSCRIPT moreover, some suitable nanomaterials, such as transition metals or their oxides, can establish

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redox-active centers on the interface and accelerate the interface electron transfer rate [38].

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ACCEPTED MANUSCRIPT Table 1. Most separately used nanomaterials for anode interface modification in MFC; MCD indicate maximum current density.

Anode modification

CNT

Graphene

Support Glassy carbon Carbon cloth Carbon cloth Textile fiber Sponge Sponge Carbon cloth Carbon cloth Graphite plate Graphite

Polymer

Metal Oxide

Metal

ITO glass Carbon cloth Au plate Au plate Carbon cloth Carbon felt Carbon felt Carbon cloth Carbon paper/MnO2 Carbon paper/WO3 Carbon paper/TiO2 ITO glass/Iron Oxide Activated carbon/Iron Oxide Graphite/Au Graphite/Pd Carbon paper/Au

Influent

Method Drop and dry coating Dip and bake Electrodeposition Dipping-drying Dipping-drying Dipping-drying Electrophoresis Chemical reduction Electrochemical exfoliation Electrochemical exfoliation

Luria-Bertani Broth Acetate Lactate Domestic wastewater Glucose Glucose Glucose Acetate Acetate Tryptic soy broth

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MCD with MCD without nanomaterial nanomaterial (mA/m2) (mA/m2) 97 300 2650 2400 7200 4 2.13*10 245 5.5 1500 4

1.02*10

4

Refs

S. oneidensis MR-1 Mixed culture S. oneidensis MR-1 Mixed culture Mixed culture Mixed culture P. aeruginosa Mixed culture Mixed culture

Single chamber Single chamber Single chamber Double chamber Double chamber Double chamber Double chamber Double chamber Single chamber

[39] [40] [25] [41] [42] [24] [43] [44] [45]

Escherichia coli

Single chamber

[46]

1250 320 65 70 1190 70 500 283 900

Mixed culture Mixed culture S. loihica PV-4 S. loihica PV-4 S. loihica PV-4 Mixed culture S. decolorationis S12 S. oneidensis MR-1 Mixed culture

Single chamber Double chamber Single chamber Single chamber Double chamber Double chamber Double chamber Double chamber Double chamber

[47] [48] [22] [49] [50] [51] [52] [53] [54]

0.25*10

4

T P

I R

C S U

N A

M

Configuration

1.2 110 260 900 2800 4 1.44*10 158 2.6 930

Microorganism

In situ polymerization Chemical deposition

Starch Acetate Lactate Lactate Lactate Acetate Lactic acid Lactate Glucose

2.5*10 900 170 130 2400 110 2740 1639 2000

Painting method Soaking- calcination Chitosan-binding

Lactate Lactate Acetate

40 2000 35

30 1100 30

S. oneidensis MR-1 S. loihica PV-4 S. loihica PV-4

Double chamber Double chamber Single chamber

[55] [56] [57]

Rolling-Pressing

Acetate

2000

1500

Mixed culture

Single chamber

[58]

Sputter coating Sputter coating Sputter coating

Lactate Lactate Glucose

744 137 149

70 70 125

S. oneidensis MR-1 S. oneidensis MR-1 S. oneidensis MR-1

Single chamber Single chamber Single chamber

[59] [59] [60]

T P E

Electrochemical polymerization

C C

A

10

ACCEPTED MANUSCRIPT 3.1 Separate utilization of the nanomaterials CNT has been extensively studied to enhance the EET process on the anode surface due to their conductivity and structure properties [61, 62]. CNT can be fabricated on the surface of glassy carbon [39], carbon paper [25], carbon cloth [40] and graphite [63] to form the porous

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anode structure. The mechanism illustration proved that the CNT network was able to

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substantially enhance the c-type cytochromes/electrode interaction and the microbial adhesion

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on the surface. Yi Cui and his coworkers designed 3D macro porous electrode with CNT decoration on the surface. The CNT layers provided more active sites for bacteria adhesion

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and facilitated the electron transfer from exoelectrogens to the anodes [24, 41, 42]. CNT can

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also be used as the interfacial modification material to increase the sensitivity of a microbial biosensor by promoting the electron transfer between the bacteria and the electrode [64-66].

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The excellent properties of graphene include good mechanical strength, high chemical

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stability, excellent conductivity, and large surface area [67]. Graphene can be deposited on the carbon cloth anode to form a hybrid network, which significantly promoted the bacterial

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growth on the anode and the electricity generation in MFC [43, 44]. In addition, graphene can

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be in situ formed on the surface of graphite electrode by the electrochemical exfoliation method and the modified anode achieved ~2 to 4 times higher current generation in MFC [45, 46]. Both the CNT and graphene modification on anode surface in the MFCs can create large surface area and increase the conductivity of the anode，which benefited bacteria adhesion and accelerated the electron transfer from bacteria to the anode. However, although the fabrication processes of the CNT and graphene modification are simple，the stability of the surface nanostructures are low, which inhibited the long-term operation of MFC. 11

ACCEPTED MANUSCRIPT Many kinds of conductive polymers have been used to modify the anode surface to enhance the EET rate. Conductive porous polyaniline (PANI) nano-structures was developed on the anode of MFC [22, 47, 48], achieving a distinctive improvement in current generation compared with the control. When Polypyrrole (PPy) nanostructures were fabricated on anode

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surface [49, 52, 68], ~2 to 5 times higher EET current and rather long-term stability of the

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MFC were obtained. In a previous study, poly (3,4-ethylene dioxythiophene) (PEDOT) was

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electrochemically polymerized on the anode of MFC, which improved the power output by 43% [50]. Otherwise, poly (aniline-co-aminophenol) (PAOA) was also used to modify carbon felt

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anode, with the maximum power density of the MFC being increased by 18% compared with

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unmodified anode [51]. The higher roughness and electrochemical activity of polymer modified anode can increase the bacteria loading on the surface and facilitate the

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bioelectricity collection. Besides, the electrochemical polymerization process used for

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polymer modification could be easily tuned and the higher stability of polymer favors the long-term operation of the MFC. Specially, PPy could be coated on the surface of individual S.

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oneidensis MR-1, which showed that not only direct contact-based EET is facilitated, but also

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the viability of cells is improved [53]. The cells with PPy coating exhibited 4.8-fold higher electricity generation than the pure cells. The higher biocompatibility of polymer materials than CNT and graphene can also promote the biofilm formation on the anode surface. However, compared with CNT and graphene, the lower conductivity of polymer impeded the further higher electricity generation from the MFC system. Several kinds of metal oxides or metals have been utilized to modify the anode interface to accelerate the EET rate. Nano-structure MnO2 [54], WO3 [55], TiO2 [56] and iron oxide [57] 12

ACCEPTED MANUSCRIPT have been used to modify the anode surface with much higher electricity collection than the control anode. These nanostructures enhanced the bacterial adhesion on the anode and their electrochemical activity can accelerate the electron transfer rate between bacteria and anode. Iron oxide nanomaterial can also be mixed into activated carbon powder as an anode for

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MFCs [58]. During EET process, iron oxide serves as redox couple between Fe (Ⅱ) and Fe

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(Ⅲ) at the interface of biofilm and anode, which accelerated the electron transfer from

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bacteria to the electrode. The graphite anodes decorated with gold or palladium nanoparticles were used in the MFCs, which achieved ~2 times higher bioelectricity output [59, 60]. It was

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discovered that the size and morphology of nanoparticles were important factors affecting the

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EET rate. Besides, the electrochemically active bacteria could readily attach on the Au-sputtered carbon paper and form anodic biofilm readily. However, the disadvantage of

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metal/metal oxide modification is that it can not build a 3D structure on the anode surface to

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relieve the mass transfer inhibition induced by the thick biofilm.

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ACCEPTED MANUSCRIPT Table 2. Nanomaterials utilization in combination for anode interface modification in MFC; MCD indicates maximum current density.

Anode modification

CNT/Graphene

Metal or metal oxide/Graphene Graphene/Polymer

Metal oxide or Metal//Polymer

Graphene/CNT/Polymer

MCD with nanomaterial (mA/m2)

T P

Refs

S. putrefaciens CN32 S. oneidensis MR1

Double chamber Single chamber

[69] [70]

900

S. oneidensis MR1

Double chamber

[71]

250

S. oneidensis MR-1

Double chamber

[23]

1000

E.coli

Double chamber

[72]

550 2700 568 1278 100 2590 4610 3650 948.59

400 1080 400 300 20 600 1520 1825 501.44

E.coli Mixed culture Mixed culture E.coli E.coli Mixed culture E. coli E. coli Mixed culture

Double chamber Double chamber Double chamber Double chamber Single chamber Double chamber Single chamber Double chamber Double chamber

[73] [74] [75] [76] [21] [77] [78] [79] [20]

Method

Carbon cloth Carbon Paper

Freeze-drying Electrochemical Depositon

Lactate Lactate

2500 1900

ND

Freeze-drying

Glucose

5000

Nickel foam

Electrochemical polymerization Electrochemical deposition PTFE-binding Nafion-binding Dipping-drying Polymerization Press-drying Spray/dry Press-drying Press-drying PVA binding

Lactate

4000

Glucose

3590

Carbon cloth Carbon cloth Carbon paper ND Nickel foam Gold Electrode Carbon felt Nickel foam Stainless steel/Iron Oxide Carbon cloth/Pd Carbon felt/ WO3

Metal Oxide/MWCNT/Polymer Metal Oxide/Graphene/Polymer

Carbon cloth

D E

T P E

C C

A

Sponge Carbon cloth Glass carbon

Glucose Acetate Glucose Glucose Glucose Acetate Glucose Glucose Acetate

MCD without nanomaterial (mW/m2)

Configuration

Support

Carbon paper

CNT/Polymer

Influent

I R

C S U

N A

M

450 250

Microorganism

Nafion-binding PTFE-binding

Acetate Acetate

1100 2500

900 1100

S. oneidensis MR-1 S.putrefaciens

Double chamber Single chamber

[80] [81]

Dip-coating Drop-drying Drop-drying

LB broth Acetate Glucose

5.95*104 4730 2900

2.80*104 1690 1400

E.coli Mixed culture E. coli

Single chamber Double chamber Double chamber

[82] [83] [84]

Drop-drying

Glucose

2800

1300

E.coli

Double chamber

[85]

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ACCEPTED MANUSCRIPT 3.2 The nanomaterials utilization in combination Despite the separate utilization of nanoparticles for interface modification, the nanomaterials can be used in combination, which showed better performance on enhancing EET process by keeping the advantages and avoiding the disadvantages of the nanomaterials.

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For example, the combination of CNT with other nanomaterials can retain the feature of high

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length of CNT like conductive cellular pili produced by some electrochemically active

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microbes. In addition, the large surface area would offer a plenty of space for modification with other nanomaterials, which can improve the electrocatalytic capability of CNT [86, 87].

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Combination of CNT and graphene are the most studied carbon nanomaterials with the

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virtues of good conductivity, excellent stability, and outstanding biocompatibility. CNT shows an excellent electrochemical property for many bioelectrochemical processes, but it’s

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insufficient to provide 3D architecture with enough interface for bacterial adhesion [88].

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Graphene can form 3D architecture with the high specific surface area by suitable cross-linking. However, graphene is easy to form agglomerates during the fabrication process

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due to their strong van der Waals interactions [89, 90]. Porous hybrid anode could be

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fabricated by inserting multiwalled CNT (MWCNT) as a scaffold into the graphene skeleton [69, 70]. The insertion of MWCNT can both effectively inhibit the aggregation of graphene sheets and act as the bridge to increase the connection between graphene. This hybrid anode structure, with a higher surface area for E. coli immobilization, higher porosity for efficient mass transport and lower charge transfer resistance, delivered much higher current output than pure MWCNT or graphene. The larger surface area of graphene can provide more sites for metal oxide or metal 15

ACCEPTED MANUSCRIPT nanoparticles decoration, which could increase the biocompatibility and electrochemical activity of graphene. The anode decorated with both graphene and Pt nanoparticles with higher specific surface area and conductivity was used in MFC, which enhanced the EET from bacteria to the anode [71]. The anode surface could be simultaneously decorated with

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the polymer (PANI or PEDOT) and graphene, which outperformed the non-modified and

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separately modified one [23, 72, 91]. Graphene powders can also be modified on the anode

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surface with polymer binders such as PTFE, which achieved 25% to 170% higher electricity collected by the anode [73, 74]. On the one hand, the graphene and polymer decoration can

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enhance the bacteria adhesion with large surface area and the polymer binding can reinforce

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the interaction between graphene and anode surface; on the other hand, the insertion of graphene could reduce the resistance of polymer and promote the formation of 3D structure,

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which facilitated the mass transfer of the substrate and ions in the biofilm.

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Polyethyleneimine (PEI) [75], polypyrrole (PPy) [76], PANI [21], and poly (vinyl alcohol) (PVA) [77] have been used to modify the anode surface together with CNTs in the

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bioelectrochemical system. The CNT dispersion in the polymer matrix provided a 3D network

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with a high specific surface area and reduced the electron transfer resistance of the anode. CNTs were used as the backbone of this hybrid anode, which can circumvent the restrictions of pure CNTs including instability and toxicity, and the disadvantages of the pure polymer such as poor conductivity and small specific surface area [61]. The PANI was utilized to combine with the WO3 [78] or TiO2 [79] nanoparticle and used as the anode in MFCs, delivering ~2 to 3 fold power output in comparison to the control. The iron oxide nanomaterial was ever utilized as the anode interface decoration with PVA as a 16

ACCEPTED MANUSCRIPT binder to enhance the anode performance in electricity collection [20]. Pt/WO3 nanoplate can be fixed on the carbon cloth anode with the aid of PTFE binder and almost 45% higher power density was achieved as compared to the control electrode [81]. In a recent study, Pd nanoparticles were fabricated by a pure strain of S. oneidensis and coated on carbon cloth

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anode surface with the binding of PTFE [80]. The metal oxide or metal nanoparticles

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modified anode with a polymer as binder showed enhanced electron uptake ability and

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efficiency, which attributed to the excellent electrocatalytic ability of metal oxide or metal and conductivity of the polymer. The polymer could improve the low stability of metal oxide or

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metal nano-catalyst on anode surface and provide a large surface area for nano-catalyst

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loading.

In some cases, more than two kinds of nanomaterials can be used together to modify the

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anode surface of the MFC system. Sponges coated with graphene and CNT through a

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dip-coating method (polydimethylsiloxane as the binder) were fabricated and used as the anode of MFC, providing a large conductive surface for E. coli growth and 1.1 times higher

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electricity generation [82]. TiO2 and SnO2 nanoparticles with MWCNT as the support were

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fabricated and fixed on the anode surface with polymer as binder [83, 84], which increased current generation from the MFC. The greater electron collection performance can be attributed to the enhanced interfacial electron transfer, the higher surface area and better biocompatibility of this nano interface. Graphene and SnO2 nanoparticles with high specific surface area and electrochemical activity were fabricated on the anode surface of MFC with the binding of PTFE [85], achieving a power density of 2.8 and 4.8 times larger than that of just graphene coated and bare anodes. It was obvious that, with the participation of many 17

ACCEPTED MANUSCRIPT kinds nanomaterial, the disadvantages of individual nanomaterial can be greatly avoided; And the advantages, including long-term stability, large surface area, and high electrochemical activity can be simultaneously achieved. The excellent anode properties, including large surface area, high conductivity, high

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electrochemical activity and long-term stability, can be simultaneously achieved with various

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nanomaterial. In addition, the mesopores and micropores in the 3D structure are beneficial for

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bacteria adhesion and can be easily fabricated with various nanomaterial participation. It is our belief that these 3D anode fabricated with various nanomaterial can exhibit excellent

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properties for future applications in enhancing the EET process. This belief is actually proved

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by the increased number of works about the nanomaterial modification in combination within the last 10 years. Actually, every kind of nanomaterial mentioned above all showed a certain

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level of enhancement ability for EET; however, the appropriate combination of these

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nanomaterials showed better performance for higher EET efficiency than separate utilization. The main reason behind this trend is that the nanomaterials modification in combination can

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overcome the shortcomings and keep the advantages of individual nanomaterial.

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4. Inside-biofilm modification The biofilm in a self–produced polymeric matrix would gradually form and cover the electrode/bacteria interface, which would seriously limit the efficiency of the interface nanomaterials modification for promoting the EET rate. Specifically, the biofilm develops through four steps: bacterial surface attachment, monolayer formation, multilayer formation and formation of a polymeric matrix [92]. Thus, if the conductive nanomaterials are inserted into the inner part of the biofilm, the electron transfer rate from bacteria to the anode interface 18

ACCEPTED MANUSCRIPT can be facilitated.

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4.1. Iron oxide

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Figure 1. Schematic picture of the Shewanella/Fe2O3 (A) [93], SEM image of bacteria/MWCNT hybrid biofilm (B) [94], and the schematic picture of Shewanella/graphene/CNT (C) hybrid network of anode biofilm [95]. As shown in (A), the EET electrons were transferred to the ITO surface through the Fe2O3 nanoparticles; in the SEM image of bacteria/MWCNT hybrid biofilm (B), MWCNT could facilitate the electron transfer through the biofilm; Shewanella/graphene/CNT hybrid conductive biofilm (C) has been demonstrated to enhance the bacteria adhesion and direct-contact-based electron transfer from outer membrane c-type cytochromes to electrode.

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Conductive iron oxide can be used as electron tranfer conduit inside the biofilm for distant EET. Hashimoto et. al reported that Fe2O3 nano-colloids can force the Shewanella cells to self-assemble into an interconnected bacteria-nanomaterial network (Figure 1A), which resulted in fiftyfold current generation than the control [93]. The electron transfer conduit in the biofilm network enables the abundant cells located at a distance from the electrode to participate in the current generation. Afterwards, another study from this group found that iron oxide nanomaterials could also enhance extracellular electron generation from Geobacter 19

ACCEPTED MANUSCRIPT species and the microbial/mineral conductive network was developed in the presence of iron oxide nanomaterial [96]. It was also found that the inside-biofilm minerals can enhance the c-type cytochromes expression. In another study, it was reported that the decolorization rate of Aeromonas jandaei strain SCS5 was significantly enhanced by cell aggregation immobilized

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with magnetic Fe3O4 nanoparticles inside compared to immobilized cells only [97]. And the

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possible reasons can be due to the ability of Fe3O4 nanoparticles to facilitate microbial EET to

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electron acceptors through the aggregation. 4.2. Carbon nanomaterials

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A bacteria/MWCNT hybrid biofilm (Figure 1B) was fabricated through an

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adsorption/filtration method in our recent work. With this hybrid biofilm, the current density is increased by 46.2% and start-up time is reduced by 53.8% compared with naturally grown

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biofilm [94]. The researcher figured out a method to fabricated a hybrid electroactive biofilm

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by culturing S. oneidensis MR1 with graphene and CNT together [95]. And this hybrid conductive biofilm (Figure 1C) has been demonstrated to enhance the bacteria adhesion and

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direct-contact-based electron transfer from outer membrane c-type cytochromes to electrode.

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The current density generated by this hybrid biofilm reached 0.12 mA/cm2, which was significantly higher than the naturally grown biofilm (0.02 mA/cm2). The anode surface can also be coated with the mixture of magnetite/MWCNT nano-composite and E. coli cells, which helped the electron transfer from bacteria to the anode by the MWCNT channels inside biofilm [98]. Meanwhile, the magnetite inside the biofilm created a magnetic field and attracted more bacteria on the anode. The results showed that the anode with this hybrid biofilm generated a power density of 1050 mW/m2, which was 30% higher than the control 20

ACCEPTED MANUSCRIPT one. Along with facilitating the EET rate, the nanomaterials can also alter the EET route. In a recent study, the electron flow route within S. oneidensis MR-1 cell can be altered by CNT [99]. CNTs added into the cell-immobilized alginate beads can lead to a shift of intracellular nitrobenzene reduction to extracellular reduction, resulting a 74% improvement in

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nitrobenzene reduction efficiency.

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5. Interspecies modification

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Recent study has reported that microorganisms with EET ability in sedimentary environments may utilize the electric current, which was conducted by bacterial nanowires with

outer-membrane

cytochromes,

to

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combined

connect

spatially

segregated

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bio-geochemical redox processes [100]. Such direct electron transfer mechanism has also been recently studied in the co-cultures of Geobacter species [101, 102]. Multicultural

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microbial communities are also essential biocatalysts in the systems for wastewater treatment,

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environmental remediation, and energy production from biomass [103]. The interspecies electron transfer rate within these communities is especially important to biochemical reaction

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possibilities and rates. The nanoparticles, including iron oxide and carbon nanomaterial, have

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been employed as the electron conduit for higher direct IET rate between corresponding microbial species [104]. 5.1. Iron oxide

21

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Figure 2. SEM images of the syntrophic enrichments with nanoFe3O4 [105]. Iron oxide nanoparticles accumulated on the cell surface and connected the cells to each other, builting the electron transfer pathway for IET. Anaerobic digestion is a widely used bioenergy recovery technology by producing

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methane from organic wastes in anaerobic condition; however, the low efficiency and long retention time of anaerobic digestion restricted its practical application. Conductive

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nanomaterials were reported to be capable of enhancing the electron transfer between fermentative bacteria and methanogens in the anaerobic digestion system with higher methane production. Nano Fe3O4 could significantly accelerated the methane production in sludge by promoting the syntrophic butyrate oxidation [105]. It was discovered that this acceleration effect increased with the increase of nano Fe3O4 concentration but was dismissed when Fe3O4 was coated with silica that insulated the mineral from electrical conduction. This result indicated that the conductivity may play an important role in facilitating the IET process. As 22

ACCEPTED MANUSCRIPT shown in Figure 2, Fe3O4 nanoparticles accumulated on the cell surface and connected the cells to each other, builting the electron transfer pathway for IET. In another study, three different kinds of iron oxide nanoparticles (conductive magnetite, semiconductive haematite, and insulative ferrihydrite) were mixed in an anaerobic culture system inoculated with rice

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paddy field soil [106-108]. The results showed that the addition of semiconductive haematite

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and conductive magnetite nanoparticles significantly stimulated the methanogenesis from

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acetate and ethanol, while the methanogenesis was suppressed in the presence of insulative ferrihydrite. Iron oxide nanoparticles were also reported to improve the methane production

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from lignocellulosic biomass [109, 110] or the effluent of the hydrogen-producing reactor

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[111]. The above conclusions were also supported by our recent research, where iron oxide nanoparticles increased the biogas and subsequent methane production from the expanded

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eletrons to methanogens [112].

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granular sludge blanket reactor with these nanoparticles as electron transfer conduit to transfer

Besides promoting the methane production, the magnetite nanoparticles addition showed

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a positive impact on the improvement of metals stabilization in the anaerobic digestate [113],

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which can also be due to the enhanced EET process in the multicultural system. Iron oxide nanoparticles can also be used to facilitate the substrate degradation process by accelerating the IET rate. In a previous study, the conductive magnetite nanoparticles were reported to be able to wire up acetate-oxidizing bacteria to trichloroethene dechlorinating bacteria and result in 2 fold dechlorination rate [114]. And this study raised the possibility that the contaminants transformation can be improved by employing the conductive magnetite nanoparticles in bioelectrochemical remediation systems. Similarly, conductive magnetite nanoparticles were 23

ACCEPTED MANUSCRIPT reported to facilitate IET from G. sulfurreducens to Thiobacillus denitrificans and promote acetate oxidation coupled with nitrate reduction [115]. 5.2. Carbon nanomaterials Along with iron oxide nanoparticles, CNTs were also added in the methanogenic sludge

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of anaerobic wastewater treatment systems [116]. The results showed that CNTs in the sludge

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induced much faster substrate utilization and methane production. The sludge conductivity

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was also enhanced by the CNTs addition, which might promote direct IET between anaerobic fermentative bacteria and methanogens. The municipal solid waste incinerator fly ash with

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nano size was added to the anaerobic digestion reactors and enhanced the biogas production

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by accelerating the electron transfer [117]. In our recent work, MWCNTs were added in the anaerobic digestion reactor with beet sugar industrial wastewater [112]. The results showed

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that no significant difference of COD removal but 12.6% more methane production was

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observed and MWCNTs act as electron transfer pathway for IET.

6. Conclusions and perspectives

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This review tries to provide a comprehensive description of diverse nanomaterials that

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can be used for facilitating EET process. In conclusion, the nanomaterials, including oligomer, CNT, graphene, mental, metal oxides, and polymer, have been utilized to modify the anode and to enhance the electron transfer rate during different microbial EET processes. The large surface area and low electron transfer resistance of the nanomaterials can improve the bacteria adhesion and accelerate the electron transfer process respectively. Meanwhile, a direct contact between outer membrane c-type cytochromes and electron acceptors can be effectively established by the nanomaterials modification. Thus, in most cases, the enhanced EET rate by 24

ACCEPTED MANUSCRIPT the nanomaterials is a synergistic effect. However, it should not be ignored that, some nanomaterials mentioned above display certain antimicrobial activity against microorganism through the physical and chemical damage to the cells [118]. A number of physicochemical factors of the nanomaterial including

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the nano-size, shape and surface functional groups can influence their antimicrobial activities.

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Thus, in the design and fabrication process, the physical/chemical properties of the

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nanomaterials should be adjusted to minimize the antimicrobial activity and the nanomaterial dosage should be optimized to balance the antimicrobial activity and the enhancement effect

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on EET. Particularly, although the performance of the nanomaterials used in combination is

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usually better than that of seperate utilization, the antimicrobial activity of the nanomaterials may also be enhanced by hybridizing with other nanomaterials.

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As illustrated in this review, all the steps of EET process, including inside-membrane,

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interface between bacteria and an electron acceptor, inside-biofilm and interspecies, can be accelerated by the nanoparticles, indicating that EET process can be manipulated by many

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ways. It is obvious that most of these modifications just happened on the interface between

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bacteria and an electron acceptor. CNT, graphene, polymer, and metal oxide/metal were utilized for the interface modification. The interface modification with these nanomaterials combinations showed more excellent performance than the individual utilization, for the shortcomings of nanomaterials can be made up through the combination. Research trend during the recent years shows that more and more researchers tend to combine the nanomaterials together to optimize the EET enhancement effect by uniting the advantages of individual nanomaterial. 25

ACCEPTED MANUSCRIPT Other kinds of modification, including inside-membrane, inside-biofilm, and interspecies modifications, should be paid more attention in the future because all the steps play an important role in EET process besides the interface electron transfer process. The inside-membrane step of EET, which is limited by the electrochemical reactions of proteins

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involved in EET process, determines the efficiency of electron transfer from the inner part of

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cells to the extracellular electron acceptors through the membrane. As the first step of EET

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process, currently the inside-membrane modification only includes the modification with oligomer and some metals, indicating that there is still a lot of scope in this area.

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Inside-biofilm modification with nanomaterials do not only enhance the long-distance

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electron transfer process from bacteria located at a distance from the electron acceptor but also improve the substrate diffusion situation from the solution to the inner part of the biofilm.

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However, only some iron oxide and CNTs were utilized for this kind of modification. More

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nanomaterials and easy fabrication method should be developed for the construction of inside-biofilm electron transfer conduit pathways. For interspecies modification, the

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modification nanomaterials also just include iron oxide and carbon nanomaterials and other

process.

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kinds of nanomaterials with better performance should be developed to facilitate the IET

From the view of material fabrication, the nanomaterials used to enhance the EET process need specific design to fit different EET progress. For example, for the transmembrane EET process, the in-situ grown or transmembrane nanomaterials with small size are favoured to increase the permeability of the membrane or the electron transfer ability of corresponding proteins. For the EET interface process between bacteria and electrode, 26

ACCEPTED MANUSCRIPT beside conductivity and surface area, both catalytic and biocompatibility of the nanomaterials should be taken into consideration. The 2D or 3D nanomaterials with good biocompatibility and high conductivity are favored to facilitate the inside-biofilm EET process and the interspecies EET. Considering the fast development of nanomaterial science, it can be

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expected that there will be more research using nanomaterials to promote the EET process.

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Acknowledgements

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This work was supported by the National Key R&D Program of China (Grant No. 2016YFE0106500), National Natural Science Fund of China (Grant No. 51408156). Authors

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also acknowledged the International Cooperating Project between China and European Union

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(Grant No. 2014DFE90110) and Open Project of State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology (No. QA201609-01 and

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ESK201404).

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ACCEPTED MANUSCRIPT Reference [1] B.E. Logan, K. Rabaey, Conversion of Wastes into Bioelectricity and Chemicals by Using Microbial Electrochemical Technologies, Science, 337 (2013) 686-690. [2] X. Wang, Y.J. Feng, H.M. Wang, Y.P. Qu, Y.L. Yu, N.Q. Ren, N. Li, E. Wang, H. Lee, B.E. Logan, Bioaugmentation for Electricity Generation from Corn Stover Biomass Using Microbial Fuel Cells, Environmental science & technology, 43 (2009) 6088-6093. [3] U. Schroder, Anodic electron transfer mechanisms in microbial fuel cells and their energy efficiency, Physical chemistry chemical physics : PCCP, 9 (2007) 2619-2629.

PT

[4] K.Y. Kim, K.J. Chae, M.J. Choi, F.F. Ajayi, A. Jang, C.W. Kim, I.S. Kim, Enhanced Coulombic efficiency in glucose-fed microbial fuel cells by reducing metabolite electron losses using dual-anode electrodes, Bioresource

RI

technology, 102 (2011) 4144-4149.

[5] K.Y. Kim, W.L. Yang, B.E. Logan, Impact of electrode configurations on retention time and domestic

SC

wastewater treatment efficiency using microbial fuel cells, Water Research, 80 (2015) 41-46. [6] Y. Kim, M.C. Hatzell, A.J. Hutchinson, B.E. Logan, Capturing power at higher voltages from arrays of microbial fuel cells without voltage reversal, Energy & Environmental Science, 4 (2011) 4662-4667.

NU

[7] X. Wu, F. Zhao, N. Rahunen, J.R. Varcoe, C. Avignone-Rossa, A.E. Thumser, R.C. Slade, A role for microbial palladium nanoparticles in extracellular electron transfer, Angewandte Chemie, 50 (2011) 427-430. [8] P. Zhang, J. Liu, Y. Qu, Y. Feng, Enhanced Shewanella onedensis MR-1 anode performance by adding

MA

Fumarate in microbial fuel cell, Chem Eng J, (2017).

[9] D. Li, J. Liu, H.M. Wang, Y.P. Qu, J. Zhang, Y.J. Feng, Enhanced catalytic activity and inhibited biofouling of cathode in microbial fuel cells through controlling hydrophilic property, Journal Of Power Sources, 332 (2016) 454-460.

D

[10] D. Li, Y.P. Qu, J. Liu, G.H. Liu, J. Zhang, Y.J. Feng, Enhanced Oxygen and Hydroxide Transport in a Cathode Interface by Efficient Antibacterial Property of a Silver Nanoparticle-Modified, Activated Carbon Cathode in

PT E

Microbial Fuel Cells, ACS applied materials & interfaces, 8 (2016) 20814-20821. [11] Y. Du, Y.J. Feng, Y.P. Qu, J. Liu, N.Q. Ren, H. Liu, Electricity Generation and Pollutant Degradation Using a Novel Biocathode Coupled Photoelectrochemical Cell, Environmental science & technology, 48 (2014) 7634-7641.

CE

[12] Y. Qiao, S.-J. Bao, C.M. Li, Electrocatalysis in microbial fuel cells—from electrode material to direct electrochemistry, Energy & Environmental Science, 3 (2010) 544-553. (2016).

AC

[13] F. Yu, C.X. Wang, J. Ma, Applications of Graphene-Modified Electrodes in Microbial Fuel Cells, Materials, 9 [14] S.K. Chaudhuri, D.R. Lovley, Electricity generation by direct oxidation of glucose in mediatorless microbial fuel cells, Nature biotechnology, 21 (2003) 1229-1232. [15] S. Cheng, H. Liu, B.E. Logan, Increased power generation in a continuous flow MFC with advective flow through the porous anode and reduced electrode spacing, Environmental science & technology, 40 (2006) 2426-2432. [16] B. Min, B.E. Logan, Continuous electricity generation from domestic wastewater and organic substrates in a flat plate microbial fuel cell, Environmental science & technology, 38 (2004) 5809-5814. [17] D. Li, Y. Qu, J. Liu, W. He, H. Wang, Y. Feng, Using ammonium bicarbonate as pore former in activated carbon catalyst layer to enhance performance of air cathode microbial fuel cell, Journal of Power Sources, 272 (2014) 909-914. [18] X. Wang, N. Gao, Q. Zhou, H. Dong, H. Yu, Y. Feng, Acidic and alkaline pretreatments of activated carbon

28

ACCEPTED MANUSCRIPT and their effects on the performance of air-cathodes in microbial fuel cells, Bioresource technology, 144 (2013) 632-636. [19] H.M. Wang, D. Li, J. Liu, L.C. Liu, X.T. Zhou, Y.P. Qu, J. Zhang, Y.J. Feng, Microwave-assisted synthesis of nitrogen-doped activated carbon as an oxygen reduction catalyst in microbial fuel cells, Rsc Advances, 6 (2016) 90410-90416. [20] D.A. Jadhav, A.N. Ghadge, M.M. Ghangrekar, Enhancing the power generation in microbial fuel cells with effective utilization of goethite recovered from mining mud as anodic catalyst, Bioresource technology, 191 (2015) 110-116. [21] Y. Qiao, C.M. Li, S.-J. Bao, Q.-L. Bao, Carbon nanotube/polyaniline composite as anode material for

PT

microbial fuel cells, Journal of Power Sources, 170 (2007) 79-84.

[22] C.M. Ding, H. Liu, Y. Zhu, M.X. Wan, L. Jiang, Control of bacterial extracellular electron transfer by a

RI

solid-state mediator of polyaniline nanowire arrays, Energy & Environmental Science, 5 (2012) 8517-8522. [23] Y.-C. Yong, X.-C. Dong, M.B. Chan-Park, H. Song, P. Chen, Macroporous and Monolithic Anode Based on

SC

Polyaniline Hybridized Three-Dimensional Graphene for High-Performance Microbial Fuel Cells, ACS Nano, 6 (2012) 2394–2400.

[24] X. Xie, M. Ye, L. Hu, N. Liu, J.R. McDonough, W. Chen, H.N. Alshareef, C.S. Criddle, Y. Cui, Carbon

NU

nanotube-coated macroporous sponge for microbial fuel cell electrodes, Energy Environ. Sci., 5 (2012) 5265-5270.

[25] X.W. Liu, J.J. Chen, Y.X. Huang, X.F. Sun, G.P. Sheng, D.B. Li, L. Xiong, Y.Y. Zhang, F. Zhao, H.Q. Yu,

MA

Experimental and theoretical demonstrations for the mechanism behind enhanced microbial electron transfer by CNT network, Scientific reports, 4 (2014) 3732.

[26] J.J. Gooding, R. Wibowo, J. Liu, W. Yang, D. Losic, S. Orbons, F.J. Mearns, J.G. Shapter, D.B. Hibbert, Protein electrochemistry using aligned carbon nanotube arrays, Journal of the American Chemical Society, 125 (2003)

D

9006-9007.

[27] Z.-H. Liao, J.-Z. Sun, D.-Z. Sun, R.-W. Si, Y.-C. Yong, Enhancement of power production with tartaric acid

PT E

doped polyaniline nanowire network modified anode in microbial fuel cells, Bioresource technology, 192 (2015) 831-834.

[28] L. Shi, H. Dong, G. Reguera, H. Beyenal, A. Lu, J. Liu, H.-Q. Yu, J.K. Fredrickson, Extracellular electron transfer mechanisms between microorganisms and minerals, Nature Reviews Microbiology, (2016).

CE

[29] C.M. Ajo-Franklin, A. Noy, Crossing Over: Nanostructures that Move Electrons and Ions across Cellular Membranes, Advanced Materials, 27 (2015) 5797-5804. [30] E.D. Melton, E.D. Swanner, S. Behrens, C. Schmidt, A. Kappler, The interplay of microbially mediated and

AC

abiotic reactions in the biogeochemical Fe cycle, Nature Reviews Microbiology, 12 (2014) 797-808. [31] R. Yang, Y. Xu, X.-D. Dang, T.-Q. Nguyen, Y. Cao, G.C. Bazan, Conjugated Oligoelectrolyte Electron Transport/Injection Layers for Organic Optoelectronic Devices, Journal of the American Chemical Society, 130 (2008) 3282-3283.

[32] J.P. Logan E. Garner, Scott M. Dyar, Arkadiusz Chworos,, a.G.C.B. James J. Sumner, Modification of the Optoelectronic Properties of Membranes via Insertion of Amphiphilic Phenylenevinylene Oligoelectrolytes, J. AM. CHEM. SOC., (2010) 10042-100052. [33] L.E. Garner, A.W. Thomas, J.J. Sumner, S.P. Harvey, G.C. Bazan, Conjugated oligoelectrolytes increase current response and organic contaminant removal in wastewater microbial fuel cells, Energy & Environmental Science, 5 (2012) 9449. [34] H. Hou, X. Chen, A.W. Thomas, C. Catania, N.D. Kirchhofer, L.E. Garner, A. Han, G.C. Bazan, Conjugated Oligoelectrolytes Increase Power Generation in E. coli Microbial Fuel Cells, Advanced Materials, 25 (2013)

29

ACCEPTED MANUSCRIPT 1593-1597. [35] N.D. Kirchhofer, X. Chen, E. Marsili, J.J. Sumner, F.W. Dahlquist, G.C. Bazan, The conjugated oligoelectrolyte DSSN+ enables exceptional coulombic efficiency via direct electron transfer for anode-respiring Shewanella oneidensis MR-1—a mechanistic study, Physical Chemistry Chemical Physics, 16 (2014) 20436-20443. [36] K. Sivakumar, V.B. Wang, X.F. Chen, G.C. Bazan, S. Kjelleberg, S.C.J. Loo, B. Cao, Membrane permeabilization underlies the enhancement of extracellular bioactivity in Shewanella oneidensis by a membrane-spanning conjugated oligoelectrolyte, Applied microbiology and biotechnology, 98 (2014) 9021-9031. [37] D.R. Lovley, Bug juice: harvesting electricity with microorganisms, Nature Reviews Microbiology, 4 (2006) 497-508.

PT

[38] H.E. Jeong, I. Kim, P. Karam, H.J. Choi, P. Yang, Bacterial recognition of silicon nanowire arrays, Nano letters, 13 (2013) 2864-2869.

RI

[39] L. Peng, S.J. You, J.Y. Wang, Carbon nanotubes as electrode modifier promoting direct electron transfer from Shewanella oneidensis, Biosensors & bioelectronics, 25 (2010) 1248-1251.

SC

[40] H.-Y. Tsai, C.-C. Wu, C.-Y. Lee, E.P. Shih, Microbial fuel cell performance of multiwall carbon nanotubes on carbon cloth as electrodes, Journal of Power Sources, 194 (2009) 199-205.

[41] W.Z.H.R.L. Xing Xie, Chong Liu, Meng Ye, Wenjun Xie, Bianxiao Cui,, a.Y.C. Craig S. Criddle, Enhancing the

NU

Nanomaterial Bio-Interface by Addition of Mesoscale Secondary Features Crinkling of Carbon Nanotube Films To Create Subcellular Ridges, ACS Nano, 8 (2014) 11958-11965.

[42] X. Xie, L. Hu, M. Pasta, G.F. Wells, D. Kong, C.S. Criddle, Y. Cui, Three-dimensional carbon nanotube-textile

MA

anode for high-performance microbial fuel cells, Nano letters, 11 (2011) 291-296. [43] J. Liu, Y. Qiao, C.X. Guo, S. Lim, H. Song, C.M. Li, Graphene/carbon cloth anode for high-performance mediatorless microbial fuel cells, Bioresource technology, 114 (2012) 275-280. [44] P. Gangadharan, I.M. Nambi, J. Senthilnathan, V.M. Pavithra, Heterocyclic aminopyrazine-reduced graphene

D

oxide coated carbon cloth electrode as an active bio-electrocatalyst for extracellular electron transfer in microbial fuel cells, Rsc Advances, 6 (2016) 68827-68834.

PT E

[45] J. Tang, S. Chen, Y. Yuan, X. Cai, S. Zhou, In situ formation of graphene layers on graphite surfaces for efficient anodes of microbial fuel cells, Biosensors and Bioelectronics, 71 (2015) 387-395. [46] A.T. Najafabadi, N. Ng, E. Gyenge, Electrochemically exfoliated graphene anodes with enhanced biocurrent production in single-chamber air-breathing microbial fuel cells, Biosensors & bioelectronics, 81 (2016) 103-110.

CE

[47] Y. Zhao, K. Watanabe, R. Nakamura, S. Mori, H. Liu, K. Ishii, K. Hashimoto, Three‐Dimensional Conductive Nanowire Networks for Maximizing Anode Performance in Microbial Fuel Cells, Chemistry–A European Journal, 16 (2010) 4982-4985.

AC

[48] B. Lai, X. Tang, H. Li, Z. Du, X. Liu, Q. Zhang, Power production enhancement with a polyaniline modified anode in microbial fuel cells, Biosensors and Bioelectronics, 28 (2011) 373-377. [49] C. Ding, H. Liu, M. Lv, T. Zhao, Y. Zhu, L. Jiang, Hybrid bio-organic interfaces with matchable nanoscale topography for durable high extracellular electron transfer activity, Nanoscale, 6 (2014) 7866-7871. [50] X. Liu, W. Wu, Z. Gu, Poly (3,4-ethylenedioxythiophene) promotes direct electron transfer at the interface between Shewanella loihica and the anode in a microbial fuel cell, Journal of Power Sources, 277 (2015) 110-115. [51] C. Li, L. Zhang, L. Ding, H. Ren, H. Cui, Effect of conductive polymers coated anode on the performance of microbial fuel cells (MFCs) and its biodiversity analysis, Biosensors and Bioelectronics, 26 (2011) 4169-4176. [52] C. Feng, L. Ma, F. Li, H. Mai, X. Lang, S. Fan, A polypyrrole/anthraquinone-2, 6-disulphonic disodium salt (PPy/AQDS)-modified anode to improve performance of microbial fuel cells, Biosensors and Bioelectronics, 25 (2010) 1516-1520.

30

ACCEPTED MANUSCRIPT [53] R.B. Song, Y.C. Wu, Z.Q. Lin, J. Xie, C.H. Tan, J.S.C. Loo, B. Cao, J.R. Zhang, J.J. Zhu, Q.C. Zhang, Living and Conducting: Coating Individual Bacterial Cells with In Situ Formed Polypyrrole, Angew Chem Int Edit, 56 (2017) 10516-10520. [54] X.-B. Gong, S.-J. You, Y. Yuan, J.-N. Zhang, K. Sun, N.-Q. Ren, Three-Dimensional Pseudocapacitive Interface for Enhanced Power Production in a Microbial Fuel Cell, ChemElectroChem, 2 (2015) 1307-1313. [55] F. Zhang, S.-J. Yuan, W.-W. Li, J.-J. Chen, C.-C. Ko, H.-Q. Yu, WO3 nanorods-modified carbon electrode for sustained electron uptake from Shewanella oneidensis MR-1 with suppressed biofilm formation, Electrochimica Acta, 152 (2015) 1-5. [56] X. Jia, Z. He, X. Zhang, X. Tian, Carbon paper electrode modified with TiO 2 nanowires enhancement

PT

bioelectricity generation in microbial fuel cell, Synthetic Metals, 215 (2016) 170-175.

[57] J.Y. Ji, Y.J. Jia, W.G. Wu, L.L. Bai, L.Q. Ge, Z.Z. Gu, A layer-by-layer self-assembled Fe2O3 nanorod-based

RI

composite multilayer film on ITO anode in microbial fuel cell, Colloid Surface A, 390 (2011) 56-61. [58] X.H. Peng, H.B. Yu, X. Wang, N.S.J. Gao, L.J. Geng, L.N. Ai, Enhanced anode performance of microbial fuel

SC

cells by adding nanosemiconductor goethite, Journal Of Power Sources, 223 (2013) 94-99. [59] Y. Fan, S. Xu, R. Schaller, J. Jiao, F. Chaplen, H. Liu, Nanoparticle decorated anodes for enhanced current generation in microbial electrochemical cells, Biosensors and Bioelectronics, 26 (2011) 1908-1912.

NU

[60] M. Sun, F. Zhang, Z.-H. Tong, G.-P. Sheng, Y.-Z. Chen, Y. Zhao, Y.-P. Chen, S.-Y. Zhou, G. Liu, Y.-C. Tian, A gold-sputtered carbon paper as an anode for improved electricity generation from a microbial fuel cell inoculated with Shewanella oneidensis MR-1, Biosensors and Bioelectronics, 26 (2010) 338-343.

MA

[61] A.A. Yazdi, L. D'Angelo, N. Omer, G. Windiasti, X.N. Lu, J. Xu, Carbon nanotube modification of microbial fuel cell electrodes, Biosensors & bioelectronics, 85 (2016) 536-552. [62] G.-C. Zhao, Z.-Z. Yin, L. Zhang, X.-W. Wei, Direct electrochemistry of cytochrome c on a multi-walled carbon nanotubes modified electrode and its electrocatalytic activity for the reduction of H2O2, Electrochemistry

D

Communications, 7 (2005) 256-260.

[63] X.M. Zhang, M. Epifanio, E. Marsili, Electrochemical characteristics of Shewanella loihica on carbon

PT E

nanotubes-modified graphite surfaces, Electrochimica Acta, 102 (2013) 252-258. [64] S. Timur, U. Anik, D. Odaci, L. Gorton, Development of a microbial biosensor based on carbon nanotube (CNT) modified electrodes, Electrochemistry Communications, 9 (2007) 1810-1815. [65] F.J. Rawson, D.J. Garrett, D. Leech, A.J. Downard, K.H.R. Baronian, Electron transfer from Proteus vulgaris to

CE

a covalently assembled, single walled carbon nanotube electrode functionalised with osmium bipyridine complex: Application to a whole cell biosensor, Biosensors & bioelectronics, 26 (2011) 2383-2389. [66] G. Wang, J.-J. Xu, H.-Y. Chen, Interfacing cytochrome c to electrodes with a DNA – carbon nanotube

AC

composite film, Electrochemistry Communications, 4 (2002) 506-509. [67] K.S. Novoselov, Z. Jiang, Y. Zhang, S. Morozov, H. Stormer, U. Zeitler, J. Maan, G. Boebinger, P. Kim, A. Geim, Room-temperature quantum Hall effect in graphene, Science, 315 (2007) 1379-1379. [68] Y. Yuan, S. Kim, Polypyrrole-coated reticulated vitreous carbon as anode in microbial fuel cell for higher energy output, B Korean Chem Soc, 29 (2008) 168-172. [69] L. Zou, Y. Qiao, X.S. Wu, C.M. Li, Tailoring hierarchically porous graphene architecture by carbon nanotube to accelerate extracellular electron transfer of anodic biofilm in microbial fuel cells, Journal Of Power Sources, 328 (2016) 143-150. [70] Y.X. Huang, X.W. Liu, J.F. Xie, G.P. Sheng, G.Y. Wang, Y.Y. Zhang, A.W. Xu, H.Q. Yu, Graphene oxide nanoribbons greatly enhance extracellular electron transfer in bio-electrochemical systems, Chemical communications, 47 (2011) 5795-5797. [71] S. Zhao, Y. Li, H. Yin, Z. Liu, E. Luan, F. Zhao, Z. Tang, S. Liu, Three-dimensional graphene/Pt nanoparticle

31

ACCEPTED MANUSCRIPT composites as freestanding anode for enhancing performance of microbial fuel cells, Science Advances, 1 (2015). [72] Y. Wang, C.E. Zhao, D. Sun, J.R. Zhang, J.J. Zhu, A Graphene/Poly(3,4-ethylenedioxythiophene) Hybrid as an Anode for High-Performance Microbial Fuel Cells, Chempluschem, 78 (2013) 823-829. [73] Y. Zhang, G. Mo, X. Li, W. Zhang, J. Zhang, J. Ye, X. Huang, C. Yu, A graphene modified anode to improve the performance of microbial fuel cells, Journal of Power Sources, 196 (2011) 5402-5407. [74] L. Xiao, J. Damien, J. Luo, H.D. Jang, J. Huang, Z. He, Crumpled graphene particles for microbial fuel cell electrodes, Journal of Power Sources, 208 (2012) 187-192. [75] J.-J. Sun, H.-Z. Zhao, Q.-Z. Yang, J. Song, A. Xue, A novel layer-by-layer self-assembled carbon

PT

nanotube-based anode: Preparation, characterization, and application in microbial fuel cell, Electrochimica Acta, 55 (2010) 3041-3047.

RI

[76] Y. Zou, C. Xiang, L. Yang, L.-X. Sun, F. Xu, Z. Cao, A mediatorless microbial fuel cell using polypyrrole coated carbon nanotubes composite as anode material, International Journal of Hydrogen Energy, 33 (2008)

SC

4856-4862.

[77] H. Ren, S. Pyo, J.I. Lee, T.J. Park, F.S. Gittleson, F.C.C. Leung, J. Kim, A.D. Taylor, H.S. Lee, J. Chae, A high power density miniaturized microbial fuel cell having carbon nanotube anodes, Journal of Power Sources, 273

NU

(2015) 823-830.

[78] Y.Q. Wang, B. Li, L.Z. Zeng, D. Cui, X.D. Xiang, W.S. Li, Polyaniline/mesoporous tungsten trioxide composite as anode electrocatalyst for high-performance microbial fuel cells, Biosensors & bioelectronics, 41 (2013)

MA

582-588.

[79] Y. Qiao, S.-J. Bao, C.M. Li, X.-Q. Cui, Z.-S. Lu, J. Guo, Nanostructured polyaniline/titanium dioxide composite anode for microbial fuel cells, Acs Nano, 2 (2007) 113-119.

[80] X.C. Quan, B. Sun, H.D. Xu, Anode decoration with biogenic Pd nanoparticles improved power generation in

D

microbial fuel cells, Electrochimica Acta, 182 (2015) 815-820. [81] J.L. Varanasi, A.K. Nayak, Y. Sohn, D. Pradhan, D. Das, Improvement of power generation of microbial fuel

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cell by integrating tungsten oxide electrocatalyst with pure or mixed culture biocatalysts, Electrochimica Acta, 199 (2016) 154-163.

[82] H.-T. Chou, H.-J. Lee, C.-Y. Lee, N.-H. Tai, H.-Y. Chang, Highly durable anodes of microbial fuel cells using a reduced graphene oxide/carbon nanotube-coated scaffold, Bioresource technology, 169 (2014) 532-536.

CE

[83] Z. Wen, S. Ci, S. Mao, S. Cui, G. Lu, K. Yu, S. Luo, Z. He, J. Chen, TiO 2 nanoparticles-decorated carbon nanotubes for significantly improved bioelectricity generation in microbial fuel cells, Journal of Power Sources, 234 (2013) 100-106.

AC

[84] A. Mehdinia, E. Ziaei, A. Jabbari, Multi-walled carbon nanotube/SnO 2 nanocomposite: a novel anode material for microbial fuel cells, Electrochimica Acta, 130 (2014) 512-518. [85] A. Mehdinia, E. Ziaei, A. Jabbari, Facile microwave-assisted synthesized reduced graphene oxide/tin oxide nanocomposite and using as anode material of microbial fuel cell to improve power generation, International Journal of Hydrogen Energy, 39 (2014) 10724-10730. [86] X.L. Zuo, S.J. He, D. Li, C. Peng, Q. Huang, S.P. Song, C.H. Fan, Graphene Oxide-Facilitated Electron Transfer of Metalloproteins at Electrode Surfaces, Langmuir, 26 (2010) 1936-1939. [87] J.L. Chang, K.H. Chang, C.C. Hu, W.L. Cheng, J.M. Zen, Improved voltammetric peak separation and sensitivity of uric acid and ascorbic acid at nanoplatelets of graphitic oxide, Electrochemistry Communications, 12 (2010) 596-599. [88] K. Hyun, S.W. Han, W.G. Koh, Y. Kwon, Direct electrochemistry of glucose oxidase immobilized on carbon nanotube for improving glucose sensing, International Journal Of Hydrogen Energy, 40 (2015) 2199-2206.

32

ACCEPTED MANUSCRIPT [89] D. Li, M.B. Muller, S. Gilje, R.B. Kaner, G.G. Wallace, Processable aqueous dispersions of graphene nanosheets, Nature nanotechnology, 3 (2008) 101-105. [90] Y. Si, E.T. Samulski, Synthesis of water soluble graphene, Nano letters, 8 (2008) 1679-1682. [91] L. Huang, X. Li, Y. Ren, X. Wang, In-situ modified carbon cloth with polyaniline/graphene as anode to enhance performance of microbial fuel cell, International Journal of Hydrogen Energy, (2016). [92] C.C. Goller, T. Romeo, Environmental influences on biofilm development, Curr Top Microbiol, 322 (2008) 37-66. [93] R. Nakamura, F. Kai, A. Okamoto, G.J. Newton, K. Hashimoto, Self-constructed electrically conductive bacterial networks, Angewandte Chemie, 48 (2009) 508-511.

PT

[94] P. Zhang, J. Liu, Y. Qu, J. Zhang, Y. Zhong, Y. Feng, Enhanced performance of microbial fuel cell with a bacteria/multi-walled carbon nanotube hybrid biofilm, Journal of Power Sources, 361 (2017) 318-325.

RI

[95] C.-e. Zhao, J. Wu, Y. Ding, V.B. Wang, Y. Zhang, S. Kjelleberg, J.S.C. Loo, B. Cao, Q. Zhang, Hybrid Conducting Biofilm with Built-in Bacteria for High-Performance Microbial Fuel Cells, ChemElectroChem, 2 (2015) 654-658.

SC

[96] S. Kato, K. Hashimoto, K. Watanabe, Iron-Oxide Minerals Affect Extracellular Electron-Transfer Paths of Geobacter spp, Microbes and Environments, 28 (2013) 141-148.

[97] S.C.D. Sharma, Q. Sun, J.W. Li, Y.W. Wang, F. Suanon, J.Y. Yang, C.P. Yu, Decolorization of azo dye methyl red nanoparticles, Int Biodeter Biodegr, 112 (2016) 88-97.

NU

by suspended and co-immobilized bacterial cells with mediators anthraquinone-2,6-disulfonate and Fe3O4 [98] I.H. Park, Y.H. Heo, P. Kim, K.S. Nahm, Direct electron transfer in E. coli catalyzed MFC with a

MA

magnetite/MWCNT modified anode, RSC Advances, 3 (2013) 16665.

[99] F.-F. Yan, Y.-R. He, C. Wu, Y.-Y. Cheng, W.-W. Li, H.-Q. Yu, Carbon Nanotubes Alter the Electron Flow Route and Enhance Nitrobenzene Reduction byShewanella oneidensisMR-1, Environmental Science & Technology Letters, 1 (2014) 128-132.

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[100] L.P. Nielsen, N. Risgaard-Petersen, H. Fossing, P.B. Christensen, M. Sayama, Electric currents couple spatially separated biogeochemical processes in marine sediment, Nature, 463 (2010) 1071-1074.

PT E

[101] H.E.F. Zarath M. Summers, Ching Leang, Ashley E. Franks,Nikhil S. Malvankar, Derek R. Lovley, Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria, Science, 330 (2010) 3.

[102] M. Morita, N.S. Malvankar, A.E. Franks, Z.M. Summers, L. Giloteaux, A.E. Rotaru, C. Rotaru, D.R. Lovley,

CE

Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates, MBio, 2 (2011) e00159-00111.

[103] Q.W. Cheng, D.F. Call, Hardwiring microbes via direct interspecies electron transfer: mechanisms and

AC

applications, Environ Sci-Proc Imp, 18 (2016) 968-980. [104] B. Karn, T. Kuiken, M. Otto, Nanotechnology and in Situ Remediation: A Review of the Benefits and Potential Risks, Environ Health Persp, 117 (2009) 1823-1831. [105] H.J. Li, J.L. Chang, P.F. Liu, L. Fu, D.W. Ding, Y.H. Lu, Direct interspecies electron transfer accelerates syntrophic oxidation of butyrate in paddy soil enrichments, Environmental microbiology, 17 (2015) 1533-1547. [106] S. Kato, R. Nakamura, F. Kai, K. Watanabe, K. Hashimoto, Respiratory interactions of soil bacteria with (semi)conductive iron-oxide minerals, Environmental microbiology, 12 (2010) 3114-3123. [107] S. Kato, K. Hashimoto, K. Watanabe, Methanogenesis facilitated by electric syntrophy via (semi)conductive iron-oxide minerals, Environmental microbiology, 14 (2012) 1646-1654. [108] S. Zhou, J. Xu, G. Yang, L. Zhuang, Methanogenesis affected by the co-occurrence of iron (III) oxides and humic substances, FEMS microbiology ecology, 88 (2014) 107-120. [109] D. Ma, J. Wang, T. Chen, C. Shi, S. Peng, Z. Yue, Iron Oxide Promoted Anaerobic Process of the Aquatic

33

ACCEPTED MANUSCRIPT Plant of Curly Leaf Pondweed, Energy & Fuels, 29 (2015) 4356-4360. [110] Z. Yang, R. Guo, X. Shi, C. Wang, L. Wang, M. Dai, Magnetite nanoparticles enable a rapid conversion of volatile fatty acids to methane, RSC Advances, 6 (2016) 25662-25668. [111] Z. Yang, X. Xu, R. Guo, X. Fan, X. Zhao, Accelerated methanogenesis from effluents of hydrogen-producing stage in anaerobic digestion by mixed cultures enriched with acetate and nano-sized magnetite particles, Bioresource technology, 190 (2015) 132-139. [112] J.J. Ambuchi, Z. Zhang, L. Shan, D. Liang, P. Zhang, Y. Feng, Response of Anaerobic Granular Sludge to Iron Oxide Nanoparticles and Multi-Wall Carbon Nanotubes during Beet Sugar Industrial Wastewater Treatment, Water Research, (2017).

PT

[113] F. Suanon, Q. Sun, D. Mama, J.W. Li, B. Dimon, C.P. Yu, Effect of nanoscale zero-valent iron and magnetite (Fe3O4) on the fate of metals during anaerobic digestion of sludge, Water Research, 88 (2016) 897-903.

RI

[114] F. Aulenta, S. Rossetti, S. Amalfitano, M. Majone, V. Tandoi, Conductive magnetite nanoparticles accelerate the microbial reductive dechlorination of trichloroethene by promoting interspecies electron transfer

SC

processes, ChemSusChem, 6 (2013) 433-436.

[115] S. Kato, K. Hashimoto, K. Watanabe, Microbial interspecies electron transfer via electric currents through conductive minerals, P Natl Acad Sci USA, 109 (2012) 10042-10046. nanotube exposure, Water research, 70 (2015) 1-8.

NU

[116] L.-L. Li, Z.-H. Tong, C.-Y. Fang, J. Chu, H.-Q. Yu, Response of anaerobic granular sludge to single-wall carbon [117] H.M. Lo, H.Y. Chiu, S.W. Lo, F.C. Lo, Effects of micro-nano and non micro-nano MSWI ashes addition on

MA

MSW anaerobic digestion, Bioresource technology, 114 (2012) 90-94. [118] R. Das, C.D. Vecitis, A. Schulze, B. Cao, A.F. Ismail, X.B. Lu, J.P. Chen, S. Ramakrishna, Recent advances in

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CE

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nanomaterials for water protection and monitoring, Chem Soc Rev, 46 (2017) 6946-7020.

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Graphical abstract

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ACCEPTED MANUSCRIPT Highlights ●The

nanomaterials for accelerating extracellular electron transfer are reviewed.

●These

nanomaterials are classified into four groups depending on interaction sites.

●Advantages

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research potentials of these nanomaterials are suggested.

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●Future

and disadvantages of each type nanomaterial are discussed.

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