Review article
Genetic engineering strategies for performance enhancement of bioelectrochemical systems: A review

https://doi.org/10.1016/j.seta.2021.101332Get rights and content

Highlights

  • Various types of BES can be used for sustainable energy requirements.

  • Genetic and metabolic constraint of microbial catalyst limits BES application.

  • Electroactive microbes possess direct and indirect electron transfer mechanisms.

  • Genetic modification of microbial catalyst can improve BES performance.

Abstract

Bioelectrochemical system (BES) is a microbial metabolism based innovative technology that offers sustainable energy solution. Electroactive microbes possess unique cellular features for direct and indirect extracellular electron transfer (EET) to electrodes in BES. Genetic engineering paves the path to augment low EET rate and limited metabolic capacity of native electroactive microbes; or to confer EET ability onto non-electroactive microbes. A critical analysis of such gene modification strategies is required to explore its role in establishing efficient and promising BES. In this review, the five major types of BES are briefly discussed based upon its downstream application. Further, the EET mechanisms of model electroactive microbes are summarized with their gene modification targets; for enhancing EET and metabolic capacity. The key findings of this review are: cytochromes, pilin and electron shuttles are the major gene targets for improving EET rate, and metabolic genes are targeted for H2 and valuable product synthesis. BES application where genetic engineering strategies have been less explored and holds potential have been identified. Finally, the critical review and the future perspective of BES are summarized.

Introduction

Depletion of fossil fuels causes energy shortage and environmental problems, suggesting establishing sustainable alternative energy sources. A bioelectrochemical system (BES) is an innovative technology that provides an inexpensive and ecofriendly approach to meet the future energy needs [1]. In fact, the scope of BES goes beyond just energy production to wastewater treatment, bioremediation, production of industrially important chemicals, biosensors and resource recovery [2], [3].

BES can be broadly categorized into various types (microbial fuel cell (MFC), microbial electrolysis cell (MEC), microbial desalination cell (MDC), microbial electrosynthesis cell (MESC) and microbial solar cell (MSC)) depending on their application. However, scalable performance remains the bottleneck towards commercial application of BES. Innovative BES reactor configuration, electrode modification, isolation of novel electroactive microbes and genetic engineering of microbial catalyst are studied to address this problem. Several research groups have investigated on electron transfer pathways of model electroactive microbes and on synthetic biology strategies for enhancing extracellular electron transfer (EET) of microorganisms [4], [5], [6], [7], [8]. Physical, chemical and genetic engineering strategies have been summarized for improving the metabolic functionalities of electroactive microbes in MFC and MESC [9]. Extensive survey of literature revealed that most of the reports focused only on the application of synthetic biology for one specific type of BES i.e. MFC or one particular type of genetic modification strategy. Further, the reactor design of BES, modification of electrode material, various separation membrane and novel cathodic catalyst have been discussed in the recent reviews [10], [11], [12], [13]. Since, the scope of BES is much more than harvesting electrical energy alone in MFC, a critical review on the BES type specific genetic engineering strategies is needed to identify the specific gene modification targets for the development of particular type of BES.

This review will briefly discuss various types of BES and EET pathways of model electroactive microbes; then critically review the genetic engineering approaches for enhancement of BES performance. The main objective of this review is to highlight successful gene modification strategies for a particular type of BES application and limitations of such strategies. BES application where genetic engineering strategies have been less explored and holds potential have been identified. By discussing the advances of gene modification strategies for a specific type of BES application herein, the future prospects of genetic engineering strategies in the development of specific BES type is discussed.

Section snippets

Bioelectrochemical system

By definition, BES is an “electrochemical device that uses microbial catalyst capable of electron exchange with electrode”. Microbes that can release electrons to extracellular acceptors are exoelectrogens and microbes that accept electrons from external donors are electrotrophs [14]. Fig. 1 illustrates the schematic representation of BES reactor along with microbe-electrode interaction. Anodic chamber consists of exoelectrogenic microbes that can oxidize the organics in anolyte and cathodic

Extracellular electron transfer in electroactive microbes

The first ever report on electrical activity of microbes came from measuring the galvanic potential generated by two microbial species i.e., Saccharomyces cerevisiae and Escherichia coli while degrading organic substrates [29]. Although the idea of generating electricity through microbial metabolism is more than 100 years old, any development in BES came only after the discovery of electroactive microbes capable of generating viable current densities. Shewanella and Geobacter species were

Genetically engineered bioelectrochemical system

The limitations of microbial catalyst in BES have been discussed in the above section. Strategies for enhancement of BES performance like physical and chemical pretreatment of microbial cells, entrapment of electroactive microbes over electrode surface and application of electrochemical potential or magnetic field for enriching electroactive communities have been widely adopted [9]. Genetic engineering makes it possible to augment EET rate of microbial catalyst in BES by editing genes to

Critical review

Genetic engineering has been extensively used for studying the EET mechanism of model electroactive microbes and to identify the key components of EET. Multiple genes have been targeted by genetic engineering to either enhance EET or augment the metabolic capacity of the microbial catalyst in BES. It is essential to identify the promising gene modification targets based on BES application and the microbial catalyst used in specific BES. The promising strategies for different type of BES along

Conclusion and future perspective

Understanding the EET pathways of model electroactive microbes have enabled researchers to successfully overexpress these pathways in wild type electroactive microbes as well as extend this property to industrially important non-electroactive microbes using synthetic biology approaches. The metabolic capacity of the microbial catalyst in BES has been extrapolated to make microbial factories for novel substrate oxidation or product synthesis. However, all the successful genetic engineering

CRediT authorship contribution statement

Parini Surti: Conceptualization, Data curation, Writing - original draft. Suresh Kumar Kailasa: Supervision, Writing - review & editing. Arvind Kumar Mungray: Funding acquisition, Supervision, Writing - review & editing.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgement

Grant received from SERB-DST, Government of India (File No. EEQ/2016/000802) to carry out this work is duly acknowledged.

References (107)

  • G. Kumar et al.

    A review on bio-electrochemical systems (BESs) for the syngas and value added biochemicals production

    Chemosphere

    (2017)
  • Z. Jiang et al.

    Degradation of organic contaminants and steel corrosion by the dissimilatory metal-reducing microorganisms Shewanella and Geobacter spp

    Int Biodeterior Biodegrad

    (2020)
  • G. Reguera et al.

    The electrifying physiology of Geobacter bacteria, 30 years on

    Adv Microb Physiol

    (2019)
  • F. Wang et al.

    Structure of Microbial Nanowires Reveals Stacked Hemes that Transport Electrons over Micrometers

    Cell

    (2019)
  • A. Venkataraman et al.

    Quorum sensing regulates electric current generation of Pseudomonas aeruginosa PA14 in bioelectrochemical systems

    Electrochem Commun

    (2010)
  • K.D. Bewley et al.

    Multi-heme proteins: Nature’s electronic multi-purpose tool

    Biochim Biophys Acta - Bioenerg

    (2013)
  • J. Liu et al.

    Chassis engineering for microbial production of chemicals: from natural microbes to synthetic organisms

    Curr Opin Biotechnol

    (2020)
  • L. Su et al.

    A hybrid cyt c maturation system enhances the bioelectrical performance of engineered Escherichia coli by improving the rate-limiting step

    Biosens Bioelectron

    (2020)
  • X.Y. Yong et al.

    Enhancement of bioelectricity generation by manipulation of the electron shuttles synthesis pathway in microbial fuel cells

    Bioresour Technol

    (2014)
  • T. Lin et al.

    Engineered Shewanella oneidensis-reduced graphene oxide biohybrid with enhanced biosynthesis and transport of flavins enabled a highest bioelectricity output in microbial fuel cells

    Nano Energy

    (2018)
  • T. Kasai et al.

    Overexpression of the adenylate cyclase gene cyaC facilitates current generation by Shewanella oneidensis in bioelectrochemical systems

    Bioelectrochemistry

    (2019)
  • Y.C. Yong et al.

    Bioelectricity enhancement via overexpression of quorum sensing system in Pseudomonas aeruginosa-inoculated microbial fuel cells

    Biosens Bioelectron

    (2011)
  • D. Choi et al.

    Metabolically engineered glucose-utilizing Shewanella strains under anaerobic conditions

    Bioresour Technol

    (2014)
  • B. Awate et al.

    Stimulation of electro-fermentation in single-chamber microbial electrolysis cells driven by genetically engineered anode biofilms

    J Power Sources

    (2017)
  • Y.C. Yong et al.

    Increasing intracellular releasable electrons dramatically enhances bioelectricity output in microbial fuel cells

    Electrochem Commun

    (2012)
  • X.Y. Yong et al.

    Enhancement of bioelectricity generation by cofactor manipulation in microbial fuel cell

    Biosens Bioelectron

    (2014)
  • F. Golitsch et al.

    Proof of principle for an engineered microbial biosensor based on Shewanella oneidensis outer membrane protein complexes

    Biosens Bioelectron

    (2013)
  • D. Pant et al.

    Bioelectrochemical systems (BES) for sustainable energy production and product recovery from organic wastes and industrial wastewaters

    RSC Adv

    (2012)
  • T. Zheng et al.

    Progress and Prospects of Bioelectrochemical Systems: Electron Transfer and Its Applications in the Microbial Metabolism

    Front Bioeng Biotechnol

    (2020)
  • S. Beblawy et al.

    Extracellular reduction of solid electron acceptors by Shewanella oneidensis

    Mol Microbiol

    (2018)
  • J. Zhao et al.

    Microbial extracellular electron transfer and strategies for engineering electroactive microorganisms

    Biotechnol Adv

    (2020)
  • M.A. Teravest et al.

    Transforming exoelectrogens for biotechnology using synthetic biology

    Biotechnol Bioeng

    (2016)
  • S.M. Glaven

    Bioelectrochemical systems and synthetic biology: more power, more products

    Microb Biotechnol

    (2019)
  • G. Mohanakrishna et al.

    Reactor design for bioelectrochemical systems. Microb. Fuel Cell A Bioelectrochemical Syst. that Convert. Waste to Watts

    Springer International Publishing

    (2017)
  • S.G.A. Flimban et al.

    Overview of recent advancements in the microbial fuel cell from fundamentals to applications: Design, major elements, and scalability

    Energies

    (2019)
  • B.R. Dhar et al.

    Membranes for bioelectrochemical systems: challenges and research advances

    Environ Technol (United Kingdom)

    (2013)
  • B.E. Logan et al.

    Electroactive microorganisms in bioelectrochemical systems

    Nat Rev Microbiol

    (2019)
  • Lovley DR, Walker DJF. Geobacter Protein Nanowires. Front Microbiol 2019;10....
  • S.A. Patil et al.

    Electron transfer mechanisms between microorganisms and electrodes in bioelectrochemical systems

    Bioanal Rev

    (2012)
  • Jadhav DA. Performance enhancement of microbial fuel cells through electrode modifications along with development of...
  • P. Pushkar et al.

    Real textile and domestic wastewater treatment by novel cross-linked microbial fuel cell (CMFC) reactor

    Desalin Water Treat

    (2016)
  • H. Luo et al.

    Selective recovery of Cu2+ and Ni2+ from wastewater using bioelectrochemical system

    Front Environ Sci Eng

    (2015)
  • H. Liu et al.

    Microbial electrosynthesis of organic chemicals from CO2 by Clostridium scatologenes ATCC 25775T

    Bioresour Bioprocess

    (2018)
  • D.A. Jadhav et al.

    Recent progress towards scaling up of MFCs. Microb. Fuel Cell A Bioelectrochemical Syst. that Convert

    Waste to Watts, Springer International Publishing

    (2017)
  • Potter.

    Electrical effects accompanying the decomposition of organic compounds. Proc R Soc London Ser B

    Contain Pap a Biol Character

    (1911)
  • B.H. Kim et al.

    Electrochemical activity of an Fe(III)-reducing bacterium, Shewanella putrefaciens IR-1, in the presence of alternative electron acceptors

    Biotechnol Tech

    (1999)
  • D.R. Bond et al.

    Electrode-reducing microorganisms that harvest energy from marine sediments

    Science (80-)

    (2002)
  • Y. Jiang et al.

    Molecular underpinnings for microbial extracellular electron transfer during biogeochemical cycling of earth elements

    Sci China Life Sci

    (2019)
  • D. Coursolle et al.

    Reconstruction of Extracellular Respiratory Pathways for Iron(III) Reduction in Shewanella Oneidensis Strain MR-1

    Front Microbiol

    (2012)
  • H. Von Canstein et al.

    Secretion of flavins by Shewanella species and their role in extracellular electron transfer

    Appl Environ Microbiol

    (2008)
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