Molecular mechanisms of microbial transmembrane electron transfer of electrochemically active bacteria

doi:10.1016/j.cbpa.2020.06.006

Current Opinion in Chemical Biology

Volume 59, December 2020, Pages 104-110

https://doi.org/10.1016/j.cbpa.2020.06.006 Get rights and content

Abstract

Electrochemically active bacteria (EAB) can release electrons generated by anaerobic respiration to various electron acceptors in various bioelectrochemical systems via transmembrane electron transfer (TET). This renders EAB an important application in terms of energy generation. In this review, recent progress in research toward the TET process of EAB is outlined. Differences in TET process between Gram-positive and Gram-negative EAB are analyzed from a cellular structure perspective to comprehensively understand the molecular mechanism involved in TET. In addition, possible avenues for increasing TET efficiency and power generation capacity of EAB are also explored in depth.

Introduction

Electrochemically active bacteria (EAB) are currently studied because of their unique ability to exhibit extracellular electron transfer (EET) capacity. EAB can release electrons to solid electrodes in various bioelectrochemical systems including microbial fuel cells (MFCs) and microbial electrolysis cells (MECs) for bioenergy production, electrosynthesis of methane or hydrogen, as well as seawater desalination [1,2]. Because of their widespread value in bioelectrochemical systems, EAB are receiving increasing attention, and the environmental distribution, and applications of EAB in bioelectrochemical systems have been well described in recent reviews [2,3].

The electrons from anaerobic respiration of EAB are delivered to extracellular cytochromes through transmembrane electron transfer (TET), which is defined therein as the entire process encompassing electron input, transmembrane delivery, and extracellular release. Hence, TET pathway depends on the cell structures of EAB. As early as 1884, bacteria had been divided into distinct classifications – Gram-positive and Gram-negative by using Gram stain method. Further investigations reveal the profound difference in the structure of their cell wall and membrane, which may lead to a potential impact on the TET of EAB. Therefore, in this review, we briefly summarize current research advances in the TET mechanisms of EAB, including both Gram-positive and Gram-negative bacteria. Then, we outlook the possible approaches to enhance the TET capacities of EAB for bioenergy generation.

Section snippets

TET mechanism of Gram-negative EAB

Gram-negative EAB contain an inner membrane and an outer membrane, which are separated by a periplasmic space. Generally, the electrons derived from the oxidation of organic substrates are found to be coupled with the formation of the reduced form of nicotinamide adenine dinucleotide (NADH). For the TET of Gram-negative EAB, electron flow from NADH to extracellular electron acceptors must traverse the inner membrane, periplasmic space, and then the outer membrane. Figure 1 illustrates the TET

TET mechanism of Gram-positive EAB

Generally, Gram-positive bacteria are enveloped by a thicker cell wall (20–80 nm) composed of peptidoglycan [45]. Because of such a spatial barrier, direct EET to electrodes had been considered to be difficult to achieve for Gram-positive bacteria. In the last decade, an increasing number of Gram-positive bacteria have been found to have EET capacity. But their bioelectrochemical efficiency is lower than that of typical Gram-negative EAB like Shewanella and Geobacter [46]. As a result,

Conclusions and outlook

In this review, we outline the recent progress in the studies on the TET mechanism of EAB. Gram-negative EAB demonstrate excellent bioelectrochemical performance. However, the complexity of the TET process, especially the transperiplasm and trans-outer-membrane, is the bottleneck that limits the further improvement of their extracellular electricity production. Although the current energy-producing ability of Gram-positive bacteria is relatively poor due to the presence of single-membrane

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.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (51878317, 21590812 and 51821006).

References (59)

C. Sánchez et al.
Microbial electrochemical technologies: electronic circuitry and characterization tools
Biosens Bioelectron
(2020)
Q. Wang et al.
Microfluidic dielectrophoresis illuminates the relationship between microbial cell envelope polarizability and electrochemical activity
Sci Adv
(2019)
D. Min et al.
Enhancing extracellular electron transfer of Shewanella oneidensis MR-1 through coupling improved flavin synthesis and metal-reducing conduit for pollutant degradation
Environ Sci Technol
(2017)
Y. Yang et al.
Enhancing bidirectional electron transfer of Shewanella oneidensis by a synthetic flavin pathway
ACS Synth Biol
(2015)
B. Methe et al.
Genome of Geobacter sulfurreducens: metal reduction in subsurface environments
Science
(2003)
J. Liu et al.
Identification and characterization of MtoA: a decaheme c-type cytochrome of the neutrophilic Fe(II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1
Front Microbiol
(2012)
F. Wang et al.
Structure of microbial nanowires reveals stacked hemes that transport electrons over micrometers
Cell
(2019)
P. Parameswaran et al.
Kinetic, electrochemical, and microscopic characterization of the thermophilic, anode-respiring bacterium Thermincola ferriacetica
Environ Sci Technol
(2013)
N.L. Costa et al.
How thermophilic Gram-positive organisms perform extracellular electron transfer: characterization of the cell surface terminal reductase OcwA
mBio
(2019)
B.E. Logan et al.
Conversion of wastes into bioelectricity and chemicals by using microbial electrochemical technologies
Science
(2012)

B.E. Logan et al.

Electroactive microorganisms in bioelectrochemical systems

Nat Rev Microbiol

(2019)

G.E. Pinchuk et al.

Genomic reconstruction of Shewanella oneidensis MR-1 metabolism reveals a previously uncharacterized machinery for lactate utilization

Proc Natl Acad Sci USA

(2009)

A. Hirose et al.

Electrochemically active bacteria sense electrode potentials for regulating catabolic pathways

Nat Commun

(2018)

C.S. Madsen et al.

NADH dehydrogenases Nuo and Nqr1 contribute to extracellular electron transfer by Shewanella oneidensis MR-1 in bioelectrochemical systems

Sci Rep

(2019)

J.W. van Beilen et al.

All three endogenous quinone species of Escherichia coli are involved in controlling the activity of the aerobic/anaerobic response regulator ArcA

Front Microbiol

(2016)

D. Coursolle et al.

Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1

Mol Microbiol

(2010)

Y. Jiao et al.

Deciphering the electron transport pathway for graphene oxide reduction by Shewanella oneidensis MR-1

J Bacteriol

(2011)

E.C. Salas et al.

Reduction of graphene oxide via bacterial respiration

ACS Nano

(2010)

B.M. Fonseca et al.

Mind the gap: cytochrome interactions reveal electron pathways across the periplasm of Shewanella oneidensis MR-1

Biochem J

(2013)

S. Beblawy et al.

Extracellular reduction of solid electron acceptors by Shewanella oneidensis

Mol Microbiol

(2018)

G. Sturm et al.

A dynamic periplasmic electron transfer network enables respiratory flexibility beyond a thermodynamic regulatory regime

ISME J

(2015)

V.P. Delgado et al.

Improvement of the electron transfer rate in Shewanella oneidensis MR-1 using a tailored periplasmic protein composition

Bioelectrochemistry

(2019)

J. Li et al.

Rediverting electron flux with an engineered CRISPR-ddAsCpf1 system to enhance pollutant degradation capacity of Shewanella oneidensis

Environ Sci Technol

(2020)

T. Kasai et al.

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

Bioelectrochemistry

(2019)

Z.H. Cheng et al.

Promoting bidirectional extracellular electron transfer of Shewanella oneidensis MR-1 for hexavalent chromium reduction via elevating intracellular cAMP level

Biotechnol Bioeng

(2020)

E. Marsili et al.

Shewanella secretes flavins that mediate extracellular electron transfer

Proc Natl Acad Sci USA

(2008)

A. Okamoto et al.

Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones

Proc Natl Acad Sci USA

(2013)

S. Xu et al.

Disentangling the roles of free and cytochrome-bound flavins in extracellular electron transport from Shewanella oneidensis MR-1

Electrochim Acta

(2016)

N.J. Kotloski et al.

Flavin electron shuttles dominate extracellular electron transfer by Shewanella oneidensis

mBio

(2013)

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Molecular mechanisms of microbial transmembrane electron transfer of electrochemically active bacteria

Abstract

Introduction

Section snippets

TET mechanism of Gram-negative EAB

TET mechanism of Gram-positive EAB

Conclusions and outlook

Declaration of competing interest

Acknowledgements

Biosens Bioelectron

Sci Adv

Environ Sci Technol

ACS Synth Biol

Science

Front Microbiol

Cell

Environ Sci Technol

mBio

Conversion of wastes into bioelectricity and chemicals by using microbial electrochemical technologies

Science

Electroactive microorganisms in bioelectrochemical systems

Nat Rev Microbiol

Genomic reconstruction of Shewanella oneidensis MR-1 metabolism reveals a previously uncharacterized machinery for lactate utilization

Proc Natl Acad Sci USA

Electrochemically active bacteria sense electrode potentials for regulating catabolic pathways

Nat Commun

NADH dehydrogenases Nuo and Nqr1 contribute to extracellular electron transfer by Shewanella oneidensis MR-1 in bioelectrochemical systems

Sci Rep

All three endogenous quinone species of Escherichia coli are involved in controlling the activity of the aerobic/anaerobic response regulator ArcA

Front Microbiol

Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1

Mol Microbiol

Deciphering the electron transport pathway for graphene oxide reduction by Shewanella oneidensis MR-1

J Bacteriol

Reduction of graphene oxide via bacterial respiration

ACS Nano

Mind the gap: cytochrome interactions reveal electron pathways across the periplasm of Shewanella oneidensis MR-1

Biochem J

Extracellular reduction of solid electron acceptors by Shewanella oneidensis

Mol Microbiol

A dynamic periplasmic electron transfer network enables respiratory flexibility beyond a thermodynamic regulatory regime

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Bioelectrochemistry

Rediverting electron flux with an engineered CRISPR-ddAsCpf1 system to enhance pollutant degradation capacity of Shewanella oneidensis

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