Overview of electroactive microorganisms and electron transfer mechanisms in microbial electrochemistry

https://doi.org/10.1016/j.biortech.2021.126579Get rights and content

Highlights

Abstract

Electroactive microorganisms acting as microbial electrocatalysts have intrinsic metabolisms that mediate a redox potential difference between solid electrodes and microbes, leading to spontaneous electron transfer to the electrode (exo-electron transfer) or electron uptake from the electrode (endo-electron transfer). These microbes biochemically convert various organic and/or inorganic compounds to electricity and/or biochemicals in bioelectrochemical systems (BESs) such as microbial fuel cells (MFCs) and microbial electrosynthesis cells (MECs). For the past two decades, intense studies have converged to clarify electron transfer mechanisms of electroactive microbes in BESs, which thereby have led to improved bioelectrochemical performance. Also, many novel exoelectrogenic eukaryotes as well as prokaryotes with electroactive properties are being continuously discovered. This review presents an overview of electroactive microorganisms (bacteria, microalgae and fungi) and their exo- and endo-electron transfer mechanisms in BESs for optimizing and advancing bioelectrochemical techniques.

Introduction

Bioelectrochemical systems (BESs) represent an emerging branch of biotechnology capable of converting organic or inorganic source into valuable products by catalytic action of electro-active microorganisms. The first observation of the BES was made by Potter over a hundred years ago when he reported the generation of an electric potential by the bacterium Bacillus coli (E. coli) and Saccharomyces cerevisiae cultivated in a galvanic cell (Potter, 1911). However, the study did not present the mechanism of such microbial electricity generation and garnered little attention. In 1931, Cohen reported a potential generation of as high as 35 V by connecting multiple microbial fuel cells (MFCs) in series (Cohen, 1931). During the 1980 s, Bennetto and co-workers continued to study electric potential generation from organic compounds using different redox mediators in MFCs (Bennetto et al., 1983, Allen and Bennetto, 1993). However, the ability of bacteria to reduce metals and chemicals other than oxygen under anaerobic conditions remained unclear until the 1980 s. Proof of electron transfer reactions without mediators was observed in a pure culture of Shewanella putrefaciens (Kim et al., 1999).

Application of electrode-microorganism interactions for bioelectricity generation, wastewater treatment, biosensors, and production of hydrogen gas was reported in a BES (Santoro et al., 2017, Schneider et al., 2016). The concept of the MFC has garnered much attention due to its unique ability to simultaneous treat organic wastes and generate electricity through a bio-catalytic mechanism. In the anode of the MFC, oxidation of organic compounds by electroactive microorganisms occurs in anaerobic conditions; electricity is then generated when the free electrons are delivered to the anode and passed through an external circuit towards the cathode (Fig. 1). Some examples of electron exchange at microbial anodes are also found in fungi, especially yeast, that have been known for their electrogenic function directing electron transfer reactions via cytochrome-c (Ducommun et al., 2010).

In recent years, the cathodic reaction approach in BES has been extensively adopted due to its cost-effective operation, use of non-metal catalysts, and biochemical production by cathodic biocatalysts, novel endo-electrogen emergence, etc. Acquisition of value-added multi-carbon chemicals is achieved by carbon dioxide reduction at the cathode using biocatalysts such as acetogenic bacteria (Table 1). This process is called microbial electrosynthesis (MES) and has been of great interest for a decade (Kazemi et al., 2015). In contrast to electrogenesis, electrotrophic microbes in the cathode shift CO2 to multi-chain organic carbons such as acetate, volatile fatty acids, and alcohols (Song et al., 2022, 2021). In addition, fungi and microalgae are also known to catalyse the same reaction at the cathode (Table 2, Table 3).

In this review, the authors discuss the exo- and endo-electron transfer mechanisms of different electroactive microorganisms in microbial electrochemical systems. Emphasis on unique cellular components and microbial interactions with electrodes are highlighted to survey recent progress and studies on the BES.

Section snippets

Electroactive microbes in bio-electrochemical system

Diverse classes of microorganisms, (Proteobacteria, Firmicutes, and Acidobacteirapyla, and microalgae, fungi, and yeast) representing different ecological and environmental conditions have been examined in BESs. This is mainly because microorganisms are ubiquitous and metabolically versatile, able to inhabit in a wide range of physiological conditions. Though the electroactive capability of the bacterium E. coli was first reported in 1911, the specific mechanism of exo-electron delivery was not

Electron transfer mechanisms

The anode as the sole electron acceptor collects free electrons either from electron mediators or directly from the microbial cell. The ways that electrons are transferred from microbes to the electrode are broadly classified into two categories – direct and indirect electron transfer – based on the contact between the cell and the anode (Fig. 5). In the direct transfer systems, electrons are transferred from bacteria to the electrode directly without the involvement of external mediators. In

Engineered electroactive bacteria

With advancements in genetic engineering and synthetic biology, attempts to improve the performance of electroactive bacteria have focused on altering the genetics of electron transfer phenomenon. Other than the Shewanella and Geobacter species, the rate of electron transfer and efficiency in electroactive bacteria are modest. With the rapid emergence of analytical technologies and advancements in biotechnology, researchers have begun manipulating strains to construct engineered electroactive

Conclusions and future perspectives

Electron transfer mechanisms of electroactive microorganisms in diverse microbial community have been elucidated under limited cultivation conditions in the BES. Cellular secretions such as cytochromes and flavins involved in electron transport processes facilitate understanding complex electrode-microbe interactions. The microbial electron transfer phenomenon offers an excellent opportunity via interdisciplinary research in biotechnology, electrochemistry, and material science for industrial

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.

Acknowledgment

This work was supported by a National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (NRF-2020R1A2C2012106).

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    These authors contributed equally to this study.

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