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化学进展 2022, Vol. 34 Issue (2): 397-410 DOI: 10.7536/PC201221 前一篇   后一篇

• 综述 •

基于电活性菌群的生物电催化体系的有效构筑及其强化胞外电子传递过程的应用

赵聪媛1†, 张静3†, 陈铮1,2,3,*(), 李建1, 舒烈琳1, 纪晓亮1   

  1. 1 温州医科大学公共卫生与管理学院 浙江省流域水环境与健康风险研究重点实验室 温州 325035
    2 福建技术师范学院近海流域环境测控治理福建省高校重点实验室 福清 350300
    3 厦门大学嘉庚学院 环境与工程学院 漳州 363105
  • 收稿日期:2020-12-15 修回日期:2021-02-18 出版日期:2022-02-20 发布日期:2022-03-24
  • 通讯作者: 陈铮
  • 基金资助:
    “光健康”国家重点研发计划(2017YFB0403700); 浙江省公益技术应用研究项目(LGF22E080002); 浙江省教育厅一般科研项目(Y202045506); 国家自然科学基金项目(41807035)
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Effective Constructions of Electro-Active Bacteria-Derived Bioelectrocatalysis Systems and Their Applications in Promoting Extracellular Electron Transfer Process

Congyuan Zhao1†, Jing Zhang3†, Zheng Chen1,2,3(), Jian Li1, Lielin Shu1, Xiaoliang Ji1   

  1. 1 School of Public Health and Management, Zhejiang Provincial Key Laboratory of Watershed Science & Health, Wenzhou Medical University, Wenzhou 325035, China
    2 Fujian Provincial Key Lab of Coastal Basin Environment, Fujian Polytechnic Normal University, Fuqing 350300, China
    3 School of Environmental Science & Engineering, Tan Kah Kee College, Xiamen University, Zhangzhou 363105, China
  • Received:2020-12-15 Revised:2021-02-18 Online:2022-02-20 Published:2022-03-24
  • Contact: Zheng Chen
  • About author:
    † These authors contributed equally to this work
  • Supported by:
    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)

传统的电活性微生物(Electro-Active Bacteria,EAB)主导的胞外电子传递(Extracellular Electron Transfer,EET)效率较低,极大程度地限制了微生物电催化在环境及工业中的应用。为打破这一瓶颈,近年来多国科学家尝试开发先进的催化材料以强化生物电催化体系(Bio-Electrocatalytic System,BES)中的电子传递效能。借用材料科学、电微生物学及合成生物学技术等多学科手段尝试将传统无机催化材料及电活性微生物进行理性优化,将有望强化电子的传递通量和效率。这种优化升级推动了传统单一的无机催化材料向活体生物催化材料过渡,并有望朝着向更精细化、智能可控的先进材料升级改造,也为拓展先进材料的规模化应用提供更有利的技术支撑。本文对现阶段几种强化EET的有效手段用以有效构筑BES展开综述,包括了微生物-石墨烯改性复合材料、原位杂化光催化半导体材料自组装微生物、核/壳装配的生物材料及接种基因工程菌等内容,最后总结了微生物活体生物材料所面临的挑战及未来在环境应用中所面临的机遇。

关键词： 胞外电子传递, 生物电催化体系, 半导体材料, 合成生物学, 电子流通量

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

Key words: extracellular electron transfer(EET), bio-electrocatalytic system(BES), semiconducting materials, synthetic biology, electron flux
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图1 HNQ-PVA-GO复合材料回收去除Cr(Ⅵ)的效果对比(a),重复循环三次后回收得到的HNQ-PVA-GO实物图(b)及复合材料强化还原去除Cr(Ⅵ)的机理图(c)[38]
Fig. 1 Comparison of the removals of Cr(Ⅵ) resulting from the addition of HNQ-PVA-GO composite in three reaction cycles (a), the physical picture of recovered HNQ-PVA-GO after three reaction cycles (b) and schematic representation of proposed Cr(Ⅵ) reduction mechanism by S. xiamenensis in the presence of HNQ-PVA-GO composite (c)[38]. Copyright, 2019, Wiley
图2 石墨烯与S. xiamenensis接枝的活体复合材料强化还原去除废水中Cr(Ⅵ)机理图[41]
Fig. 2 Mechanism of enhanced bioreduction of Cr(Ⅵ) in wastewater by using living GO-S. xiamenensis composited biomaterial[41]. Copyright 2019, ACS
图3 半导体材料CdS在光催化下产生光电子-空穴的环境过程及应用(a)[48],将半导体材料的光电还原与微生物胞外电子亲密耦合强化EET的设计思路 (b),基于CdS纳米粒子原位杂化自组装到微生物表面形成生物杂化体的构筑(c)[23],以胞外H2O和CO2为底物,生物杂化体可通过Wood-Ljungdahl途径还原获得可再生燃料、药物、高附加值化学品及生物聚合物等(d)[23,25,49,50]
Fig. 3 Environmental process and application of semiconducting CdS-based photocatalysis (a)[48], a design of specific bio-system to promote intimate coupling of microbial and photoelectrochemical processes (b), the construction of biohybrids through biologically precipitating CdS nanoparticles on the surface of microbes (c)[23], and enhanced photosynthetic production of renewable fuels, pharmaceutical, value-added chemicals and biopolymer from extracellular CO2 and H2O via the Wood-Ljungdahl pathway (d)[23,25,49,50]
表1 光催化半导体自组装微生物杂化体的环境应用
Table 1 Environmental applications of biohybrids by self-assembling photocatalytic semiconductor.
Application Biohybrid Illumination Remarkable results ref
Decolorization of
methyl orange		 G. sulfurreducens-CdS QDs
biohybrid		 LED
3.07±0.14 mW/cm2		 Decolorization rate of biohybrid was 6-fold that of control group
Decolorization rate of the biohybrid was up to 100% after 3 h		 57
Conversion of carbon dioxide to methane M. barkeri-CdS QDs
biohybrid		 UV
1.0±0.14 mW/cm2		 The generation rate of methane is 0.19 mol/h
1.5-fold of mcrA gene copies compared to that of control were increased in biohybrid		 55
Denitriffication of
nitrate to generate nitrous oxide		 T.denitrificans-CdS QDs
biohybrid		 UV
3.07±0.14 mW/cm2		 Reduction quantum efficiency of nitrate was up to 2.0%
Denitrification rate was more than 70% higher than that of control group		 59
Hydrogen generation E. coli-CdS QDs biohybrid LED
2000 W/m2		 >30% hydrogen production was increased than that of control group
Appreciated quantum efficiency (~9.59%) was obtained under visible light radiation		 60
Hydrogen generation E. coli-CdS NPs biohybrid Xenon lamp
350 W		 Hydrogen production efficiency was twice than that of control group
Hydrogen was continuously produced within 96 h under natural aerobic condition		 61
Dinitrogen reduction to ammonia Nitrogenase MoFe
protein-CdS QDs biohybrid		 LED
3.5 mW/cm2		 Biological nitrogen fixation rate was up to 64% in biohybrids
Biological nitrogen fixation rate was up to 64% in biohybrids		 62
Synthesis of acetic acid from carbon dioxide Moorella thermoacetica-
CdS NPs biohybrid		 LED
405 nm		 CdS nanoparticles stimulated the activity of IMPDH
Glycolysis and TCA cycle processes were activated		 63
Synthesis of acetic acid from carbon dioxide Moorella thermoacetica-
CdS NPs biohybrid		 Violet LED with photon flux of
5×1018 cm-2/s		 More than 90% of CO2 was converted into acetic acid in biohybrids
Biohybrids exhibited nearly 10-fold quantum yields than that of averages determined for plants and algae		 46
Conversion of DHS to SA Saccharomyces cerevisiae-InP biohybrid LED
5.6 mW/cm2		 SA/DHS conversion rate was increased by 35-fold than control group
Nearly 24-fold of SA yield was accumulated in biohybrids than control group		 58
Biological nitrogen fixation R. palustris-CdS biohybrid LED
8 mW/cm2		 Photosynthetic efficiency was increased by 6.73%
Accumulated biomass was 2-fold of control group		 56
Light-driven ethylene and PHB synthesis from carbon dioxide Cupriavidus
necator-CdS@ZnS QDs biohybrid		 UV
365 nm		 Yield C2H4 in of biohybrids was 15-fold higher than that of control group
Yield of PHB obtained from biohybrids was 1.5-fold of control group		 64
Application Biohybrid Illumination Remarkable results ref
Light-driven ammonia and hydrogen synthesis from nitrogen and water Azotobacter vinelandii-CdS@ZnS biohybrid UV
400 nm		 Hydrogen production was 19-fold higher than that of control group
Ammonia production was 3-fold higher than that of control group		 64
Conversion of nitrogen to ammonia-nitrogen R.palustris-CdS NPs
biohybrid		 Microaerobic-light
3000 lx		 The activity of cysteine desulfhydrase was not affected by nitrogenase cofactors
CdS NPs up-regulated the expression of nitrogen fixation gene (vnfG) by 2.3 times		 65
Enhanced carbon dioxide reduction and organic chemical production R.palustris-CdS NPs
biohybrid		 LED
8 mW/cm2		 The amounts of PHB, solid biomass and carotenoids were increased by 39%, 17% and 35%, respectively
Photosynthetic efficiency was increased from 4.31% to 5.98%		 66
Oxygenic photosynthesis of acetic acid from carbon dioxide TiO2-MnPc + Moorella
thermoacetica-CdS NPs
biohybrid		 Xenon lamp
75 W		 Coupled biohybrid system resulted in an increased production of acetic acid than that of biohybrid alone
MnPc stimulated the catalytic activity of reducing cysteine		 67
Synthesis of acetic acid from carbon dioxide M. thermoacetica-CdS
biohybrid		 Xenon lamp
75 W		 Rate of photoelectrons transferring was positively correlated with the activity of hydrogenase
Quantum efficiency of acetic acid synthesis was positively correlated with the activity of hydrogenase within first 24 h		 20
Conversion of nitrogen to ammonia-nitrogen Xanthobacter autotrophicus-CoPi biohybrid sunlight Conversion of CO2 into organic carbon was markedly increased in Calvin Cycle
Reduction of N2 into ammonia was apparently improved (>40% of reduction efficiency)		 68
Synthesis of acetic acid from carbon dioxide Morella thermoacetica-MOF biohybrid Xenon lamp
75W		 Microbial mortality was decreased by 20%
Time for synthesizing acetic acid was shortened by 50%		 69
Denitriffication of
nitrate to generate
nitrogen		 Thiobacillus denitrificans-CdS@Mn3O4 biohybrid Xenon lamp
100 mW/cm2		 Nitrate reduction rate was increased by 28%
No lag period was existed in photoelectric denitrification		 70
Hydrogen generation E. coli-AglnS2/In2S3
biohybrid		 LED
1400 W/m2		 More than 1660 μmol of hydrogen was accumulated
within 3 h quantum efficiency was reached to 3.3%		 71
图4 M. thermoacetica-MOF包裹体系的设计与构筑:单层MOF的设计与合成(a); M. thermoacetica 在伸展及二分裂繁殖时,MOF仍可以原位紧紧地包裹在菌体表面(b); 在分子界面层面上,MOF的无机团簇和菌体细胞壁上的磷酸基团之间能形成多价配位键(c); ROS被细胞表面包裹的MOF所猝灭(d)[76]
Fig. 4 Construction of a M. thermoacetica-MOF wrapping system: the design and synthesis of monolayer MOF (a), monolayer MOF spontaneously wraps around M. thermoacetica, allowing for elongation and separation of cells (b), MOF tightly wraps the surface of bacteria cell through multivalent coordination bonds form between the inorganic clusters of MOF and the phosphate moieties of teichoic acid on cell wall (c), and decomposition of ROS by MOF coating on cell surface (d)[76]. Copyright, 2018, PNAS
图5 添加Mn3O4涂层修饰Thiobacillus denitrificans-CdS生物杂化体在光照条件下监测到·OH (a)、H2O2 (b)、N O 3 --N (c)与N2O-N (d)浓度变化。其中,在光照条件下ROS立即被Mn3O4纳米酶猝灭俘获 (e),而Mn3O4纳米酶-CdS涂层在细胞表面与液相层中间形成一个保护壳使菌体免受ROS的侵蚀 (f)[70]
Fig. 5 Concentrations of ·OH (a), H2O2 (b), N O 3 --N (c) and N2O-N (d) in T. denitrificans-CdS@Mn3O4 under illumination. Therein, ROS from neighboring CdS nanoparticles is immediately decomposed by Mn3O4 nano-enzyme (e), and Mn3O4-CdS could act as a separating shell for T. denitrificans to prevent from the damage by ROS (f)[70]. Copyright 2020, ACS
图6 “S捕集器”(a)及“SP捕集器”(b)在S. oneidensis原位组装的示意图;在MFC中接种不同菌种对应的输出电流(c),non-turnover(d)和turnover(e)条件下的循环伏安曲线;S. oneidensis@SP与电极之间的电子转移途径(f)、不同MFC对应的电化学阻抗谱曲线(g)及功率输出曲线(h)[79]
Fig. 6 Schematic illustrations for the assembly of “S collector” (a) and “SP collector” (b) on a S. oneidensis cell are depicted. The performance of current output (c) and CV curves of MFCs that were incubated with different strains under non-turnover (d) and turnover (e) conditions are profiled. Therein, the electron transfer pathway (f) for S. oneidensis@SP cell with an electrode is proposed. In addition, the electrochemical impedance spectroscopy curves (g) and power output curves (h) of MFCs that were incubated with different strains are profiled[79]. Copyright 2020, Nature Publishing Group
图7 为提升EET效率,可通过从头合成路径、补救合成路径及通用合成路径来强化S. oneidensis MR-1中NAD+的生物合成。分别监测接种不同基因重组的工程菌的MFC体系中的最大电压输出(b)及乳酸盐消耗(c)以评估EET效率[82]
Fig. 7 To improve EET rate, modular design to enhance NAD+ biosynthesis in S. oneidensis MR-1 is conducted through three modules (i.e., de novo biosynthesis, salvage biosynthesis and universal biosynthesis) (a). The voltage output (b) and lactate consumption (c) in MFCs that were incubated with different S. oneidensis recombinant strains are monitored to evaluate EET performance[82]. Copyright 2018, Nature Publishing Group
图8 基于优化基因回路来定向强化电活性细菌的EET设计思路(a),以CRISPR-ddAsCpf1平台策略以强化S. oneidensis MR-1胞外电子流定向传递的概念图(b);以fccA、dmsE及cctA功能基因定向表达的S. oneidensis MR-1还原降解甲基橙的速率常数(c)及其动力学曲线(d),dmsE功能基因定向表达的S. oneidensis MR-1的Cr(Ⅵ)还原速率常数(e)及其动力学曲线(f)[90]
Fig. 8 An elucidation of the design to enhance EET via optimizing genetic circuit of ERB (a), a diagram of enhanced tuning electron flux of S. oneidensis MR-1 by CRISPR-ddAsCpf1-based rediverting strategy, the rate constant (c) and associated kinetic curves of MO biodegradation by S. oneidensis MR-1 that was overexpressed with fccA, dmsE and cctA (d), and the normalized reaction constant of the Cr(Ⅵ) bioreduction (e) and associated kinetic curves by S. oneidensis MR-1 that was overexpressed with dmsE (f)[90], respectively. Copyright 2020, ACS Group
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