Elsevier

Bioresource Technology

Volume 271, January 2019, Pages 439-448
Bioresource Technology

Review
Bidirectional extracellular electron transfers of electrode-biofilm: Mechanism and application

https://doi.org/10.1016/j.biortech.2018.09.133Get rights and content

Highlights

  • Comprehensive analysis of the bidirectional EET of a single electrode-biofilm.

  • Summary of current study using pure culture capable of bidirectional EET.

  • Side-by-side discussing of the application and challenges of bidirectional EET.

Abstract

The extracellular electron transfer (EET) between microorganisms and electrodes forms the basis for microbial electrochemical technology (MET), which recently have advanced as a flexible platform for applications in energy and environmental science. This review, for the first time, focuses on the electrode-biofilm capable of bidirectional EET, where the electrochemically active bacteria (EAB) can conduct both the outward EET (from EAB to electrodes) and the inward EET (from electrodes to EAB). Only few microorganisms are tested in pure culture with the capability of bidirectional EET, however, the mixed culture based bidirectional EET offers great prospects for biocathode enrichment, pollutant complete mineralization, biotemplated material development, pH stabilization, and bioelectronic device design. Future efforts are necessary to identify more EAB capable of the bidirectional EET, to balance the current density, to evaluate the effectiveness of polarity reversal for biocathode enrichment, and to boost the future research endeavors of such a novel function.

Introduction

Microbial electrochemical technology (MET) employs electrochemical active bacteria (EAB) as the catalysts for at least one of the two electrodes (anode and cathode) in an electrochemical cell to conduct the oxidation and reduction reactions (Zou and He, 2018). Microbial fuel cell (MFC) is the original and fundamental case of MET, which shows the promising of directly electric energy recovery from the degradation of pollutants in wastewater. Within the past decade, the steady-state volumetric power density of miniaturized MFCs was reported to over 10,000 W/m3 (Ren et al., 2016). Meanwhile, the scale of MFC reactors have also advanced from the bench scale with couples to dozens of milliliters, to the pilot scale with a maximum volume of 250 L in an individual reactor (Feng et al., 2014), and a total volume of 1000 L in a modularized system (Liang et al., 2018). However, the practical application of MFCs is largely restricted by the inevitable diminished power in large scales when feeding with actual wastewater with a poor conductivity and a limited buffer ability, which makes it generally insufficient to justify the high capital cost (Jiang et al., 2018b, Jiang and Zeng, 2018, Logan et al., 2015, Wu et al., 2016). With the integration of microbiology, electrochemistry, materials science, and many other research areas of relevance together, the MET recently has advanced as such a flexible platform that dozens of functions have been invented and explored (Champigneux et al., 2018, Choudhury et al., 2017, Wang and Ren, 2013, Yu et al., 2018b). Among these, the emerging MET without the requirement for large numbers of electrode assemblies or high current/power density outputs, such as electro-fermentation, electric syntrophy, electro-stimulation, microbial photo-electrosynthesis, and environmental biosensing, is recently highlighted by some outstanding reviews (Jiang et al., 2018c, Kracke et al., 2018, Sasaki et al., 2018). In addition, the synergy between MET and conventional wastewater treatment processes (e.g., anaerobic digestion (AD), membrane bioreactor (MBR), constructed wetland (CW), capacitive deionization (CDI), and Fenton process) has shown the promising of practical application in large scale, rather than using the MET as a standalone technology (Li and Yu, 2016, Tee et al., 2016, Xu et al., 2015).

Despite the variation in constructions and purposes, the basis of MET is the unique electrical communication, i.e., extracellular electron transfer (EET) process, between the EAB and electrodes. The EET process could be divided into the outward EET (from the EAB to electrode) and the inward EET (from the electrode to EAB), according to the direction. The outward EET is generally conducted at the bioanode, where substrate like carbohydrate is served as the electron donor while the electrode is served as the electron acceptor, and it could be adopted for the production of electricity, bioremediation, and wastewater treatment (Choudhury et al., 2017, Pandey et al., 2016). In contrast, the inward EET is generally conducted at the biocathode, where the electrode is served as the solid electron donor while different types of final electron donors could be used for various applications, including the production of valuable products, wastewater treatment, and heavy metal or nutrient recovery (Kracke et al., 2015, Lovley and Nevin, 2011, Rosenbaum et al., 2011, Tremblay et al., 2017, Yu et al., 2018b).

Recently, the using of a single biofilm-electrode to comparatively understand the mechanism of the bidirectional EET process, and explore its various function in water-energy nexus has received a growing research interest. Biofilm-electrode with the bidirectional EET process shares unique community structure, operational mode, and multiple functions, which all distinguish it from conventional cases where only the unidirectional EET is considered (Kumar et al., 2017). There are some excellent reviews focused on the EAB in the anode (Kumar et al., 2016, Logan, 2009), the electroactive autotrophic in the cathode (Rosenbaum et al., 2011, Tremblay and Zhang, 2015), the using of electrode modification to boost the outward EET (Sonawane et al., 2017, Yazdi et al., 2016), the mechanism of EET conducted separately by bioanode and biocathode (Choi and Sang, 2016, Kumar et al., 2017, Nealson and Rowe, 2016), and also the assessment of electron donor (Pandey et al., 2016), and acceptors (Ucar et al., 2017) in MET. The objectives of this review are, for the first time, to provide an overview of current status of research in biofilm-electrode with the bidirectional EET process, and to analyze the challenges and perspectives of this biotechnology. Being more specific and focused, this review is mainly limited to investigate and elucidate: (1) the EAB in pure culture reported with the capability of bidirectional EET; (2) the problems and applications of bidirectional EET using electrode-biofilm without polarity reversal; (3) the applications of bidirectional EET with polarity reversal for pollutant removal, biotemplated material development, and bioelectronic device design; (4) the challenges faced by the practical application of bidirectional EET in future research endeavors and also the promising technical solutions.

Section snippets

EET process and involved EABs

Although some debates in this research field still exist, the mechanisms of the outward EET are well studied, whereas, while the intricacies of inward EET has not been fully elucidated yet (Nealson and Rowe, 2016). In this section, the outward EET and inward EET are briefly introduced, and then those EABs capable of bidirectional EET and their various applications are summarized.

Bidirectional EET without polarity reversal

There are only few microorganisms tested in pure culture with the capability of bidirectional EET, however, the mixed culture based bidirectional EET offers great prospects for pollutant removal, biotemplated material development, and bioelectronic device design. Actually, the problems and applications of bidirectional EET are directly associated with where polarity reversal is applied to a MET based device. In this section, the bidirectional EET without polarity reversal will be firstly

Bidirectional EET with polarity reversal once only

The operational mode of polarity reversal once only in microbial electrolysis cell (MEC) reactors is generally achieved by first enriching a bioanode in anodic condition with an outward EET process, followed by direct inversion of the bioanode to function as a biocathode, providing a cathodic condition with an inward EET process. The polarity reversal can be achieved by switching the setting of electrode potentials and/or the feeding of substrates. The main goals of polarity reversal once only

Periodic polarity reversal (PPR)

In the operational mode of periodic polarity reversal (PPR), the roles of bioanode and biocathode is switched periodically due to the capability of bidirectional EET of a same piece of biofilm-electrode. Typically, electrode reactions with products such as easily separated gases (hydrogen, nitrogen, and methane) and water, are suitable for the operational mode of periodic polarity reversal. With such periodic polarity reversal (Fig. 5), the pH degradant across the ion exchange membrane can be

Challenges and future prospects

The characters of bidirectional EET of a same biofilm-electrode provide a unique opportunity to elucidate various routes of EET pathways. The bidirectional EET of a single electrode-biofilm also holds great prospects for pollutant removal, biotemplated electrode material development, and bioelectronic design. However, some biotechnological barriers are yet to be solved for a widely utilization of such a unique bidirectional EET capability in the advanced MET platform.

There is a need to identify

Conclusions

This review mainly emphasizes on the fundamentals and applications of bidirectional EET of a single electrode-biofilm. The characters of bidirectional EET of a same biofilm-electrode provide a unique opportunity to elucidate the EET mechanism, despite that the microorganisms tested in pure culture with bidirectional EET are so limited. The bidirectional EET carries great prospects for biocathode enrichment, pollutant complete mineralization, biotemplated material development, pH stabilization,

Acknowledgments

This work was supported by the National Science Foundation of China (51478447, 51878175) and Central Guidance on the Development of Local Science and Technology (Fujian, 2017L3003).

References (150)

  • E. Croese et al.

    Influence of setup and carbon source on the bacterial community of biocathodes in microbial electrolysis cells

    Enzyme Microb. Technol.

    (2014)
  • L. Darus et al.

    Fully reversible current driven by a dual marine photosynthetic microbial community

    Bioresour. Technol.

    (2015)
  • Y. Feng et al.

    A horizontal plug flow and stackable pilot microbial fuel cell for municipal wastewater treatment

    Bioresour. Technol.

    (2014)
  • E.G. Ferreira Mercuri et al.

    Energy by microbial fuel cells: scientometric global synthesis and challenges

    Renew. Sustain. Energy Rev.

    (2016)
  • Q. Fu et al.

    Bioelectrochemical analyses of a thermophilic biocathode catalyzing sustainable hydrogen production

    Int. J. Hydrogen Energy

    (2013)
  • T.D. Harrington et al.

    Neutral red-mediated microbial electrosynthesis by Escherichia coli, Klebsiella pneumoniae, and Zymomonas mobilis

    Bioresour. Technol.

    (2015)
  • R.M. Hartline et al.

    Substrate and electrode potential affect electrotrophic activity of inverted bioanodes

    Bioelectrochemistry

    (2016)
  • J. Houghton et al.

    Supercapacitive microbial fuel cell: characterization and analysis for improved charge storage/delivery performance

    Bioresour. Technol.

    (2016)
  • T. Jafary et al.

    A comprehensive study on development of a biocathode for cleaner production of hydrogen in a microbial electrolysis cell

    J. Clean. Prod.

    (2017)
  • Y. Jiang et al.

    Bioelectrochemical systems for simultaneously production of methane and acetate from carbon dioxide at relatively high rate

    Int. J. Hydrogen Energy

    (2013)
  • Y. Jiang et al.

    Enhancing the response of microbial fuel cell based toxicity sensors to Cu (II) with the applying of flow-through electrodes and controlled anode potentials

    Bioresour. Technol.

    (2015)
  • Y. Jiang et al.

    Periodic polarity reversal for stabilizing the pH in two-chamber microbial electrolysis cells

    Appl. Energy

    (2016)
  • Y. Jiang et al.

    Expanding the product spectrum of value added chemicals in microbial electrosynthesis through integrated process design—a review

    Bioresour. Technol.

    (2018)
  • Y. Jiang et al.

    A novel microbial fuel cell sensor with biocathode sensing element

    Biosens. Bioelectron.

    (2017)
  • Y. Jiang et al.

    Microbial fuel cell sensors for water quality early warning systems: fundamentals, signal resolution, optimization and future challenges

    Renew. Sustain. Energy Rev.

    (2018)
  • Y. Jiang et al.

    A novel microbial fuel cell sensor with a gas diffusion biocathode sensing element for water and air quality monitoring

    Chemosphere

    (2018)
  • F. Kracke et al.

    Balancing cellular redox metabolism in microbial electrosynthesis and electro fermentation – a chance for metabolic engineering

    Metab. Eng.

    (2018)
  • R. Kumar et al.

    Exoelectrogens: Recent advances in molecular drivers involved in extracellular electron transfer and strategies used to improve it for microbial fuel cell applications

    Renew. Sustain. Energy Rev.

    (2016)
  • D.-J. Lee et al.

    Treatment and electricity harvesting from sulfate/sulfide-containing wastewaters using microbial fuel cell with enriched sulfate-reducing mixed culture

    J. Hazard. Mater.

    (2012)
  • W. Li et al.

    Simultaneous pH self-neutralization and bioelectricity generation in a dual bioelectrode microbial fuel cell under periodic reversion of polarity

    J. Power Sour.

    (2014)
  • W.-W. Li et al.

    Advances in energy-producing anaerobic biotechnologies for municipal

    Engineering

    (2016)
  • P. Liang et al.

    One-year operation of 1000-L modularized microbial fuel cell for municipal wastewater treatment

    Water. Res.

    (2018)
  • D.R. Lovley et al.

    A shift in the current: new applications and concepts for microbe-electrode electron exchange

    Curr. Opin. Biotechnol.

    (2011)
  • W. Miran et al.

    Chlorinated phenol treatment and in situ hydrogen peroxide production in a sulfate-reducing bacteria enriched bioelectrochemical system

    Water Res.

    (2017)
  • M.T. Noori et al.

    Biofouling inhibition and enhancing performance of microbial fuel cell using silver nano-particles as fungicide and cathode catalyst

    Bioresour. Technol.

    (2016)
  • P. Pandey et al.

    Recent advances in the use of different substrates in microbial fuel cells toward wastewater treatment and simultaneous energy recovery

    Appl. Energy

    (2016)
  • N. Pous et al.

    Bidirectional microbial electron transfer: switching an acetate oxidizing biofilm to nitrate reducing conditions

    Biosens. Bioelectron.

    (2016)
  • F.J. Rawson et al.

    Mediated electrochemical detection of electron transfer from the outer surface of the cell wall of Saccharomyces cerevisiae

    Electrochem. Commun.

    (2012)
  • H. Ren et al.

    Regulating the respiration of microbe: a bio-inspired high performance microbial supercapacitor with graphene based electrodes and its kinetic features

    Nano Energy

    (2015)
  • M. Rimboud et al.

    Different methods used to form oxygen reducing biocathodes lead to different biomass quantities, bacterial communities, and electrochemical kinetics

    Bioelectrochemistry

    (2017)
  • M. Rosenbaum et al.

    Cathodes as electron donors for microbial metabolism: which extracellular electron transfer mechanisms are involved?

    Bioresour. Technol.

    (2011)
  • R.A. Rozendal et al.

    Towards practical implementation of bioelectrochemical wastewater treatment

    Trends Biotechnol.

    (2008)
  • C. Santoro et al.

    Self-powered supercapacitive microbial fuel cell: the ultimate way of boosting and harvesting power

    Biosens. Bioelectron.

    (2016)
  • K. Sasaki et al.

    Electrochemical biotechnologies minimizing the required electrode assemblies

    Curr. Opin. Biotechnol.

    (2018)
  • J.M. Sonawane et al.

    Recent advances in the development and utilization of modern anode materials for high performance microbial fuel cells

    Biosens. Bioelectron.

    (2017)
  • T.S. Song et al.

    Graphene/biofilm composites for enhancement of hexavalent chromium reduction and electricity production in a biocathode microbial fuel cell

    J. Hazard. Mater.

    (2016)
  • L. Soussan et al.

    Electrochemical reduction of CO2 catalysed by Geobacter sulfurreducens grown on polarized stainless steel cathodes

    Electrochem. Commun.

    (2013)
  • L. Soussan et al.

    The open circuit potential of Geobacter sulfurreducens bioanodes depends on the electrochemical adaptation of the strain

    Electrochem. Commun.

    (2013)
  • E. Atci et al.

    A fumarate microbiosensor for use in biofilms

    J. Electrochem. Soc.

    (2016)
  • F. Aulenta et al.

    Linking bacterial metabolism to graphite cathodes: electrochemical insights into the h2-producing capability of desulfovibrio sp

    ChemSusChem

    (2012)
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