Redox dependent metabolic shift in Clostridium autoethanogenum by extracellular electron supply

There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

Abstract

Background

Microbial electrosynthesis is a novel approach that aims at shifting the cellular metabolism towards electron-dense target products by extracellular electron supply. Many organisms including several acetogenic bacteria have been shown to be able to consume electrical current. However, suitable hosts for relevant industrial processes are yet to be discovered, and major knowledge gaps about the underlying fundamental processes still remain.

Results

In this paper, we present the first report of electron uptake by the Gram-positive, ethanol-producing acetogen, Clostridium autoethanogenum. Under heterotrophic conditions, extracellular electron supply induced a significant metabolic shift away from acetate. In electrically enhanced fermentations on fructose, acetate production was cut by more than half, while production of lactate and 2,3-butanediol increased by 35-fold and threefold, respectively. The use of mediators with different redox potential revealed a direct dependency of the metabolic effect on the redox potential at which electrons are supplied. Only electrons delivered at a redox potential low enough to reduce ferredoxin caused the reported effect.

Conclusions

Production in acetogenic organisms is usually challenged by cellular energy limitations if the target product does not lead to a net energy gain as in the case of acetate. The presented results demonstrate a significant shift of carbon fluxes away from acetate towards the products, lactate and 2,3-butanediol, induced by small electricity input (~0.09 mol of electrons per mol of substrate). This presents a simple and attractive method to optimize acetogenic fermentations for production of chemicals and fuels using electrochemical techniques. The relationship between metabolic shift and redox potential of electron feed gives an indication of possible electron-transfer mechanisms and helps to prioritize further research efforts.

Electronic supplementary material

The online version of this article (doi:10.1186/s13068-016-0663-2) contains supplementary material, which is available to authorized users.

Related collections

Most cited references 24

Record: found
Abstract: found
Article: not found

Energy conservation via electron bifurcating ferredoxin reduction and proton/Na(+) translocating ferredoxin oxidation.

Wolfgang Buckel, Rudolf Thauer (2013)

The review describes four flavin-containing cytoplasmatic multienzyme complexes from anaerobic bacteria and archaea that catalyze the reduction of the low potential ferredoxin by electron donors with higher potentials, such as NAD(P)H or H(2) at ≤ 100 kPa. These endergonic reactions are driven by concomitant oxidation of the same donor with higher potential acceptors such as crotonyl-CoA, NAD(+) or heterodisulfide (CoM-S-S-CoB). The process called flavin-based electron bifurcation (FBEB) can be regarded as a third mode of energy conservation in addition to substrate level phosphorylation (SLP) and electron transport phosphorylation (ETP). FBEB has been detected in the clostridial butyryl-CoA dehydrogenase/electron transferring flavoprotein complex (BcdA-EtfBC), the multisubunit [FeFe]hydrogenase from Thermotoga maritima (HydABC) and from acetogenic bacteria, the [NiFe]hydrogenase/heterodisulfide reductase (MvhADG-HdrABC) from methanogenic archaea, and the transhydrogenase (NfnAB) from many Gram positive and Gram negative bacteria and from anaerobic archaea. The Bcd/EtfBC complex that catalyzes electron bifurcation from NADH to the low potential ferredoxin and to the high potential crotonyl-CoA has already been studied in some detail. The bifurcating protein most likely is EtfBC, which in each subunit (βγ) contains one FAD. In analogy to the bifurcating complex III of the mitochondrial respiratory chain and with the help of the structure of the human ETF, we propose a conformational change by which γ-FADH(-) in EtfBC approaches β-FAD to enable the bifurcating one-electron transfer. The ferredoxin reduced in one of the four electron bifurcating reactions can regenerate H(2) or NADPH, reduce CO(2) in acetogenic bacteria and methanogenic archaea, or is converted to ΔμH(+)/Na(+) by the membrane-associated enzyme complexes Rnf and Ech, whereby NADH and H(2) are recycled, respectively. The mainly bacterial Rnf complexes couple ferredoxin oxidation by NAD(+) with proton/sodium ion translocation and the more diverse energy converting [NiFe]hydrogenases (Ech) do the same, whereby NAD(+) is replaced by H(+). Many organisms also use Rnf and Ech in the reverse direction to reduce ferredoxin driven by ΔμH(+)/Na(+). Finally examples are shown, in which the four bifurcating multienzyme complexes alone or together with Rnf and Ech are integrated into energy metabolisms of nine anaerobes. This article is part of a Special Issue entitled: The evolutionary aspects of bioenergetic systems. Copyright © 2012 Elsevier B.V. All rights reserved.

0 comments Cited 247 times – based on 0 reviews      Review now

Bookmark

Record: found
Abstract: found
Article: not found

Clostridium ljungdahlii represents a microbial production platform based on syngas.

Michael Köpke, Claudia Held, Sandra Hujer … (2010)

Clostridium ljungdahlii is an anaerobic homoacetogen, able to ferment sugars, other organic compounds, or CO(2)/H(2) and synthesis gas (CO/H(2)). The latter feature makes it an interesting microbe for the biotech industry, as important bulk chemicals and proteins can be produced at the expense of CO(2), thus combining industrial needs with sustained reduction of CO and CO(2) in the atmosphere. Sequencing the complete genome of C. ljungdahlii revealed that it comprises 4,630,065 bp and is one of the largest clostridial genomes known to date. Experimental data and in silico comparisons revealed a third mode of anaerobic homoacetogenic metabolism. Unlike other organisms such as Moorella thermoacetica or Acetobacterium woodii, neither cytochromes nor sodium ions are involved in energy generation. Instead, an Rnf system is present, by which proton translocation can be performed. An electroporation procedure has been developed to transform the organism with plasmids bearing heterologous genes for butanol production. Successful expression of these genes could be demonstrated, leading to formation of the biofuel. Thus, C. ljungdahlii can be used as a unique microbial production platform based on synthesis gas and carbon dioxide/hydrogen mixtures.

0 comments Cited 199 times – based on 0 reviews      Review now

Bookmark

Record: found
Abstract: found
Article: found

Is Open Access

Structural and functional analysis of cellular networks with CellNetAnalyzer

Steffen Klamt, Julio Saez-Rodriguez, Ernst Gilles (2007)

Background Mathematical modelling of cellular networks is an integral part of Systems Biology and requires appropriate software tools. An important class of methods in Systems Biology deals with structural or topological (parameter-free) analysis of cellular networks. So far, software tools providing such methods for both mass-flow (metabolic) as well as signal-flow (signalling and regulatory) networks are lacking. Results Herein we introduce CellNetAnalyzer, a toolbox for MATLAB facilitating, in an interactive and visual manner, a comprehensive structural analysis of metabolic, signalling and regulatory networks. The particular strengths of CellNetAnalyzer are methods for functional network analysis, i.e. for characterising functional states, for detecting functional dependencies, for identifying intervention strategies, or for giving qualitative predictions on the effects of perturbations. CellNetAnalyzer extends its predecessor FluxAnalyzer (originally developed for metabolic network and pathway analysis) by a new modelling framework for examining signal-flow networks. Two of the novel methods implemented in CellNetAnalyzer are discussed in more detail regarding algorithmic issues and applications: the computation and analysis (i) of shortest positive and shortest negative paths and circuits in interaction graphs and (ii) of minimal intervention sets in logical networks. Conclusion CellNetAnalyzer provides a single suite to perform structural and qualitative analysis of both mass-flow- and signal-flow-based cellular networks in a user-friendly environment. It provides a large toolbox with various, partially unique, functions and algorithms for functional network analysis.CellNetAnalyzer is freely available for academic use.

0 comments Cited 162 times – based on 0 reviews      Review now

Bookmark

All references

Author and article information

Contributors

Frauke Kracke: frauke.kracke@uq.net.au

Bernardino Virdis: b.virdis@awmc.uq.edu.au

Paul V. Bernhardt: p.bernhardt@uq.edu.au

Korneel Rabaey: Korneel.Rabaey@UGent.be

Jens O. Krömer: j.kromer@awmc.uq.edu.au

Journal

Journal ID (nlm-ta): Biotechnol Biofuels

Journal ID (iso-abbrev): Biotechnol Biofuels

Title: Biotechnology for Biofuels

Publisher: BioMed Central (London )

ISSN (Electronic): 1754-6834

Publication date (Electronic): 16 November 2016

Publication date PMC-release: 16 November 2016

Publication date Collection: 2016

Volume: 9

Electronic Location Identifier: 249

Affiliations

[1 ]Centre for Microbial Electrochemical Systems, The University of Queensland, Brisbane, QLD 4072 Australia

[2 ]Advanced Water Management Centre, The University of Queensland, Brisbane, QLD 4072 Australia

[3 ]School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane, QLD 4072 Australia

[4 ]Laboratory of Microbial Ecology and Technology, Faculty of Bioscience Engineering, Universiteit Ghent, Ghent, Belgium

Article

Publisher ID: 663

DOI: 10.1186/s13068-016-0663-2

PMC ID: 5112729

PubMed ID: 27882076

SO-VID: 6ef89e8a-a939-4514-a924-8ee373771559

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 19 March 2016

Date accepted : 4 November 2016

Custom metadata

ScienceOpen disciplines: Biotechnology

Keywords: microbial electrosynthesis,bio production,gas fermentation,wood-ljungdahl pathway,extracellular electron transport,redox mediator,acetogen,rnf complex

Data availability:

ScienceOpen disciplines: Biotechnology

Keywords: microbial electrosynthesis, bio production, gas fermentation, wood-ljungdahl pathway, extracellular electron transport, redox mediator, acetogen, rnf complex

Redox dependent metabolic shift in Clostridium autoethanogenum by extracellular electron supply

Read this article at

Abstract

Background

Results

Conclusions

Electronic supplementary material

Related collections

Genome Engineering using CRISPR

Most cited references 24

Energy conservation via electron bifurcating ferredoxin reduction and proton/Na(+) translocating ferredoxin oxidation.

Clostridium ljungdahlii represents a microbial production platform based on syngas.

Structural and functional analysis of cellular networks with CellNetAnalyzer

Author and article information

Contributors

Journal

Affiliations

Article

History

Categories

Custom metadata

Comments

Comment on this article

Similar content 56

Cited by 25

Most referenced authors 211