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Effective Constructions of Electro-Active Bacteria-Derived Bioelectrocatalysis Systems and Their Applications in Promoting Extracellular Electron Transfer Process

Congyuan Zhao , Jing Zhang , Zheng Chen , Jian Li , Lielin Shu , Xiaoliang Ji

Progress in Chemistry ›› 2022, Vol. 34 ›› Issue (2) : 397 -410.

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Progress in Chemistry ›› 2022, Vol. 34 ›› Issue (2) : 397-410 DOI: 10.7536/PC201221
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Effective Constructions of Electro-Active Bacteria-Derived Bioelectrocatalysis Systems and Their Applications in Promoting Extracellular Electron Transfer Process
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Abstract

The low extracellular electron transfer (EET) efficiency dominated by electro-active bacteria (EAB) in traditional bio-electrocatalytic systems (BESs) has largely restrained the applications of microbial electrocatalysis in environmental and industrial fields. To break this bottleneck, many scientists from the world attempted to develop advanced catalysts to improve the efficiency of electron transfer in BESs. It is expected that rational optimization by multi-disciplines technologies, including material science, electronic microbiology and synthetic biology, will improve the electron flux and efficiency of electron transfer. This optimization might promote the transition from traditional inorganic catalysts towards living catalytic biomaterials which promises to upgrade to be more precise, intelligent and controllable advanced materials in the future. The promotion will provide more beneficial technical support for the large scale application of advanced materials. Herein, this paper summarizes the effective constructions of several kinds of BESs (including employing graphene/microbes composited materials, in-situ semiconducting photocatalytic self-assembled biohybrids, core/shell-coated biohybrids and genetically manipulated engineering strains). In addition, the mechanisms regarding the strategies for strengthening EET are also elaborated in this paper. At last, current challenges that exist for microbes-based living biomaterials and underlying opportunities of biomaterials used in more environmental applications in the future are summarized.

Contents

1 Introduction

2 BESs constructed with EAB and inorganic/organic materials

2.1 Modified graphene improves the performance of BES

2.2 Engineering biohybrids by self-assembling with microorganism and photocatalytic semiconductors

2.3 Core/shell coated biohybrids

3 Improved performance of BES by incubating with genetically manipulated strains

3.1 Enlarged intracellular“electronic pools”

3.2 Manipulation of engineering strains by CRISPR technology

4 Conclusion and outlook

Graphical abstract

Keywords

extracellular electron transfer(EET) / bio-electrocatalytic system(BES) / semiconducting materials / synthetic biology / electron flux

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Congyuan Zhao, Jing Zhang, Zheng Chen, Jian Li, Lielin Shu, Xiaoliang Ji. Effective Constructions of Electro-Active Bacteria-Derived Bioelectrocatalysis Systems and Their Applications in Promoting Extracellular Electron Transfer Process. Progress in Chemistry, 2022, 34(2): 397-410 DOI:10.7536/PC201221

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1 Introduction

Microbial extracellular electron transfer has been involved in a variety of new energy development and environmental remediation fields, such as hydrogen production, methane production, degradation of organic pollutants, bio-metallurgy and remediation of metal pollutants through anaerobic microbial fermentation[1][2][3][4][5]. These processes are mainly microbial electrocatalytic processes through the two-way exchange of electrons and energy between electroactive microorganisms (EAB) and the external environment[6,7]. It can not be ignored that the efficiency of traditional EAB-dominated extracellular electron transfer (EET) is low, which greatly restricts the large-scale promotion and application of EAB in the field of electrocatalysis. In order to break through this key technical bottleneck, scholars at home and abroad have tried to develop advanced catalytic materials to improve the electron shuttle rate of Bio-Electrocatalytic System (BES). It is worth noting that human beings have found many kinds of self-assembled materials formed by natural succession from nature, and found their superior catalytic performance, precise nanostructure and good biocompatibility, which burst out new design inspiration and promoted the exploration of material science from macro to micro. These advances have correspondingly promoted the application of materials science in BES. From the early discovery of quinone compounds with electron shuttle effect in humus, to the later preparation of biochar from biomass resources, to the recent rise of carbon catalytic materials (such as graphene), these new attempts and discoveries are undoubtedly milestones in the development of material science and microbial electrocatalysis[8][9][10,11]. Continuous exploration has improved our understanding of new materials and inspired scientists to improve the various properties of materials at the micron and nanometer scales in order to achieve more diverse, complex and demanding BES.
In most BES, the electron transfer process between EAB and the extracellular electron acceptor interface is the key link affecting the electrocatalytic performance[12,13]. In particular, due to the interfacial orientation of electroactive redox proteins, it is difficult for traditional single inorganic catalytic materials to effectively promote the effective release of slow transfer electrons retained at the interface, which has largely become a bottleneck limiting the application of BES[14,15]. Considering the complex spatial distribution of reactants in BES, in order to improve the enzymatic reaction, scientists have gradually tried to modify the surface of inorganic catalytic materials, and try to graft EAB in-situ on functional materials to improve the biocompatibility of materials[16,17]. This greatly promotes the enrichment and growth of biofilm on the surface of electrode materials, improves the energy conversion efficiency, and realizes the transformation of catalytic materials.
Microorganisms are the representatives of delicate and intelligent living organisms, which can regulate the external electron transport flux through intracellular metabolism. It can be rationally assumed that if specific biological modification technology is used to design and reconstruct specific microbial components or enhance their functions, it is expected to break the "barrier" of low efficiency of traditional EET. Considering the increasingly severe energy demand and the low efficiency of traditional microbial electrocatalytic system, it is extremely necessary to build an advanced electrocatalytic system with high performance, refinement, low consumption and sustainability to meet the needs of engineering practice[18,19]. To this end, scientists from many countries have begun to try to use synthetic biology to help build new BES, and to ignite the "dawn" of hope for the development of new energy sources and the synthesis of high value-added products[20⇓⇓~23]. With the continuous attempt and exploration of synthetic biology technology, the scientific community has a new definition of the concept and definition of advanced materials, and has constantly improved people's understanding of the functions and applications of new materials.Even in order to enhance the performance of living biomaterials, organic microorganisms and inorganic catalytic materials are built together to achieve the effect of learning from each other's strengths and weaknesses[24][22,25]. For example, a "molecular bridge" is built between the electroactive protein and the exogenous inorganic catalytic material electrode, which strengthens the in situ electron transfer ability between the electron donor/electron acceptor at the molecular level, shortens the reaction time at the micro-nano scale, and improves the electrocatalytic performance of BES[26,27]. It can be seen that the combination of organic life and inorganic high-performance catalytic materials to achieve the effective construction of microbial living biomaterials will provide a source of innovation and vitality for the design of more advanced and intelligent biomaterials, and is expected to promote the upgrading of living catalytic materials to more intelligent advanced materials.
This article will focus on the construction and application of several typical BES based on the reported research and the previous work of our team, in order to explore the mechanism of BES in the process of strengthening EET. In particular, from the perspective of electromicrobiology and synthetic biology, this paper looks forward to the construction of more advanced and intelligent microbial living catalytic materials, in order to make a more scientific and reasonable interpretation of the future "biological inspiration or biomimetic materials", and to open up a broader development prospect for the future development of new energy and environmental pollution control.

2 BES Based on Microorganism-Organic/Inorganic Materials

2.1 Microorganism-Graphene Modified Composite

2.1.1 Graphene surface modified/loaded quinone compound composite material

In traditional BES, EET is often enhanced by the addition of soluble quinones, such as Anthraquinone-2,6-disulphonate (AQDS), Anthraquinone-2-sulfonate (AQS), and 2-hydroxy-1,4-naphthoquinone (HNQ)[8]. However, these quinones are often soluble and difficult to be biodegraded, and the secondary recovery is difficult, so the engineering application is often limited. Graphene is a new type of two-dimensional material with carbon atoms closely packed to form a single or multi-layer lattice structure, which has the characteristics of large specific surface area and high mechanical strength[28][29]. In addition, graphene has the characteristics of surface quinone/semiquinone groups and conductivity, which may show unique potential in EET process[30⇓~32][33⇓~35]. Encouraged by this, some researchers have tried to load soluble quinones on the surface of graphene to prepare solid and recyclable electron shuttle materials, thus avoiding the secondary pollution of quinones.
In recent years, many studies have made graphene compatible with microorganisms and prepared high-performance materials to enhance the EET process. Zhou Yang et al. Used Poly Urethane Foam (PUF) to load AQS on the surface of reduced Graphene Oxide (rGO) to obtain a new composite material (AQS-rGO-PUF) for exploring the application of microbial decolorization of azo dye acid red[36]. The electron transfer between AQS and rGO in the composite layer achieved a close synergistic effect, which increased the removal efficiency of acid red catalyzed by the composite by 1. 5 times and 5. 5 times, respectively, compared with the composite with AQS-PUF and rGO-PUF alone. Similarly, our research group previously loaded AQDS onto rGO to obtain AQDS-rGO composite, which was used to promote the microbial reduction and release of As (V)/Fe (III) in flooded high-arsenic soil. The results showed that the reduction and release of As (V) and Fe (III) in the soil after adding the composite were 2. 5 times and 1. 6 times higher than those in the control group, respectively[37]. In addition, our group prepared a new composite material of HNQ and GO (HNQ-PVA-GO) by using Graphene Oxide (GO) as template material and adding Polyvinyl Alcohol (PVA) (Fig. 1).The results showed that 50 mg/L Cr (Ⅵ) in wastewater could be completely removed within 72 H by adding the composite material, and the reduction efficiency of Cr (Ⅵ) was 3. 8 times higher than that of the control group, and the composite material could be recycled three times[38]. It can be seen that the new composite material formed by graphene and quinones greatly expands the application potential of graphene in environmental pollution remediation, and provides the necessary technical basis for further environmental pollution control.

2.1.2 Living Materials of Active Enzyme/Microorganism Immobilized on GO Surface Heterojunction

The super specific surface energy of GO provides more contact active sites for the interaction between microorganisms and reactants, and constructs more favorable electron shuttle "channels". In this regard, researchers have focused on the preparation of composite living materials by coupling GO with enzymes/microorganisms. In this regard, two-dimensional graphene is used as a substrate, and enzymes or microorganisms with different properties are orderly stacked on graphene in horizontal or vertical directions, thus forming a special structure (heterojunction) of copolymerization between materials with different properties. In the early stage, Ouyang et al. Prepared magnetic GO-immobilized Laccase materials and investigated the degradation efficiency of bisphenol A (BPA).The results showed that the acid adaptability, thermostability and storage stability of the loaded laccase were improved compared with the free laccase, and the activity of the loaded laccase remained 82% of its original activity after 10 times of catalytic degradation of BPA[39]. Rouhani et al. achieved effective coordination assembly of magnetic copper ferrite (CuFe2O4) nanoparticles, GO and laccase by chemical cross-linking method, and obtained a new catalyst GO-CuFe2O4-Laccase which could repeatedly and efficiently catalyze the synthesis of 4,4 '-sulfonyldiphenol (after 10 times of reuse, the activity of immobilized laccase still reached 80% of the initial activity)[40]. It can be seen that the heterojunction immobilization of small molecule active enzyme on GO surface can not only maintain the independent structure of enzyme molecules, avoid agglomeration, but also improve the stability of immobilized enzyme, and strengthen the activation energy between enzyme molecules and reactants in microenvironment (hydrophilic/hydrophobic). In addition, our research group also arranged S. xiamenensis and GO in an orderly manner through surface grafting technology, and prepared GO-S. xiamenensis composite living catalytic materials to enhance the reduction and removal of Cr (Ⅵ) in wastewater (Fig. 2)[41]. The large specific surface area of GO and the good biocompatibility of PVA make the S. xiamenensis accumulate continuously to form a thick biofilm in the repeated use, thus gathering more "governance" in the governance system. What is more gratifying is that the treatment system of living materials not only overcomes the bottleneck of most traditional BES reactions confined to anoxic environment, but also upgrades the catalytic performance of the recovered materials with the increase of cycle times. Therefore, the preparation of the living composite material by immobilizing the active enzyme or EAB heterojunction on the surface of GO not only maintains the activity of the enzyme and EAB to a certain extent, but also further provides more smooth electron transfer channels for EET, and improves the recycling times of the material, which provides the possibility for practical application.

2.2 In-situ hybrid photocatalysis semiconductor material self-assembly microbe

2.2.1 Semiconductor Photocatalytic Materials Self-Assembled Organic-Inorganic Hybrids of Non-Photosynthetic Microorganisms

In the natural environment, the photocatalytic process of semiconductor minerals and the EET process of microorganisms can form a close coupling relationship between structure and activity to a certain extent[42⇓~44]. This intimate relationship of multi-level self-assembly derived from the autonomous evolution of nature also gives more inspiration to the rational design of advanced materials. In recent years, the synthesis of specific chemicals catalyzed by this new hybrid has become a new research hotspot[23]. Semiconductor nanoparticles were in-situ grafted onto the cell membrane surface of microorganisms to form a special hybrid, which realized the complementary advantages of inorganic catalytic materials and organic microorganisms, and promoted the upgrading and transformation of substances from inorganic to organic. In the extracellular respiratory pathway of EAB, most of the electron supply is through the consumption of low molecular organic matter by EAB and the release of Bio-electrons to complete life metabolism[45]. In contrast, semiconductor materials can produce photoelectron-hole pairs under photoexcitation radiation. Photoholes (h+) with strong oxidizing property can be captured and quenched by a certain reducing agent (such as cysteine) to effectively separate and release photoelectrons, thus compensating the electron supply source required by the reduction and transformation of substances[46]. Therefore, after the semiconductor material is hybridized and self-assembled on the surface of the EAB cell membrane in situ, under specific light excitation, the EAB receives photoelectrons transmitted from the conduction band of the semiconductor material to the outer membrane protein, which strengthens the output of electron flow. In addition, the potential of photoelectrons is lower than that of most biological agents, which is more conducive to the reduction of substances[47]. Therefore, the hybrid not only saves the economic cost of organic carbon source consumption by obtaining light energy, but also does not cause burden on the environment in the whole process, which is of great significance for future environmental engineering applications.
However, how to establish a reliable and structure-activity correlation direct coupling system and make full use of this new hybrid BES? First of all, from the perspective of material design, green, sustainable and efficient have always been the important goals pursued by the development of photocatalytic materials. As a whole, EAB is the "main component" of the whole hybrid, and the nano-semiconductor material is the "key accessory" in the hybrid (Fig. 3). Then, how to select the ideal semiconductor materials, achieve efficient photocatalysis and establish a coordination mechanism with EAB is the most critical factor restricting the performance of the hybrid. The band gap energy and spectral response range have been the focus of attention in photocatalysis. Compared with other common semiconductor materials (for example, the band gap of TiO2 nanoparticles is 3.2 eV), the band gap energy of CdS nanoparticles is narrower (only 2.4 eV), which is more conducive to the excitation of photoelectron/hole pairs[48]. In the spectral response range, the nano TiO2 only responds to the ultraviolet light with the wavelength less than 387 nm, and the ultraviolet light is more likely to cause damage to microbial cells[51]. However, CdS nanoparticles respond to visible light and have a wider spectral response range, showing superior biocompatibility and being ideal semiconductor nanomaterials for hybrid assembly. At present, there have been a lot of studies on photocatalytic degradation of organic compounds, hydrogen production by water splitting and preparation of hydrocarbon fuels by photocatalytic nano-CdS[52⇓~54]. Therefore, constructing a new inorganic/organic hybrid composite system to enhance EET from the perspective of electromicrobiology is bound to tap its potential to a greater extent in future environmental engineering applications.

2.2.2 Application of new inorganic-organic hybrids in environmental engineering

Microbial/semiconductor hybrids have the advantages of strong light absorption, good biocompatibility and reusability, which make scientists try to apply them to many environmental fields. Yang Peidong et al. Successfully induced the photosensitization of Moorella thermoacetica, and used CdS nanoparticles deposited on the surface of bacteria as light collectors to obtain photoelectrons to promote the biological reduction of CO2 to synthesize acetic acid[46]. The results show that the quantum yield of the hybrid is as high as 1.6%, which is of the same order of magnitude as the average annual quantum yield of algae. Ye Jie et al. developed a Methanosarcina barkeri-CdS hybrid with high mechanical resistance and used it for photosynthetic absorption of CO2 to produce CH4[55]. Membrane proteins (such as H2ase) on the surface of bacteria are important carriers for photoelectron transfer. The CH4 production rate (0.19 mol/H) of the hybrid under light conditions was comparable to that of plants, and the copy number of mcrA gene was increased by 1.5 times. Wang et al. Found that photoelectron even promoted the biomass accumulation of Rhodopseudomonas palustris-CdS NPs hybrids in the process of nitrogen fixation (1.5 times that of the control group), enhanced the activity of nitrogenase, increased hydrogen production and corresponding reduction equivalent, strengthened the accumulation of intracellular ammonia and L-amino acids, and increased the photosynthetic rate by 6.73%[56]. In addition, these hybrids have also been successfully applied in the synthesis of high-value-added organic products such as hydrogen production, ethylene production and Polyhydroxybutyrate (PHB) (Table 1). In environmental pollution treatment, Huang et al. reported that G. sulfurreducens (CdS) -CdS hybrids directly utilized photoelectrons to achieve reductive removal of Methyl Orange (MO) under light-driven without adding organic carbon sources[57]. Among them, the extracellular membrane protein OmcB of bacteria is an important "hub" connecting the transmission between photoelectrons and extracellular electron receptors. It is worth noting that the maximum kinetic constant of MO degradation by hybrid can reach 1.441 h-1 (the highest reaction constant reported in the existing literature), which also provides a new idea for future wastewater treatment.
On the whole, BES constructed by semiconductor hybrid self-assembled microorganisms can effectively enhance the electron transfer and fully realize the conversion of light energy to electrical energy to chemical energy. Therefore, the traditional single photocatalytic material is optimized and upgraded, and more biological inspiration is given to realize the living upgrading transformation of the catalytic material, which promotes the organic integration of life science and material science, and also opens up a broader application prospect for new energy development and environmental pollution control. It is worth mentioning that semiconductor CdS nanoparticles are often used as assembly materials in the hybrids reported at this stage. This limitation depends to a large extent on the compatibility of microorganisms with "receptors" (I. E. semiconductor materials). In 2018, Joshi et al. Of Harvard University assembled nano-indium phosphide (InP) hybrid on Saccharomyces cerevisiae to provide reducing power for the synthesis of shikimic acid (an important precursor compound for some drugs and fine chemicals) by adding light energy to InP instead of the traditional pentose phosphate pathway.Thereby promoting the production of more shikimic acid by the hybrid to the greatest extent (the yield is 24 times of that synthesized only by the Saccharomyces cerevisiae)[58]. Therefore, if more matching semiconductor materials and EAB can be selected to coordinate and complement the electron transfer in the photocatalytic process and the EET process of microorganisms, it is expected to enhance the functional properties of hybrids and enrich their environmental applications, which is also a major problem to be considered and solved in the future design of photocatalytic hybrids.

2.3 Hybrids Assembled by Core/Shell Structure

2.3.1 Metal-Organic Framework-Encapsulated Biohybrid System

EAB is not only the main component of the hybrid, but also the most vulnerable component of the whole system. In particular, semiconductor materials can release a large number of Reactive Oxygen Species with oxidative activity (such as Reactive Oxygen Species, ROS) when they produce photoelectrons by photoexcitation, which is not conducive to the synthesis of end products and the metabolic growth of microorganisms (such as interfering with cell metabolism and destroying cell tissues)[72,73]. In this regard, in previous hybrid systems, "sacrificial reagents" with reducing ability (such as cysteine) were often added to quench the h+ to ensure the effective release of photoelectron flow[67]. However, this treatment method often leads to excessive dependence on sacrificial reagents and increases the cost of economic treatment, which is not conducive to the recycling economy of hybrids. In order to break this limitation, some scientists have found a new way to put on the "armor" of the fragile and sensitive EAB by means of the Metal-Organic Framework (MOF) with periodic network structure formed by self-assembly of Organic ligands and Metal ions. The MOF material has the characteristics of large specific surface area, porous channels and the like, so that the MOF material not only can effectively protect the EAB from being corroded by light h+, but also can ensure the porous channel transmission output of the released electron flow on a molecular scale[74]. For example, Liang et al. Encapsulated yeast with Zeolitic Imidazolate Frame-Work-8 (ZIF-8) to protect β-galactosidase (a non-native enzyme) from degradation by yeast[75]. Ji et al. used a monolayer of MOF[Zr6O4(OH)4(BTB)2(OH)6(H2O)6] instead of zirconia nanoparticles to encapsulate Morella thermoacetica (Fig. 4)[69]. Happily, they found that the death rate of microorganisms in the experimental group was significantly reduced by 5 times compared with the control group, and the time for catalyzing CO2 to synthesize acetic acid was shortened by 50%. In addition, due to the topology and extensibility of MOF, not only the encapsulated cells can be elongated and separated, but also the cells encapsulated by MOF can be maintained to the next generation in the later stage of expansion and reproduction.

2.3.2 Biohybrid System of Nano-enzyme Coatin

The preparation process of MOF is relatively complex and the synthesis cost is high, which also restricts the economic applicability of the hybrid to a certain extent. In contrast, nanoscale enzymes can not only maintain relatively high stability in extreme environments, but also have controllable synthesis conditions, and their catalytic ability can be coordinated. It is these advantages that have attracted much attention[77]. Therefore, it is very popular to use biological enzyme active molecules such as superoxide dismutase and catalase to load on the biological hybrid in situ. In particular, the method adopts nanoscale enzyme molecules carrying a plurality of catalytic enzyme activities (such as CeO2, Co3O4,Nano-enzymes such as MnFe2O4, V2O5, Fe3O4 and MnOx have attracted much attention. Chen Xiangyu et al. loaded Mn3O4 nanoenzyme on the surface of Thiobacillus denitrificans-CdS hybrid in situ[70]. After the T. denitrificans-CdS hybrid was coated with the T. denitrificans coating, the ROS generated during the photoelectric denitrification process was immediately eliminated (in which the concentrations of · OH and H2O2 were reduced by 90% and 26%, respectively, while the 28%,N2O emission rate was reduced by 78% as the reduction rate of N O 3 - increased, as shown in Fig. 5). This unique nano-enzyme coating not only ensures that the metabolic capacity of EAB is not damaged, but also effectively retains the simultaneous operation of the denitrification process of microorganisms and the photocatalytic reaction of CdS quantum dots. It can be seen that the in-situ loading of nanoenzyme to the hybrid not only has the advantages of easy operation and low economic cost in the synthesis process, but also greatly improves the applicability of the material and promotes the efficient and selective conversion of light energy to chemical energy.

2.3.3 Biohybrid System Constructed by Electron Trap

The lower electron exchange efficiency in the conventional biotic/abiotic interface is mainly limited by two reasons. On the one hand, EAB cells have the characteristics of "3D flexibility", which makes it difficult for most of the electron transfer channels on the surface of EAB cells to effectively contact with "2D rigid" non-biological interfaces (such as external electrodes or electron acceptors), resulting in limited interface electron transfer. In this regard, Du et al. Used Polydopamine (PDA), a polymer material with good biocompatibility, as a coating to wrap EAB, and found that the PDA-wrapped electroactive biofilm still grew well under different pH values, and the current density generated by the PDA-wrapped anode in a strong acid environment was 19 times higher than that of the control group[78]. It can be seen that the organic coating wrapped in the outer layer of EAB cells will greatly open up more channels for the effective transmission of electrons between the outer layer of EAB cell membranes and external electrodes. On the other hand, the lack of channels in the periplasmic space that can transfer electrons across the membrane leads to the retention of electrons in the periplasmic space and the formation of "electron traps", thus weakening the export of electrons. In order to break this bottleneck, Yong Yangchun and others put forward a new idea of "building electrodes on cells", and constructed a "single cell in situ electron trap" on a single S. oneidensis MR 1 cell (Fig. 6)[79]. Firstly, the "S trap" was constructed by in situ polymerization and assembly of PDA on the cell surface, which realized efficient electron transmembrane transmission. In addition, the in situ assembly of FeS nanoparticles on the cell surface and in the periplasmic space was regulated by EAB mineralization to construct a "SP trap", which could form a hybrid "protein-FeS" transmembrane electron channel with the electron channel proteins in the periplasmic space.O that electrons which are originally'idle 'in the'electron trap' are transmitted to the outside of the cell, the complete interconnection of the conductive micro/nano interface is realized, and the efficiency of interface electron transmission is improved. Notably, they inoculated the synthesized S. oneidensis @ SP complex organism into Microbial Fuel Cells (MFCs) and found that the current output was significantly enhanced, and the maximum output power obtained reached S. oneidensis, which was 15.7 times the power density (Microbial Fuel Cells) corresponding to the MFC inoculated with the wild strain, and was also the highest output power obtained by the MFC inoculated with S. oneidensis reported at this stage.
It can be seen that the new "shell structure" hybrid assembled from "bottom-up" highlights the advantages of large capacitance, high conductivity and strong stability, and opens up a new way to enhance electron transfer between biological/non-biological interfaces at the single cell level. Therefore, coating EAB cells with a "flexible and plastic" organic coating will beneficially improve the biological/abiotic electronic interface, thereby improving the efficiency of interfacial electron transfer and enhancing the performance of BES. This improvement is not only conducive to the construction of more advanced bioelectronic components in the future, but also expected to bring new opportunities for future environmental remediation and optical/electrical hybrid biocatalysis.

3 Enhanced EET process by genetically engineered bacteria

3.1 Enlarge the capacity of intracellular "electron pool"

Whether single BES or hybrid BES, EAB has always been an important producer and releaser of electrons, and its physiological activity and electron transfer effect at the electrode interface greatly restrict the performance of BES. In this regard, if the "main component" of BES can be accurately and effectively "reshaped", it will help to strengthen the function of EAB and improve the electron transfer efficiency of the electrocatalytic system. A large number of redox proteins are densely distributed in the cell membrane, periplasmic space and cytoplasm of EAB, which can be used as an important "electron pool" for intracellular electron transfer to the outside. For example, Shewanella can promote the EET process by secreting its own flavin[80]. In addition, the endogenous oxidized Form cofactor (Reduced Form of NAD) in the genus Shewanella can also provide more reducing power for the reduction reaction by oxidizing organic compounds to obtain electrons to produce Reduced form cofactor (NADH)[81]. Therefore, expanding the capacity of these intracellular "electron pools" can be an effective way to improve the efficiency of EET.
In 2015, Yang et al. Successfully expressed the flavin synthesis gene cluster of Bacillus subtilis heterologously on the Chassis Biological S. oneidensis MR 1, which increased the flavin secretion of the engineered bacteria by 26 times, strengthened the bidirectional EET efficiency and increased the EET efficiency by 15.5 times[83]. In 2017, Yu Hanqing et al. achieved directional modification of S. oneidensis MR-1 by overexpressing flavin coding gene cluster (ribD-ribC-ribBA-ribE) and metal reduction protein coding gene cluster (mtrC-mtrA-mtrB), and found that the current intensity of MFC reached S. oneidensis MR after 20 H after inoculation of genetically engineered strains[84]. Song Hao et al. Used the modular engineering strategy of synthetic biology to optimize EAB cells[82]. Starting from the genetic genes of S. oneidensis MR-1, they overexpressed 16 NADH production related genes in S. oneidensis MR-1 cells from the three pathways of de novo synthesis, salvage synthesis and general synthesis of S. oneidensis MR, respectively, and realized the metabolic optimization and reconstruction of the strain. It was found that the total amount of intracellular electron carrier NAD+ was significantly expanded, the NADH content was increased by 1.2 times, the NADH/NAD+ ratio was increased by 4.3 times, the substrate consumption rate was enhanced, and the EET rate was significantly increased (Fig. 7A). In particular, the maximum output voltage and lactate consumption rate of the MFC obtained by inoculating the engineered strain over-expressing the coding genes of ycel, pncB, nadM, nadD* and nadE* based on modular assembly (fig. 7 B) were significantly increased by 150% and 35%, respectively, compared with the MFC cultured by the wild strain (fig. 7 C, d).
It can be seen that gene editing technology can effectively improve the plasticity of EAB and greatly promote the catalytic performance of BES, which will be conducive to future environmental pollution control and energy utilization.

3.2 Application of CRISPR Platform in Construction of Genetically Engineered Strains

In BES, the good orientation of the redox protein of EAB on the electrode surface is an important prerequisite for direct and rapid electron transfer between the protein and the electrode[85⇓~87]. In this regard, if the target coding gene of the receiving terminal electron acceptor can be precisely optimized and regulated, the EET ability of EAB will be effectively improved[83]. The differences in the specificity of different redox proteins can easily lead to the introduction of electron flow generated by the metabolism of each protein into different electron receptors outside the cell[85]. There is no doubt that if the release of intracellular electron flow is too dispersed, it is easy to cause waste of electron flow and lead to a significant reduction in the amount of electron flow delivered to the target terminal electron acceptor outside the cell, and ultimately weaken the efficiency of electron transfer. First, if functional proteins that presumably compete for electrons can be filtered out by sieving, this will effectively cut off the way electrons are dispersed and transported within the cell. Secondly, by effectively identifying the target genes of electron transfer and overexpressing them, it can further promote the maximum directional conduction of intracellular electron flow to extracellular target electron receptors. Therefore, if the above two pathways can be coordinated and regulated, the efficiency of EET targeted delivery pathway will undoubtedly be greatly improved.
In recent years, with the rise of Clustered Regularly Interspaced Short Palindromic Repeats (CRISP), more and more researchers have begun to focus on the use of CRISPR/Cas system platform to assemble programmable genome elements and devote themselves to the transformation of new engineering strains[88,89]. Through this technology, the "metabolic flux" of the regulatory gene circuit can be further optimized, so that the cell factory can be optimized and the expansion of extracellular electron flow can be promoted. Recently, some researchers have begun to explore the modification of this technology[90,91].
In recent years, it has been reported that CRISPR gene editing technology has been applied to the identification and degradation of resistance genes, and even to knock out resistance genes in bacteria to prevent the horizontal transfer of resistance genes[92,93]. For example, Wu et al. Rapidly identified the functional genes related to arsenic transfer in A. hydrophilia ATCC7966 by CRISPR interference (CRISPRi) technology[91]. Li et al. creatively proposed the construction strategy of CRISPR-ddAsCpf1 gene network platform, and through effective means such as "screening-diagnosis-verification", they effectively inhibited 10 terminal reductases competing for electron transfer in S. oneidensis MR 1 and overexpressed several transcriptional proteins targeting electron transfer (Fig. 8A, B), which directionally strengthened the extracellular electron flow of S. oneidensis MR 1[90]. With the help of this strategy, a large EET network can be effectively constructed and the EET capability can be greatly improved. Among them, the MO reduction rate of the genetically engineered bacteria obtained by overexpression of three targeted genes (fccA, dmsE and cctA) was increased by at least 3 times, and the Cr (Ⅵ) reduction efficiency of the genetically engineered bacteria obtained by overexpression of five targeted genes (so0717, napB, dmsE, so2930 and nrfA, Fig. 8C, d) was increased by at least 25% (especially the Cr (Ⅵ) reduction efficiency of the dmsE gene modified strain was the highest, significantly increased. It can be seen that the strategy based on gene modular operation can accurately and effectively improve or inhibit the expression level of specific targeted genes, enhance the related functions of environmental functional microorganisms, and strengthen the effectiveness of electrons received by target terminal electron receptors. This will be of great strategic significance to promote the functional optimization of EAB and the energy recovery of BES and the synthesis of high value-added products.
Of course, there are many EAB genetic engineering strategies reported at this stage. For example, it is also one of the effective means to regulate gene circuits by releasing chemical signals to coordinate the group behavior of EAB through quorum sensing among microorganisms[94]. Chemical signal molecules released by quorum sensing can promote intercellular communication to a certain extent, enhance the activity, proliferation, viability and aggregation of EAB, and thus enhance the expression of related genes[95]. In conclusion, in the current context, the pace of developing and broadening effective synthetic biology still needs to be accelerated. In particular, how to use effective synthetic biology methods and give full play to their respective technological advantages requires researchers to invest more time and energy in the design of the overall gene circuit.

4 Conclusion and prospect

This paper summarizes the effective construction of several types of BES and their environmental applications for enhanced EET. In particular, it focuses on new inorganic/organic hybrid living composites for enhancing electron transfer flux and efficiency, clarifies the key technologies, excellent properties and breakthroughs in the construction of living hybrid materials, and points out their possible future environmental applications. Considering the diversity of BES and its large-scale application in the future, we have made the following brief outlook on the future development direction of this field.
1) Thinking based on EAB transformation design: First of all, under the premise of scientific, rational, safe and reliable, the EAB design is reconstructed to realize the refinement, standardization and decoupling of cell components.Strengthen the application of organelle function to break through the low efficiency of EET, improve the transfer flux of intracellular/extracellular electrons, continuously broaden the available carbon spectrum range, activate the metabolic pathway of EAB, and realize the top-down design and expression of target products.
2) Design thinking of living hybrid composites based on structure-activity relationship: it is necessary to start from two aspects of main components and fine accessories to realize multi-level assembly from the whole to the part. With the help of abundant bioinformatics and genome toolbox, and fine regulation and modification of the catalytic performance of environmentally friendly materials, more ideal microorganisms and advanced catalytic materials can be grafted and assembled to maximize the source of electrons that can be released.
3) Thinking of engineering application based on BES: Although it is not difficult to use cell factories to produce various compounds in the laboratory, the requirement of biochemical industry is to achieve scale enlargement under the premise of controllable cost. If the problems of cost and scale enlargement can not be solved, the significance of practical application will also be limited. Although many basic studies have been carried out to verify its scientific feasibility, more large-scale pilot tests are urgently needed to break through the transformation from laboratory to industrialization.
4) Based on the cross-integration and application expansion of materials science and other disciplines, the design and synthesis of advanced materials must be oriented to the pursuit of high precision, multi-function, intelligence and renewability. Let the idea of multi-disciplinary integration collide with the spark of wisdom and promote the intelligent upgrading of living biomaterials. At this stage, microbial/semiconductor hybrids have made significant breakthroughs in artificial carbon and nitrogen fixation. These successes will have important implications for how to combine effective BES in the future to promote grain production and harvest and achieve agricultural poverty alleviation. In particular, how to realize the transition and upgrading from tiny "super microorganisms" to large-scale "super factories" will become one of the important ways to improve crop yields in the future. Therefore, the integration of interdisciplinary key technologies to improve photosynthetic efficiency will provide an important theoretical basis and technical support for long-term and stable agricultural development in the future.

References

Publishing order | Descend order by publishing year | Descend order by cited within
[1]

Wang W K, Tang B, Liu J, Shi H J, Xu Q J, Zhao G H. Electrochimica Acta, 2019, 303: 268.
[2]

Kato S, Hashimoto K, Watanabe K. Environ. Microbiol., 2012, 14(7): 1646.
[3]

Zhuang L, Tang J, Wang Y Q, Hu M, Zhou S G. J. Hazard. Mater., 2015, 293: 37.
[4]

Wang J, Tian B Y, Bao Y H, Qian C, Yang Y R, Niu T Q, Xin B P. J. Hazard. Mater., 2018, 354: 250.
[5]

Chen Z, Wang Y P, Jiang X L, Fu D, Xia D, Wang H T, Dong G W, Li Q B. Sci. Total. Environ., 2017, 574: 1684.
[6]

Liu X B, Shi L, Gu J D. Biotechnol. Adv., 2018, 36(7): 1815.
[7]

Martinez C M, Alvarez L H. Biotechnol. Adv., 2018, 36(5): 1412.
[8]

van der Zee F P, Cervantes F J. Biotechnol. Adv., 2009, 27(3): 256.
[9]

Chen Z, Wang Y P, Xia D, Jiang X L, Fu D, Shen L, Wang H T, Li Q B. J. Hazard. Mater., 2016, 311: 20.
[10]

Ji X Y, Kang Y, Su Z G, Wang P, Ma G H, Zhang S P. ACS Sustainable Chem. Eng., 2018, 6(3): 3060.
[11]

Ren H, Tian H, Lee H S, Park T, Leung F C, Ren T L, Chae J. Nano Energy, 2015, 15: 697.
[12]

Andrieux C P, Dumas-Bouchiat J M, Saveant J M. J. Electroanal. Chem. Interfacial Electrochem., 1978, 87(1): 55.
[13]

Okamoto A, Hashimoto K, Nealson K H, Nakamura R. PNAS, 2013, 110(19): 7856.
[14]

Der B S, Machius M, Miley M J, Mills J L, Szyperski T, Kuhlman B. J. Am. Chem. Soc., 2012, 134(1): 375.
[15]

Kortemme T, Morozov A V, Baker D. J. Mol. Biol., 2003, 326(4): 1239.
[16]

Liu X B, Yu X B. ACS Energy Lett., 2020, 5(3): 867.
[17]

Su L, Ajo-Franklin C M. Curr. Opin. Biotechnol., 2019, 57: 66.
[18]

Sun J S, Li G, Wang Z H. Struct. Change Econ. Dyn., 2018, 47: 57.
[19]

Liu M, He Y E, Zhang H F, Su H, Zhang Z W. Energy, 2020, 197: 117189.
[20]

Kornienko N, Sakimoto K K, Herlihy D M, Nguyen S C, Alivisatos A P, Harris C B, Schwartzberg A, Yang P D. PNAS, 2016, 113(42): 11750.
[21]

Fang X, Kalathil S, Reisner E. Chem. Soc. Rev., 2020, 49(14): 4926.
[22]

Cestellos-Blanco S, Zhang H, Kim J M, Shen Y X, Yang P D. Nat. Catal., 2020, 3(3): 245.
[23]

Sahoo P C, Pant D, Kumar M, Puri S K, Ramakumar S S V. Trends Biotechnol., 2020, 38(11): 1245.
[24]

Roell M S, Zurbriggen M D. Curr. Opin. Biotechnol., 2020, 61: 102.
[25]

Dong G W, Wang H H, Yan Z Y, Zhang J, Ji X L, Lin M Z, Dahlgren R A, Shang X, Zhang M H, Chen Z. Sci. Total. Environ., 2020, 740: 140080.
[26]

Wei W, Sun P, Li Z, Song K, Su W, Wang B, Liu Y, Zhao J. Sci. Adv., 2018, 4(2): 1.
[27]

Sakimoto K K, Kornienko N, Yang P D. Acc. Chem. Res., 2017, 50(3): 476.
[28]

Novoselov K S, Geim A K, Morozov S V, Jiang D, Zhang Y, Dubonos S V, Grigorieva I V, Firsov A A. Science, 2004, 306(5696): 666.
[29]

Partoens B, Peeters F M. Phys. Rev. B, 2006, 74(7): 075404.
[30]

Wang J F, Yang S L, Guo D Y, Yu P, Li D, Ye J S, Mao L Q. Electrochem. Commun., 2009, 11(10): 1892.
[31]

Bagri A, Mattevi C, Acik M, Chabal Y J, Chhowalla M, Shenoy V B. Nat. Chem., 2010, 2(7): 581.
[32]

Chen C M, Zhang Q, Yang M G, Huang C H, Yang Y G, Wang M Z. Carbon, 2012, 50(10): 3572.
[33]

Yin X, Qiao S, Zhou J T, Tang X. Chem. Eng. J., 2016, 283: 160.
[34]

Zhuang L, Yuan Y, Yang G Q, Zhou S G. Electrochem. Commun., 2012, 21: 69.
[35]

Mi X, Huang G B, Xie W S, Wang W, Liu Y, Gao J P. Carbon, 2012, 50(13): 4856.
[36]

Zhou Y, Lu H, Wang J, Zhou J T, Leng X Y, Liu G F. J. Hazard. Mater., 2018, 356: 82.
[37]

Chen Z, Zhang J F, Han K Z, Yang C Y, Jiang X L, Fu D, Li Q B, Wang Y P. RSC Adv., 2017, 7(49): 31075.
[38]

Li Y X, Luo Q L, Li H, Chen Z, Shen L, Peng Y J, Wang H T, He N, Li Q B, Wang Y P. J. Chem. Technol. Biotechnol., 2019, 94(2): 446.
[39]

Ouyang K, Xie S, Zhao Y, Wang L C, Fang Q H. Ecol. Environ. Sci., 2015, 24(1): 106.
[40]

( 欧阳科, 谢珊, 赵雅, 王雷超, 方琪惠. 生态环境学报, 2015, 24(1): 106.)
[41]

Rouhani S, Rostami A, Salimi A, Pourshiani O. Biochem. Eng. J., 2018, 133: 1.
[42]

Luo Q, Chen Z, Li Y, Wang Y, Cai L, Wang L, Liu S, Wang Z, Peng Y, Wang Y. ACS Sustain. Chem. Eng., 2019, 7(14): 12611.
[43]

Lu A H, Li Y, Ding H R, Wang C Q. Bull. Mineral. Petrol. Geochem., 2018, 37(1): 1.
[44]

( 鲁安怀, 李艳, 丁竑瑞, 王长秋. 矿物岩石地球化学通报, 2018, 37(1): 1.)
[45]

Chen Z, Dong G W, Chen Y B, Wang H H, Liu S R, Chen Z J, Yang C H, Shang X, Dahlgren R. Chem. Eng. J., 2019, 372: 118.
[46]

Dong G W, Han R W, Pan Y J, Zhang C K, Liu Y, Wang H H, Ji X L, Dahlgren R A, Shang X, Chen Z, Zhang M H. J. Hazard. Mater., 2021, 401: 123362.
[47]

Chen Z, Dong G W, Gong L B, Li Q B, Wang Y P. Geomicrobiol. J., 2018, 35(7): 555.
[48]

Sakimoto K K, Wong A B, Yang P D. Science, 2016, 351(6268): 74.
[49]

Yang X G, Li Y, Lu A H, Yan Y H, Wang C Q, Wong P K. Sol. Energy Mater. Sol. Cells, 2011, 95(7): 1915.
[50]

Cheng L, Xiang Q J, Liao Y L, Zhang H W. Energy Environ. Sci., 2018, 11(6): 1362.
[51]

Sakimoto K K, Wong A B, Yang P. Science, 2016, 351(6268): 74.
[52]

Guo J L, Suástegui M, Sakimoto K K, Moody V M, Xiao G, Nocera D G, Joshi N S. Science, 2018, 362(6416): 813.
[53]

Chen X B, Mao S S. Chem. Rev., 2007, 107(7): 2891.
[54]

Ahmad Beigi A, Fatemi S, Salehi Z. J. CO2 Util., 2014, 7: 23.
[55]

Ijaz S, Ehsan M F, Ashiq M N, Karamat N, He T. Appl. Surf. Sci., 2016, 390: 550.
[56]

Li X, Liu H L, Luo D L, Li J T, Huang Y, Li H L, Fang Y P, Xu Y H, Zhu L. Chem. Eng. J., 2012, 180: 151.
[57]

Ye J, Yu J, Zhang Y Y, Chen M, Liu X, Zhou S G, He Z. Appl. Catal. B: Environ., 2019, 257: 117916.
[58]

Wang B, Xiao K M, Jiang Z F, Wang J F, Yu J C, Wong P K. Energy Environ. Sci., 2019, 12(7): 2185.
[59]

Huang S F, Tang J H, Liu X, Dong G W, Zhou S G. ACS Sustainable Chem. Eng., 2019, 7(18): 15427.
[60]

Guo J L, Suástegui M, Sakimoto K K, Moody V M, Xiao G, Nocera D G, Joshi N S. Science, 2018, 362(6416): 813.
[61]

Chen M, Zhou X F, Yu Y Q, Liu X, Zeng R J X, Zhou S G, He Z. Environ. Int., 2019, 127: 353.
[62]

Wang B, Zeng C P, Chu K H, Wu D, Yip H Y, Ye L Q, Wong P K. Adv. Energy Mater., 2017, 7(20): 1700611.
[63]

Wei W, Sun P Q, Li Z, Song K S, Su W Y, Wang B, Liu Y Z, Zhao J. Sci. Adv., 2018, 4(2): eaap9253.
[64]

Brown K A, Harris D F, Wilker M B, Rasmussen A, Khadka N, Hamby H, Keable S, Dukovic G, Peters J W, Seefeldt L C, King P W. Science, 2016, 352(6284): 448.
[65]

Zhang R T, He Y, Yi J, Zhang L J, Shen C P, Liu S J, Liu L F, Liu B H, Qiao L. Chem, 2020, 6(1): 234.
[66]

Ding Y C, Bertram J R, Eckert C, Bommareddy R R, Patel R, Conradie A, Bryan S, Nagpal P. J. Am. Chem. Soc., 2019, 141(26): 10272.
[67]

Sakpirom J, Kantachote D, Siripattanakul-Ratpukdi S, McEvoy J, Khan E. Chemosphere, 2019, 223: 455.
[68]

Wang B, Jiang Z F, Yu J C, Wang J F, Wong P K. Nanoscale, 2019, 11(19): 9296.
[69]

Sakimoto K K, Zhang S J, Yang P D. Nano Lett., 2016, 16(9): 5883.
[70]

Liu C, Sakimoto K K, ColÓn B C, Silver P A, Nocera D G. PNAS, 2017, 114(25): 6450.
[71]

Ji Z, Zhang H, Liu H, Yaghi O M, Yang P D. PNAS, 2018, 115(42): 10582.
[72]

Chen X Y, Feng Q Y, Cai Q H, Huang S F, Yu Y Q, Zeng R J, Chen M, Zhou S G. Environ. Sci. Technol., 2020, 54(17): 10820.
[73]

Jiang Z, Wang B, Yu J C, Wang J, Wong P K. Nano Energy, 2018, 46.
[74]

Dwyer D J, Kohanski M A, Collins J J. Curr. Opin. Microbiol., 2009, 12(5): 482.
[75]

Seifried H E, Anderson D E, Fisher E I, Milner J A. J. Nutr. Biochem., 2007, 18(9): 567.
[76]

Shekhah O, Liu J, Fischer R A, Wöll C. Chem. Soc. Rev., 2011, 40(2): 1081.
[77]

Liang K, Richardson J J, Doonan C J, Mulet X, Ju Y, Cui J W, Caruso F, Falcaro P. Angew. Chem. Int. Ed., 2017, 56(29): 8510.
[78]

Ji Z, Zhang H, Liu H, Yaghi O M, Yang P D. PNAS, 2018, 115(42): 10582.
[79]

Golchin J, Golchin K, Alidadian N, Ghaderi S, Eslamkhah S, Eslamkhah M, Akbarzadeh A. Artif. Cells Nanomed. Biotechnol., 2017, 45(6): 1069.
[80]

Du Q, Li T, Li N, Wang X. Environ. Sci. Tech. Let., 2017, 48(8): 345.
[81]

Yu Y Y, Wang Y Z, Fang Z, Shi Y T, Yong Y C. Nat. Commun., 2020, 11(1): 4087.
[82]

Brutinel E D, Gralnick J A. Appl. Microbiol. Biotechnol., 2012, 93(1): 41.
[83]

Han S, Gao X Y, Ying H J, Zhou C C. Green Chem., 2016, 18(8): 2473.
[84]

Li F, Li Y X, Cao Y X, Wang L, Liu C G, Shi L, Song H. Nat. Commun., 2018, 9(1): 1.
[85]

Yang Y, Ding Y Z, Hu Y D, Cao B, Rice S A, Kjelleberg S, Song H. ACS Synth. Biol., 2015, 4(7): 815.
[86]

Min D, Cheng L, Zhang F, Huang X N, Li D B, Liu D F, Lau T C, Mu Y, Yu H Q. Environ. Sci. Technol., 2017, 51(9): 5082.
[87]

Kouzuma A, Kasai T, Hirose A, Watanabe K. Front. Microbiol., 2015, 6: 609.
[88]

Meyer T E, Tsapin A I, Vandenberghe I, de Smet L, Frishman D, Nealson K H, Cusanovich M A, van Beeumen J J. OMICS: A J. Integr. Biol., 2004, 8(1): 57.
[89]

Beliaev A S, Klingeman D M, Klappenbach J A, Wu L, Romine M F, Tiedje J M, Nealson K H, Fredrickson J K, Zhou J. J. Bacteriol., 2005, 187(20): 7138.
[90]

Sander J D, Joung J K. Nat. Biotechnol., 2014, 32(4): 347.
[91]

Choi P S, Meyerson M. Nat. Commun., 2014, 5(1): 1.
[92]

Li J, Tang Q, Li Y, Fan Y Y, Li F H, Wu J H, Min D, Li W W, Lam P K S, Yu H Q. Environ. Sci. Technol., 2020, 54(6): 3599.
[93]

Wu J, Cheng Z H, Min D, Cheng L, He R L, Liu D F, Li W W. Environ. Sci. Technol., 2020, 54(6): 3306.
[94]

Cao Y X, Li X F, Li F, Song H. ACS Synth. Biol., 2017, 6(9): 1679.
[95]

Liu Q, Zhang H X, Huang X T. FEBS J., 2020, 287(4): 626.
[96]

Yang Y T, Chen J, Chen S S, Zhou S G. Acta Microbiol. Sin., 2020, 60(11): 2399.
[97]

( 杨钰婷, 陈瑾, 陈姗姗, 周顺桂. 微生物学报, 2020, 60(11): 2399.)
[98]

Whiteley M, Diggle S P, Greenberg E P. Nature, 2017, 551(7680): 313.

Funding

National Key R&D Program of China(2017YFB0403700)

Zhejiang Province Public Welfare Technology Application Research Project(LGF22E080002)

General Project of Scientific Research Program of Zhejiang Education Department(Y202045506)

National Natural Science Foundation of China(41807035)

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