Bioresource Technology 345 (2022) 126562

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Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Advances in interfacial engineering for enhanced microbial extracellular

electron transfer
Yi-Xuan Wang 1, Nannan Hou 1, Xiao-Li Liu , Yang Mu *
CAS Key Laboratory of Urban Pollutant Conversion, Department of Environmental Science and Engineering, University of Science and Technology of China, Hefei, China

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• A review on current status of interfacial

engineering enhances microbial EET.
• The strengthening mechanisms of mi­
crobial EET are summarized.
• Limitations of existing interfacial engi­
neering methods are discussed.
• Challenges and futuristic prospects of
interfacial engineering are highlighted.

A R T I C L E I N F O A B S T R A C T

Keywords: The extracellular electron transfer (EET) efficiency between electroactive microbes (EAMs) and electrode is a key
Extracellular electron transfer factor determining the development of microbial electrochemical technology (MET). Currently, the low EET
Microbial electrochemical technology efficiency of EAMs limits the application of MET in the fields of organic matter degradation, electric energy
Interfacial engineering
production, seawater desalination, bioremediation and biosensing. Enhancement of the interaction between
Electroactive microbes
EAMs and electrode by interfacial engineering methods brings bright prospects for the improvement of the EET
efficiency of EAMs. In view of the research in recent years, this mini-review systematically summarizes various
interfacial engineering strategies ranging from electrode surface modification to hybrid biofilm formation, then
to single cell interfacial engineering and intracellular reformation for promoting the electron transfer between
EAMs and electrode, focusing on the applicability and limitations of these methodologies. Finally, the possible
key directions, challenges and opportunities for future interfacial engineering to strengthen the microbial EET
are proposed in this mini-review.

1. Introduction (EAMs) transfer electrons generated by intracellular oxidized electron

donors to extracellular electron acceptors through a specific respiratory
Microbial extracellular electron transfer (EET) is a natural process chain, so as to realize the reduction of electron acceptors while main­
widely existed in biogeochemical cycles in which electroactive microbes taining the growth of the microbes itself (Kracher et al., 2016; Liang

* Corresponding author.
E-mail address: yangmu@ustc.edu.cn (Y. Mu).
1
These authors contributed equally to this work.

https://doi.org/10.1016/j.biortech.2021.126562
Received 31 October 2021; Received in revised form 7 December 2021; Accepted 9 December 2021
Available online 12 December 2021
0960-8524/© 2021 Elsevier Ltd. All rights reserved.
Y.-X. Wang et al. Bioresource Technology 345 (2022) 126562

et al., 2019; Wang et al., 2021a). Microbial EET mainly includes two EAMs and the electrode, and then promote the EET process of EAMs
pathways, including direct electron transport (DET) and indirect elec­ (Hindatu et al., 2017). Later, a new strategy was developed, which was
tron transport (IET), represented by Shewanella and Geobacter species to mix conductive nanomaterials with EAMs to form a hybrid biofilm,
among them (Shi et al., 2016). In DET, the outer membrane c-type cy­ aiming to improve the long-distance electron transport ability of EAMs
tochromes (OM c-Cyts) and conductive nanowires in EAMs help transfer and help the electrons produced by EAMs in the outer biofilm to be
electrons to the electrode. In IET, some intermediate metabolites such as transferred to electrode more quickly (Zhang et al., 2019). Next, in order
formate and H2, and redox shuttles including flavins, humic substances, to make full use of each active site on bacterial extracellular membrane,
pyocyanin phenazine and anthrahydroquinone disulfonate are served as modifiers were used in situ modification on the cell surface or insert into
the electron mediators, which can facilitate electron transfer from the the cell membrane (Jia et al., 2021). Furthermore, cells internalize
extreme outer surfaces of the biofilms to terminal electron acceptors conductive nanomaterials and some advanced synthetic biology
(Kumar et al., 2016). methods, e.g., clustered regularly interspaced short palindromic repeats
To date, the EET has been widely used in many fields including clean (CRISPR) gene editing system, have been developed for the genetic
power production, sewage treatment, bioremediation, biosensing, high- reconstruction and functional gene editing of EAMs to promote the
energy fuel conversion and synthesis, and showed a great potential for interaction between EAMs and extracellular electron receptors, thereby
development in future (Liang et al., 2019; Schroeder et al., 2015; Wang improving the microbial EET efficiency (Fan et al., 2021; Guo et al.,
& Ren, 2013). However, the relatively inefficient electron transfer be­ 2019). Indeed, there are several reviews published in this domain, while
tween EAMs and electron acceptors is the key bottleneck hindering the most of them mainly focused on surface modification by using conduc­
practical application of EET. The transfer of electrons from intracellular tive nanomaterials or structural design of the electrode and optimization
electrons to the electrode may undergo four key steps, of which the first of reactor operation parameters, aiming to promote the microbial EET of
one is transmembrane EET (Fig. 1). In this process, electrons need to EAMs and improve MET performance (Chong et al., 2019; Fan et al.,
overcome the non-conductivity and physical isolation of the membrane 2021; Zhao et al., 2020). To the best of our knowledge, only two papers
itself, and realize the electron transfer from intracellular to extracellular have reviewed promotion of the microbial EET by interfacial modifi­
(Melton et al., 2014). The second one is the interfacial EET process from cation of single cells of EAMs and construction of engineering EAMs
EAMs to the electrode surface, in which process electrons need to (Peng et al., 2018; Wang et al., 2021b). However, up to now there is lack
complete the transfer process from the surface of EAMs to the electrode of systematic review on interfacial engineering strategies aimed at
surface, thus the interfacial characteristics between the microbes and improving microbial EET efficiency.
electrodes will play an important role (Light et al., 2019). Thirdly, with In this review paper, a systematically overview focusing on
the gradual formation of biofilms, the EAMs far away from the electrode improving the EET efficiency via interfacial engineering strategies
surface need to transfer electrons to the electrode surface by means of ranging from electrode surface modification to hybrid biofilm forma­
trans-biofilm electron transfer process (Lee, 2018). Fourth, the inter­ tion, then to single cell interfacial engineering and intracellular refor­
specific electron transfer between two microbial cells is also an impor­ mation is provided. Meanwhile, the strengthening mechanisms of EET
tant form of electroactive microbial EET, and the realization of this process between EAMs and electrode are summarized. The purpose of
process requires microbial direct contact or the mediation of electron this mini-review is to summarize some of the important findings from
transfer intermediates (Wang et al., 2021c). No matter which electron relevant research areas and attempt to extract possible basic principles
transfer step is mentioned above, it is inseparable with the intrinsic from different research topics. Finally, some potential researches to
properties of EAMs and interface electron transfer efficiency. Therefore, develop the next generation methods for enhancing microbial EET ef­
constructing efficient electron transfer interface are expected to enhance ficiency and exploring strengthening mechanisms are also expected.
the interaction between EAMs and modifiers, and thus improving the
microbial EET efficiency. 2. Bacteria/electrode interfacial modification strengthens
In recent years, the research regarding the effect of interfacial en­ microbial EET
gineering on EET between EAMs and electrode is becoming increasingly
active (Sakimoto et al., 2018). Among them, the earliest and most Conductive nanomaterials generally have unique surface character­
commonly used method was to use conductive nanomaterials to modify istics, larger specific surface area, higher electrical conductivity and
the electrode surface to enhance the interfacial interaction between good biocompatibility. Previous studies have shown that the

Fig. 1. Schematic illustration for the four key steps of electrons transfer from intracellular to the electrode: (A) transmembrane EET, (B) interfacial EET process from
EAMs to the electrode surface, (C) trans-biofilm electron transfer process and (D) interspecific electron transfer between two microbial cells.

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introduction of nanomaterials could enhance the interface interaction bioelectrochemical systems (BESs) due to their unique characteristics.
between EAMs and electrode, accelerate long-distance electron transfer For example, it was found that the electricity generation capacity of
and promote the EET process of EAMs (Wang et al., 2021b). Generally, BESs inoculated with S. oneidensis MR-1 could be increased by three
the nanomaterials reported mainly include the following four cate­ times, by using carbon nanotubes to modify the carbon paper anode
gories: 1. Carbon nanomaterials, which usually have large specific sur­ (Wei et al., 2016). One of our previous studies demonstrated that the N-
face area and high electrical conductivity, are conducive to the doped graphene could significantly promote the EET of S. oneidensis MR-
colonization of EAMs and microbial EET, but some studies have showed 1, and identified that the current output of BESs was closely related to
that carbon nanomaterials have certain biological toxicity (Qiu et al., the content of pyrrolic N in the anode. Further analyses showed anodic
2017; Wang et al., 2019b), which may limit their application in this pyrrolic N doping could significantly reduce the thermodynamic and
domain; 2. Metal/metal oxide/metal sulfide nanoparticles, which have kinetic resistances of the DET and IET of S. oneidensis MR-1, thereby
smaller size and better controllability of microstructure, can not only be promoting the bacterial EET (Wang et al., 2020). However, some studies
used for electrode or microbial interface modification, but also be have showed that carbon nanomaterials have certain biological toxicity,
inserted into the cell periplasmic space to build electronic transmission which may limit their application in this domain (Peng et al., 2020; Qiu
channels (Cao et al., 2021; Wang et al., 2018; Xu et al., 2018); 3. et al., 2017).
Conductive polymers/oligomers, which usually have excellent conduc­ Moreover, some studies showed that specific functional groups,
tivity and biocompatibility, are often used as single-cell modifiers of implanted on the surface of the electrode, could form strong bonds with
EAMs to promote microbial EET or modifiers to help the formation of OM c-Cyts of EAMs, leading to a decreased electron transfer resistance
electroactive biofilms and consequently promote the long-distance and promoting the EET progress (Li & Cheng, 2019). For instance, it was
electron transfer (Hou et al., 2013; Yang et al., 2019). In addition, found that aryl-amine groups introduced into carbon anode could pro­
MOF-based conductive flexible nanomaterials, which could bond with mote the EET of Geobacter species and significantly improving the
the phospholipid bilayer of bacteria and allows for cell separation and bioelectricity output of BESs (Picot et al., 2011). Saito et al. (2011)
elongation, can play a long-term role in promoting the microbial EET of demonstrated that a small amount of -N(CH3)2 groups on carbon cloth
EAMs (Ji et al., 2018). 4. Carbon dots, which have extraordinary phys­ was sufficient to promote the EET of EAMs and consequently enhance
ical and chemical properties and extremely small size, can be ingested by BES performance (Saito et al., 2011). Lapinsonniere et al. (2013) dis­
EAMs and stimulate the physiological response of cells to enhance the closed that -B(OH)2 modification could improve the EET efficiency of
microbial EET efficiency (Liu et al., 2020; Yang et al., 2020). EAMs to some extent (Lapinsonniere et al., 2013). Besides the above
groups, it was found that peptide groups on the biofilm could interact
2.1. Electrode surface modification with amino groups on the modified electrode surface to form hydrogen
bonds and promoted the EET of EAMs (Tang et al., 2011). Beyond those,
The biofilm formed on the surface of the electrode under natural nitrogen-containing functional groups, sulfur-containing functional
conditions is thin and has poor conductivity, and the EET efficiency is groups and oxygen-containing functional groups, are often used to
relatively low (Li et al., 2020). For this reason, a series of electrode modify the electrode interface, which can significantly reduce the
interface modification means have been exploited to improve the interface electron transfer resistance, promote the microbial adhesion,
interaction between bacteria and electrode (Fig. 2). Additionally, the biofilm formation and the interface electron transfer (Ma et al.,
considering the diversity and structural complexity of EAMs, there are 2016). The functional groups used for interface modification generally
huge differences in EET process of different EAMs. Table 1 summarizes have electron-rich structures such as heteroatom conjugated structures
the proposed mechanisms of enhanced microbial EET of typical EAMs by and aromatic structures, indicating that functional groups with electron-
interfacial modification. Among these methods, carbon nanomaterials rich structures are beneficial to interface electron transfer.
modification is a most commonly used and extraordinarily effective On the other hand, many metal/metal oxide nanoparticles and
method (Wang et al., 2019b). Several kinds of typical carbon nano­ conductive polymers have been proven to be effective electrode inter­
materials, including graphene (Yang et al., 2019), carbon nanotubes face modifiers, which could significantly improve the EET efficiency of
(Wei et al., 2016) and their derivatives have been widely used as anode EAMs (Cao et al., 2021; Xu et al., 2018). For example, Zhao et al.
modifiers to improve the EET efficiency and bioelectricity generation in (2015b) reported a platinum nanoparticles decorated graphene anode,

Fig. 2. Electrode surface modification strengthens microbial EET.

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Table 1
The proposed mechanisms of enhanced microbial EET by interfacial modification.
Modifiers facilitating EET Microbes Roles Max power/current output References
2
Aryl-amine groups Mixed-culture Binding with OM c-Cyts 90 mW/m (Picot et al., 2011)
DSSN+ Mixed-culture Electron conduit ~ 4 μA (Garner et al., 2012)
Oligomers Escherichia coli Electron conduit 2.8 mW/m2 (Hou et al., 2013)
GO S. oneidensis MR-1 Conductive scaffold 843 ± 31 mW/m2 (Yong et al., 2014)
Platinum nanoparticles S. oneidensis MR-1 Conductive assistant 1460 mW/m2 (Zhao et al., 2015b)
Sludge-derived biochar Mixed-culture Conductive scaffold 568.5 mW/m2 (Ma et al., 2016)
FeS2 nanoparticles-GA Mixed-culture Conductive scaffold 3220 mW/m2 (Wang et al., 2018)
Polydopamine S. xiamenensis Conductive assistant 452.8 mW/m2 (Liu et al., 2019a)
rGO@PPy G. sulfurreducens Conductive scaffold 41.0 ± 0.2 A/m2 (Yang et al., 2019)
N-doped graphene S. oneidensis MR-1 Binding with OM c-Cyts 6.52 ± 0.06 A/m2 (Wang et al., 2020)
FeS nanoparticles S. oneidensis MR-1 Electron conduit 3210 mW/m2 (Yu et al., 2020)
Bio-palladium B. megaterium Serving as mediator NA (Jia et al., 2021)

NA: Not available.

achieving efficient EET and set a record of power output (1.46 W/m2) in 2.2. Hybrid biofilm formation
S. oneidensis MR-1 inoculated BESs (Zhao et al., 2015b). Jian et al.
(2020) prepared a Fe2O3-dopamine-polyaniline (PANI) hybrid com­ The EAMs far away from the electrode in the biofilm formed under
posite modified carbon felt anode, significantly improving the microbial natural conditions is difficult to transfer electrons efficiently to the
EET efficiency and degradation performance of indole (Jian et al., electrode surface. Therefore, some studies have shown that the use of
2020). However, it should be noted that metal/metal oxide nano­ conductive materials mixed with EAMs to form an electroactive hybrid
particles often have lipophilicity and small size effect, which may cause biofilm could ensure the electrons produced by the EAMs in the outer
direct physical damage to EAMs (Osonga et al., 2020). layer of biofilm efficiently to transfer over long distances to electrode
In addition, some research groups are committed to the development (Fig. 3). Among them, in-situ formation conductive materials by using
of three-dimensional anode materials with rich macroporous and mes­ the strong reduction ability of EAMs to form the electroactive hybrid
oporous structures, aiming to increase the bacterial capacity per unit biofilm has been demonstrated an effective way to enhance the long-
area, provide sufficient active sites for the electron shuttles and promote distance EET efficiency of EAMs. For example, Yong et al. (2014)
the microbial EET of EAMs (Guan et al., 2018). For example, a FeS2 found that adding graphene oxide (GO) into the anode of BESs could
nanoparticles modified three-dimensional (3D) graphene aerogel (GA) effectively promote the EET of S. oneidensis MR-1 (Yong et al., 2014).
electrode was fabricated, which could benefit bacterial amplification EAMs could reduce the GO in close contact with the electrode to reduced
and enrichment of Geobacter species on the electrode surface and facil­ graphene oxide (RGO), resulting in a large number of EAMs would
itates efficient EET, thus giving an unparalleled power output of 3.22 W/ adhere onto RGO surface and self-assembled into a 3D macroporous
m2 in BESs inoculated with mixed culture (Wang et al., 2018). Zou et al. network structure, thereby forming a hybrid biofilm of EAMs-RGO
(2016) prepared a 3D porous carbon nanofiber aerogel with rich mes­ conductive network, which ultimately improved the electron transfer
oporous structure by carbonizing bacterial cellulose at high tempera­ between EAMs and electrode. Bio-palladium (bio-Pd) nanoparticles
ture, which increased the active site of electron shuttles flavins synthesized by Bacillus megaterium Y-4 could act as a mediator to in­
molecule, and the twisted structure in the mesopore overcame the steric crease the redox sites in EPS, thereby promoting the electron hopping in
hindrance of flavin molecule, thus achieving the efficient EET (Zou the process of long-distance electron transmission (Jia et al., 2021). It is
et al., 2016). However, it is worth noting that synthetic 3D aerogel also reported that S. oneidensis PV-4 could use free ions in the bacterial
anode materials usually have poor mechanical properties and are diffi­ suspension to form FeS nanoparticles through biomineralization to form
cult to work in complex actual environments (Chen et al., 2012). The a hybrid electroactive biofilm. The FeS nanoparticles mixed in the bio­
development of 3D anode substitutes with high strength and flexibility is film hybridization could connect the spatially discrete redox environ­
the direction of future efforts. ment and mediate long-distance transfer of extracellular electrons
(Kondo et al., 2015). Moreover, mutant strain experiments indicated
that polysulfide reductases supplement the function of outer-membrane

Fig. 3. Biofilm hybridization strengthens microbial EET.

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cytochromes in EET process, increasing the possibility of electron individual S. oneidensis MR-1 cells with in-situ generated polypyrrole
transfer across long-distance of electroactive biofilm in sulfur-rich (PPy). The PPy-coated S. oneidensis MR-1 cells afforded an enhanced
anoxic environments. In addition, many studies have shown that the electrical conductivity with long-time viability and exhibited improved
addition of exogenous conductive materials such as metal oxides (e.g., DET efficiency, and consequently a maximum bioelectricity output as
iron oxides, manganese oxides and titanium oxide), conductive poly­ high as 0.15 W/cm2 was obtained in S. oneidensis MR-1 inoculated BESs,
mers (e.g., PANI, polypyrrole, and polythiophene), electronic shuttles which was 15 times that of the control one (Song et al., 2017). Chen et al.
(e.g., flavins, anthraquinone-2,6-disulphonic disodium salt and neutral (2018) reported a strategy for enhancing the EET efficiency of
red) could help to form a hybrid electroactive biofilm and thus promote G. sulfurreducens by in-situ formation of Au nanoparticles on the cell
the long-distance electron transport process (Kato et al., 2012; Xiao surface through biomineralization (Chen et al., 2018). In
et al., 2017; Yong et al., 2012). Notably, Freyman et al. used S. oneidensis G. sulfurreducens inoculated BESs, the maximum current density of the
MR-1 living cells, sodium alginate and cellulose as the solid filler to Au nanoparticles-loaded cells increased by 40 % compared with the
prepare conductive bioink, and constructed a reticular electroactive native cells, and the corresponding removal rate of organic substrates
hybrid biofilm with high bacterial concentration and excellent EET significantly increased. These studies indicated that the modification of
ability by 3D bio-printing technology (Freyman et al., 2019). individual microbial cells with conductive materials could significantly
enhance the EET efficiency between EAMs and electrodes. Notably, the
2.3. Single cell interfacial engineering conductive polymers/oligomers and metal/metal oxide nanoparticles
may not play a long-lasting role due to cell differentiation and growth,
Although the preparation of electroactive hybrid biofilms with resulting in lower system stability. Therefore, the development of
conductive materials can increase the EET rate of EAMs, but the conductive flexible materials may be a direction worthy of future
conductive materials cannot completely contact with all EAMs in the attention, since a previous study has shown that a flexible Zr-based
biofilm, causing a certain steric hindrance between them and resulting metal organic framework could bond with the phospholipid bilayer of
in a relatively low EET efficiency. Effective interfacial electron transport bacteria and allows for cell separation and elongation, addressing con­
demands close contact between EAMs and conductive abiotic surface cerns about the long-term properties of conductive materials (Ji et al.,
(Ding et al., 2014a; Ding et al., 2012). In order to establish an efficient 2018).
electron transmission channel between EAMs and electrode, interface On the other hand, for the sake of making modifiers interact more
modification of individual bacteria has been proven to be an effective closely with microorganisms, tiny modifiers were inserted into the
method (Fig. 4A). Recently, Yu et al. (2020) proposed a new single-cell membrane or periplasmic space to further interact with the proteins in
electronic collector concept to follow the “bottom-up strategy” to the electron chains on membrane (Kondo et al., 2015). Some studies
construct a highly effective biotic/abiotic interface. Briefly, a primary showed that a few oligomers and metal nanoparticles of the right size
electron collector that deposited on the outer membrane of S. oneidensis could be inserted into the cell membrane, break through the first barrier
MR-1 cell surface was assembled by in-situ polymerization of dopamine, of cells and accelerate the electron transfer across the cell membrane.
followed with the assembly of another electron collector by tuning the For example, Cao et al. (2021) reported a simple strategy to boost the
microbial biomineralization of FeS nanoparticles, constructing a highly EET efficiency of S. oneidensis MR-1 by introducing transmembrane and
efficient transmembrane electronic catheter, promoting the EET from outer-membrane silver nanoparticles. The resulting S. oneidensis MR-1-
individual cells to the electrode and achieving a power output of 3.21 silver BESs deliver a maximum current density of 3.85 mA/m2 and
W/m2, which set a record for the bioelectricity generation of single-cell turnover frequency of 8.6 × 105/s, and set a record among the
S. oneidensis MR-1 (Yu et al., 2020). Similarly, polydopamine coating on ever-reported S. oneidensis MR-1 inoculated BESs (Cao et al., 2021).
individual cells for enhanced EET of Shewanella. xiamenensis was real­ Additionally, conjugated short polymers not only have high electrical
ized, and a maximum power density of 0.45 W/m2 in BES was obtained, conductivity, but also the π-conjugated aromatic framework of the
far surpass that of the control one (0.075 W/m2) (Liu et al., 2019a). In molecule can delocalize the charge, and the ionic groups of the side
addition, Song et al. (2017) invented a universal method to encapsulate chain give it good water solubility. This amphiphilic molecule can

Fig. 4. (A) Cell-interfacial engineering, (B) cells internalize conductive nanomaterials and (C) internal genetic modification of cells strengthen microbial EET.

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directly cross the membrane or physically interact with the membrane, Table 2
thus improving the EET efficiency of EAMs (Ajo-Franklin & Noy, 2015; The proposed mechanisms of enhanced microbial EET by intracellular
Yang et al., 2008). Previously, a short polymer named stilbene tetraio­ reformation.
dide (DSSN + ) was synthesized and its effect on the EET of EAMs was Microbes Genes/ Roles Max References
employed (Garner et al., 2010). Research showed that DSSN + was Modifiers power/
successfully integrated into the phospholipid bilayer, with the hydro­ current
output
phobic long molecular chain of this molecule inserted vertically into the
cell membrane, and its polar end-point functional group located on the E. coli ArcA Up-regulate of 11.6 (Liu et al.,
core enzymes μW/cm2 2012)
surface of the cell outer membrane. Cyclic voltammetry scanning results
S. oneidensis MR- SO1860 and Reform NA (Ding et al.,
showed that the addition of DSSN + significantly accelerated the elec­ 1 SO3350 electroactive 2014b)
tron transfer of yeast across the biofilm, resulting in a distinct biofilm
improvement in the EET efficiency and bioelectricity generation per­ Clostridium fdh Promote 35.0 (Han et al.,
formance of BESs. In a similar study, the authors found that the addition ljungdahlii NADH mW/m2 2016)
generation
of DSSN + could increase the EET efficiency of EAMs in mixed-culture, S. oneidensis MR- ribD-ribC-ribBA- Up-regulate 37.0 (Min et al.,
and effectively improve the degradation rate of organic pollutants 1 ribE electron mW/m2 2017)
(Garner et al., 2012). In addition, the effect of the addition of DSSN + on shuttles
the EET process has also been verified in the pure bacteria system of G. sulfurreducens Phenylalanine Increase the NA (Tan et al.,
and tyrosine conductivity of 2017)
S. oneidensis MR-1. Kirchhofer et al. (2014) found that the addition of
genes nanowires
DSSN + could increase the EET rate of S. oneidensis MR-1 by 2.2 times S.oneidensis MR- nrfA、ccpA and Up-regulate 250 mA/ (Delgado
(Kirchhofer et al., 2014). Subsequent electrochemical characterizations 1 napB OM c-Cyts cm2 et al.,
showed that the addition of DSSN + mainly promoted the DET process 2019)
associated with OM c-Cyts. In a recent study from the same group, the P. aeruginosa Fimbriae Up-regulate ~ 140 (Liu et al.,
protein genes OM c-Cyts μA 2019b)
researchers designed and synthesized a series of oligomers with different
S.oneidensis MR- CymA genes Up-regulate 0.13 mW (Vellingiri
polymerization lengths and end-point functional groups. These oligo­ 1 OM c-Cyts et al.,
mers could be successfully fused into the cell membrane of E. coli, and 2019)
therefore a higher current output was obtained compared with the S. oneidensis MR- Carbon dots Activating 34.41 ± (Yang
1 intracellular 4.52 μA et al.,
control one (Hou et al., 2013).
signaling 2020)
pathways
2.4. Intracellular reformation strengthens microbial EET
NA: Not available.

2.4.1. Cells internalize conductive nanomaterials

In addition to the three interfacial modification methods mentioned formation. As a result, the CDs-fed cells increased the maximum current
above, intracellular reformation has also been demonstrated an effective output and power output by 7.34-fold and 6.46-fold, respectively,
way to facilitate the microbial EET of EAMs. Two methods for internal compared with the control one. Moreover, the enhancement efficacy
reformation of EAMs including internalization of conductive nano­ was found to be strongly dependent on the surface charge of the CDs
materials in cells and cell internal genetic modification will be listed (Yang et al., 2020). These two researches not only provide a simple and
below. In addition, considering the structural complexity of EAMs and effective strategy for improving the microbial EET performance through
versatility of functional genes, there are huge differences in EET process intracellular reformation, but more importantly, establish a basic un­
of different EAMs. Table 2 summarizes the proposed mechanisms of derstanding of the interaction between carbon-based semiconductors
enhanced microbial EET of typical EAMs by intracellular reformation. and EAMs. However, some studies have shown that it would produce
Recently, ultra-small modifiers, such as carbon quantum dots, have been strong biological toxicity when the concentration of CDs in microbes is
introduced into the cell interior, improving the metabolic activity of too high, which may induce potential environmental risk (Wang et al.,
EAMs and expanding the new idea of interface construction (Fig. 4B) 2019a; Zhao et al., 2015a).
(Guo et al., 2019). The cellular internalization of conductive nano­
materials can cause a wide range of biological responses and activate 2.4.2. Cell internal genetic modification
intracellular signaling pathways. Since the biocatalytic electron pool In the EET process, the biological characteristics of EAMs, such as the
that drives the EET pathway is located in the cytoplasm, nanomaterials intracellular electron transfer across cell membranes and biosynthesis of
entering the cytoplasm through the cell membrane may cause additional electron shuttles, have an important impact on the interaction between
interactions that affect the physiological functions and the EET effi­ cells and electron receptors and the microbial EET efficiency. The ge­
ciency of EAMs (Lu et al., 2020). For example, Liu et al. (2020) syn­ netic reconstruction and functional gene editing of EAMs carried out by
thesized carbon dots (CDs) with a diameter of about 7 nm through one- using bioengineering or synthetic biology methods have been demon­
step hydrothermal method, and found that the synthesized CDs could be strated as effective means to promote the interaction between EAMs and
internalized into the S. oneidensis MR-1 cells by simple addition. Under extracellular electron receptors, thereby improving the microbial EET
dark conditions, the internalized CDs could not only enhance the con­ efficiency (Fig. 4C). Next, we will take the following three perspectives:
ductivity of S. oneidensis MR-1, but also stimulate the physiological (1) Controllable up-regulate the conductive OM c-Cyts, (2) Promote the
response of S. oneidensis MR-1 to secrete a large amount of flavin-like synthesis and release of electron shuttles and (3) Reform the electro­
electron shuttles. Under the simulated sunlight, the electrons gener­ active biofilm, to elaborate the synthetic biology application in micro­
ated by the CDs in the cell were excited by the light to enter the intra­ bial EET promotion and analyze the corresponding strengthening
cellular metabolism, which driven the anaerobic respiration of mechanisms.
S. oneidensis MR-1 and enhanced the microbial EET efficiency (Liu et al., OM c-Cyts are high-speed channels for electrons to cross the insu­
2020). Similarly, a recent study by Yang et al. (2020) reported the lating cell membrane, which connects the intracellular electron gener­
augmentation of microbial EET with CDs feeding. The CDs-fed cells ation and the extracellular electron transport together, and it is also the
showed accelerated EET and metabolic rate, with increased intracellular intersection of DET and IET. Rational design and optimization of the OM
charge, higher adenosine triphosphate level, quicker substrate con­ c-Cyts system in EAMs is of great significance to promote the microbial
sumption and more abundant extracellular secretion. Meanwhile, the EET. Strategies such as optimization of periplasmic electron transport
CDs promoted cellular adhesion, electronegativity and biofilm chain, elimination of electron-consuming reaction in the periplasmic

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space, and overexpression of outer membrane conductive proteins are improve the microbial EET efficiency (Goedeke et al., 2011).
expected to improve electron transport rate between cells and electrode.
Vellingiri et al. (2019) found that the overexpression of CymA protein 3. Research needs and future directions
which located in the inner membrane could significantly improve the
microbial EET efficiency and bioelectricity production performance of S. Microbial EET is a research hotspot in the fields of biology, energy,
oneidensis MR-1 (Vellingiri et al., 2019). Delgado et al. (2019) revealed soil and environmental protection in recent years. The improvement of
that the replacement of some of the genes responsible for competing microbial EET efficiency is the key to whether it can move from the
electrons with heme synthesis genes in S.oneidensis MR-1 could promote laboratory to the practical application. The characteristics of microbes,
electron transfer in periplasmic space and increasing the reduction rate the properties of conductive nanomaterials, and the combination of
of iron citrate by nearly 2 times (Delgado et al., 2019). Tan et al. (2017) microbial cells and nanomaterials will all have a decisive effect on the
used genetic engineering methods to convert phenylalanine and tyrosine interface interaction between nanomaterials and microbes as well as the
at the carboxyl end of G. sulfurreducens fimbriae protein into tryptophan, interface electron transfer between microbial cells, thereby affecting the
and found that it can significantly increase the conductivity of nano­ efficiency of microbial EET.
wires (≈2000 times) (Tan et al., 2017). A recent study by Liu et al. The above-mentioned series of results show that interfacial engi­
(2019) demonstrated that the conductive fimbriae could be expressed in neering methods, including the use of numerous conductive nano­
non-conductive Pseudomonas aeruginosa by truncating the fimbriae materials to improve the interface characteristics of EAMs and electrode
protein gene of P. aeruginosa, dramatically improving the microbial EET as well as synthetic biology technology to modify EAMs, can effectively
efficiency (Liu et al., 2019b). It is reported that the manipulation of improve the interaction and the electron transfer efficiency between
mtrCAB pathway genes and biofilm-forming genes speF and uvrY126 by EAMs and electrode. However, the specific regulation mechanisms of
CRISPR-sRNA technology could regulate the EET efficiency of EAMs these methods still need to be further analyzed, and the microbial EET
(Cao et al., 2017). In addition, the synthesis and transfer of electron efficiency needs to be further improved in the process of moving towards
shuttles is one of the key factors that determine the EET rate. Recent practical applications. From the perspective of using nanomaterials to
studies demonstrated that the microbial EET rate could be greatly improve the interface properties between bacteria and bacteria or be­
increased by modifying the synthesis and transfer of soluble electron tween bacteria and electrode, the nanomaterials used to enhance the
shuttles such as riboflavin, phenazine and quinones in EAMs. For microbial EET efficiency require specific designs to match different EET
instance, Min et al. (2017) found that the co-expression of flavin pathways and solve the unique physical and chemical properties of
biosynthesis gene clusters ribD-ribC-ribBA-ribE and extracellular redox nanomaterials and microbes. The synthesis of new materials is also ur­
proteins mtrC-mtrA-mtrB in S.oneidensis MR-1 could significantly gently in need of research and development, such as materials with
improve the interaction between cells and electrode and further enhance special structures, bionic materials and natural materials. In addition,
the EET rate and bioelectricity production capacity of S.oneidensis MR-1 the strategy of combining nanomaterials with cell membranes or
(Min et al., 2017). Moreover, the core gene cluster (ribADEHC) encoding entering cells currently only includes modification of oligomers and
riboflavin synthesis in Bacillus subtilis was successfully introduced into some metals/semiconductors, indicating that there is still a lot of room
S. oneidensis MR-1 through multiple gene expression strategies in syn­ for development in material design mining. From the perspective of
thetic biology, resulting in the riboflavin yield was increased by 25.7 using synthetic biology methods to construct engineering bacteria,
times, which directly improved the EET efficiency of S. oneidensis MR-1. molecular biological methods make it possible to give EAMs stronger
The increase in riboflavin content also promoted the formation of electrical activity, and a number of studies have shown that genetically
S. oneidensis biofilm on the electrode surface, and further promoted the engineering microorganisms are superior to the corresponding wild
electron transfer efficiency directly associated with OM c-Cyts (Yang strains in terms of electrical activity and microbial EET efficiency. But so
et al., 2015). Additionally, electroactive biofilm is a dense group of far, the EET mechanisms in a large number of EAMs is still controversial,
conductive cells formed by cross-linking proteins, polysaccharides, DNA and the genetic toolbox of many microorganisms is not available.
and other polymers secreted by microorganisms, which is an important Therefore, it is necessary to identify, characterize and expand the EAMs
factor affecting the microbial EET efficiency. In a typical BES, biofilm resource library. Additionally, it is also necessary to use molecular
with high activity often contains more cells and is more favorable for biology methods to further study the metabolic network of EAMs to
electron transfer, but the biofilm formed under natural conditions is develop a toolkit for manipulating the expression of required metabolic
generally thin and contains a small number of cells, which is unfavorable pathways, establish genome-scale metabolic models of effective bacte­
for the close interaction and efficient electron transfer between EAMs rial strains, and explore complex integrated circuits to better manipulate
and electrodes. In recent years, synthetic biology has been extensively EAMs.
used to help the adhesion of EAMs to electrode surfaces, increase the Moreover, the mechanisms of the interaction between nanomaterials
thickness of electroactive biofilms and promote the close interaction and cells are urgently to be explored. Currently, relevant studies often
between EAMs and electrode. For example, a study by Lengag et al. used some apparent parameters such as the power output of MET and
(2013) showed that knocking out the GUS1240 gene encoding the PilZ conventional electrochemical characterization methods to indirectly
region of G. sulfurreducens conductive flagella could significantly in­ reveal the interaction between nanomaterials and bacteria. Since single
crease the thickness of engineering bacteria biofilm and promote the cell of EAMs can only produce ultra-low current, electrode with
close interaction between EAMs and electrode, resulting in the power numerous EAMs is needed for a distinct output signal. In addition, these
density output increased by 70 % (Leang et al., 2013). In addition, macroscopic measurement methods can neither reveal the effect of
Kouzuma et al. (2010) showed that the engineering bacteria with the modified materials on single cell activity of EAMs nor accurately clarify
polysaccharide synthesis gene SO3177 knocked out looked rougher and the interaction between EAMs and electrode in the microbial EET pro­
had stronger affinity to graphite electrodes, formed larger colonies and cess. Moreover, in view of the complex spatial pattern of BESs, the
promoted the combination of EAMs with electrode in BESs, and commonly used characterization techniques are impossible to clearly
increased the bioelectricity output by 1.5 times compared with the distinguish the mechanism behind the changes in the overall electro­
control one (Kouzuma et al., 2010). Ding et al. (2014) reported that chemical performance of BESs. Therefore, methods like nano-scale real-
knocking out the fimbriae synthesis genes SO1860 and SO3350 could time characterization methods such as single-cell imaging, in-situ
significantly increase the current output of wild-type S. oneidensis MR-1 Raman spectra, in-situ infrared spectra, synchrotron radiation-based
strain (Ding et al., 2014b). Gödeke et al. (2011) pointed out that X-ray photoelectron spectroscopy and cryo-electron microscopy and
knocking out the extracellular ribozyme-encoding gene exeM could other in-situ characterization techniques are needed to be explored, to
significantly increase the thickness of the biofilm, and consequently better understand local bacterial metabolism at high spatiotemporal

7
Y.-X. Wang et al. Bioresource Technology 345 (2022) 126562

resolution, deepen understanding of the interaction between conductive amphiphilic phenylenevinylene oligoelectrolytes. J. Am. Chem. Soc. 132 (29),
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This review explores and highlights the potential of interfacial en­ Guan, L.Z., Zhao, L., Wan, Y.J., Tang, L.C., 2018. Three-dimensional graphene-based
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herein will show a definite path to take MET forward for further improved performance of microbial fuel cell. Renew. Sust. Energy Rev. 73, 236–248.
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CRediT authorship contribution statement Ji, Z., Zhang, H., Liu, H., Yaghi, O.M., Yang, P., 2018. Cytoprotective metal-organic
frameworks for anaerobic bacteria. PNAS. 115 (42), 10582–10587.
Yi-Xuan Wang: Investigation, Writing – original draft. Nannan Jia, Y., Qian, D., Chen, Y., Hu, Y., 2021. Intra/extracellular electron transfer for aerobic
denitrification mediated by in-situ biosynthesis palladium nanoparticles. Water Res.
Hou: Investigation. Xiao-Li Liu: Investigation. Yang Mu: Supervision,
189, 116612.
Funding acquisition. Jian, M., Xue, P., Shi, K., Li, R., Ma, L., Li, P., 2020. Efficient degradation of indole by
microbial fuel cell based Fe2O3-polyaniline-dopamine hybrid composite modified
carbon felt anode. J. Hazard. Mater. 388, 122123.
Declaration of Competing Interest
Kato, S., Hashimoto, K., Watanabe, K., 2012. Microbial interspecies electron transfer via
electric currents through conductive minerals. PNAS. 109 (25), 10042–10046.
The authors declare that they have no known competing financial Kirchhofer, N.D., Chen, X., Marsili, E., Sumner, J.J., Dahlquist, F.W., Bazan, G.C., 2014.
interests or personal relationships that could have appeared to influence The conjugated oligoelectrolyte DSSN plus enables exceptional coulombic efficiency
via direct electron transfer for anode-respiring Shewanella oneidensis MR-1-a
the work reported in this paper. mechanistic study. Phys. Chem. Chem. Phys. 16 (38), 20436–20443.
Kondo, K., Okamoto, A., Hashimoto, K., Nakamura, R., 2015. Sulfur-mediated electron
Acknowledgements shuttling sustains microbial long-distance extracellular electron transfer with the aid
of metallic iron sulfides. Langmuir 31 (26), 7427–7434.
Kouzuma, A., Meng, X.Y., Kimura, N., Hashimoto, K., Watanabe, K., 2010. Disruption of
The authors wish to thank the National Natural Science Foundation the putative cell surface polysaccharide biosynthesis gene SO3177 in Shewanella
of China (52025101, U19A20108 and 51878637) for financially sup­ oneidensis MR-1 enhances adhesion to electrodes and current generation in microbial
fuel cells. Appl. Environ. Microbiol. 76 (13), 4151–4157.
porting this study. Kracher, D., Scheiblbrandner, S., Felice, A.K.G., Breslmayr, E., Preims, M., Ludwicka, K.,
Haltrich, D., Eijsink, V.G.H., Ludwig, R., 2016. Extracellular electron transfer
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