Electro-fermentation enhances H2 and ethanol co-production by regulating electron transfer and substrate transmembrane transport

Jiayu Gu; Zhen Li; Guojun Xie; Yang Yang; Binfeng Liu; Zhiyong Jason Ren; Defeng Xing

doi:10.1016/j.cej.2021.132223

Electro-fermentation enhances H₂ and ethanol co-production by regulating electron transfer and substrate transmembrane transport

Jiayu Gu, Zhen Li, Guojun Xie, Yang Yang, Binfeng Liu, Zhiyong Jason Ren, Defeng Xing

Research output: Contribution to journal › Article › peer-review

19 Scopus citations

Abstract

Electro-fermentation systems (EFSs) are an emerging technology capable of regulating microbial fermentation pathways by tuning oxidation-reduction potentials and electron flow. However, there is limited understanding of the bioenergy conversion and metabolic regulation of fermentative bacteria in EFSs. In this study, we investigated how electrode potentials in EFSs affect the metabolic products and global transcriptome expression of Ethanoligenens harbinense. The E. harbinense-inoculated anodic EFS (AEFS) with a poised potential of 0 V or the cathodic EFS (CEFS) with a poised potential of 0 V (vs. Ag/AgCl reference electrode) obtained the maximum H₂ production of 1888–1986 mL/L-medium, which increased by 23–26% compared with open-circuit fermentation (OC-EFSs). The highest H₂ yield of 1.190 ± 0.009–1.197 ± 0.001 mol-H₂/mol-glucose was obtained by the AEFS₀ and the OC-EFS. Ethanol production of AEFS_-0.4 increased by 30.7 ± 13.3% compared with OC-EFSs. In addition, glucose uptake and cell growth in the EFS were enhanced with an increase in cellular energy supply. Transcriptome analysis revealed that overexpression of the [FeFe]-hydrogenase, ferredoxin, and rubredoxin genes in the AEFS with a poised potential of 0 V promoted the H₂ production rate. Genes involved in electron transfer and reduced nicotinamide adenine dinucleotide (NADH) regeneration were upregulated in the AEFS, leading to more ethanol production. In addition, substrate transmembrane transport was suppressed by underexpression of adenosine triphosphate (ATP)-binding cassette (ABC) transporter system-related genes at lower or higher potentials. These results confirm that an EFS effectively regulates the metabolite spectrum of H₂-producing bacteria by coordinating electron transfer, NADH regeneration, and substrate transmembrane transport to provide a flexible approach for improving bioenergy production by fermentative bacteria.

Original language	English (US)
Article number	132223
Journal	Chemical Engineering Journal
Volume	429
DOIs	https://doi.org/10.1016/j.cej.2021.132223
State	Published - Feb 1 2022
Externally published	Yes

All Science Journal Classification (ASJC) codes

General Chemistry
Environmental Chemistry
General Chemical Engineering
Industrial and Manufacturing Engineering

Keywords

Biohydrogen production
Electro-fermentation
Ethanoligenens harbinense
Microbial electrochemical technology
Transcriptome

Access to Document

10.1016/j.cej.2021.132223

Cite this

@article{979722674b804eb0b5911e625a3717ae,

title = "Electro-fermentation enhances H2 and ethanol co-production by regulating electron transfer and substrate transmembrane transport",

abstract = "Electro-fermentation systems (EFSs) are an emerging technology capable of regulating microbial fermentation pathways by tuning oxidation-reduction potentials and electron flow. However, there is limited understanding of the bioenergy conversion and metabolic regulation of fermentative bacteria in EFSs. In this study, we investigated how electrode potentials in EFSs affect the metabolic products and global transcriptome expression of Ethanoligenens harbinense. The E. harbinense-inoculated anodic EFS (AEFS) with a poised potential of 0 V or the cathodic EFS (CEFS) with a poised potential of 0 V (vs. Ag/AgCl reference electrode) obtained the maximum H2 production of 1888–1986 mL/L-medium, which increased by 23–26% compared with open-circuit fermentation (OC-EFSs). The highest H2 yield of 1.190 ± 0.009–1.197 ± 0.001 mol-H2/mol-glucose was obtained by the AEFS0 and the OC-EFS. Ethanol production of AEFS-0.4 increased by 30.7 ± 13.3% compared with OC-EFSs. In addition, glucose uptake and cell growth in the EFS were enhanced with an increase in cellular energy supply. Transcriptome analysis revealed that overexpression of the [FeFe]-hydrogenase, ferredoxin, and rubredoxin genes in the AEFS with a poised potential of 0 V promoted the H2 production rate. Genes involved in electron transfer and reduced nicotinamide adenine dinucleotide (NADH) regeneration were upregulated in the AEFS, leading to more ethanol production. In addition, substrate transmembrane transport was suppressed by underexpression of adenosine triphosphate (ATP)-binding cassette (ABC) transporter system-related genes at lower or higher potentials. These results confirm that an EFS effectively regulates the metabolite spectrum of H2-producing bacteria by coordinating electron transfer, NADH regeneration, and substrate transmembrane transport to provide a flexible approach for improving bioenergy production by fermentative bacteria.",

keywords = "Biohydrogen production, Electro-fermentation, Ethanoligenens harbinense, Microbial electrochemical technology, Transcriptome",

author = "Jiayu Gu and Zhen Li and Guojun Xie and Yang Yang and Binfeng Liu and Ren, {Zhiyong Jason} and Defeng Xing",

note = "Publisher Copyright: {\textcopyright} 2021 Elsevier B.V.",

year = "2022",

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doi = "10.1016/j.cej.2021.132223",

language = "English (US)",

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TY - JOUR

T1 - Electro-fermentation enhances H2 and ethanol co-production by regulating electron transfer and substrate transmembrane transport

AU - Gu, Jiayu

AU - Li, Zhen

AU - Xie, Guojun

AU - Yang, Yang

AU - Liu, Binfeng

AU - Ren, Zhiyong Jason

AU - Xing, Defeng

PY - 2022/2/1

Y1 - 2022/2/1

N2 - Electro-fermentation systems (EFSs) are an emerging technology capable of regulating microbial fermentation pathways by tuning oxidation-reduction potentials and electron flow. However, there is limited understanding of the bioenergy conversion and metabolic regulation of fermentative bacteria in EFSs. In this study, we investigated how electrode potentials in EFSs affect the metabolic products and global transcriptome expression of Ethanoligenens harbinense. The E. harbinense-inoculated anodic EFS (AEFS) with a poised potential of 0 V or the cathodic EFS (CEFS) with a poised potential of 0 V (vs. Ag/AgCl reference electrode) obtained the maximum H2 production of 1888–1986 mL/L-medium, which increased by 23–26% compared with open-circuit fermentation (OC-EFSs). The highest H2 yield of 1.190 ± 0.009–1.197 ± 0.001 mol-H2/mol-glucose was obtained by the AEFS0 and the OC-EFS. Ethanol production of AEFS-0.4 increased by 30.7 ± 13.3% compared with OC-EFSs. In addition, glucose uptake and cell growth in the EFS were enhanced with an increase in cellular energy supply. Transcriptome analysis revealed that overexpression of the [FeFe]-hydrogenase, ferredoxin, and rubredoxin genes in the AEFS with a poised potential of 0 V promoted the H2 production rate. Genes involved in electron transfer and reduced nicotinamide adenine dinucleotide (NADH) regeneration were upregulated in the AEFS, leading to more ethanol production. In addition, substrate transmembrane transport was suppressed by underexpression of adenosine triphosphate (ATP)-binding cassette (ABC) transporter system-related genes at lower or higher potentials. These results confirm that an EFS effectively regulates the metabolite spectrum of H2-producing bacteria by coordinating electron transfer, NADH regeneration, and substrate transmembrane transport to provide a flexible approach for improving bioenergy production by fermentative bacteria.

AB - Electro-fermentation systems (EFSs) are an emerging technology capable of regulating microbial fermentation pathways by tuning oxidation-reduction potentials and electron flow. However, there is limited understanding of the bioenergy conversion and metabolic regulation of fermentative bacteria in EFSs. In this study, we investigated how electrode potentials in EFSs affect the metabolic products and global transcriptome expression of Ethanoligenens harbinense. The E. harbinense-inoculated anodic EFS (AEFS) with a poised potential of 0 V or the cathodic EFS (CEFS) with a poised potential of 0 V (vs. Ag/AgCl reference electrode) obtained the maximum H2 production of 1888–1986 mL/L-medium, which increased by 23–26% compared with open-circuit fermentation (OC-EFSs). The highest H2 yield of 1.190 ± 0.009–1.197 ± 0.001 mol-H2/mol-glucose was obtained by the AEFS0 and the OC-EFS. Ethanol production of AEFS-0.4 increased by 30.7 ± 13.3% compared with OC-EFSs. In addition, glucose uptake and cell growth in the EFS were enhanced with an increase in cellular energy supply. Transcriptome analysis revealed that overexpression of the [FeFe]-hydrogenase, ferredoxin, and rubredoxin genes in the AEFS with a poised potential of 0 V promoted the H2 production rate. Genes involved in electron transfer and reduced nicotinamide adenine dinucleotide (NADH) regeneration were upregulated in the AEFS, leading to more ethanol production. In addition, substrate transmembrane transport was suppressed by underexpression of adenosine triphosphate (ATP)-binding cassette (ABC) transporter system-related genes at lower or higher potentials. These results confirm that an EFS effectively regulates the metabolite spectrum of H2-producing bacteria by coordinating electron transfer, NADH regeneration, and substrate transmembrane transport to provide a flexible approach for improving bioenergy production by fermentative bacteria.

KW - Biohydrogen production

KW - Electro-fermentation

KW - Ethanoligenens harbinense

KW - Microbial electrochemical technology

KW - Transcriptome

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