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Title: Constraint-Based Modeling of Carbon Fixation and the Energetics of Electron Transfer in Geobacter metallireducens

Abstract

Geobacter species are of great interest for environmental and biotechnology applications as they can carry out direct electron transfer to insoluble metals or other microorganisms and have the ability to assimilate inorganic carbon. Here, we report on the capability and key enabling metabolic machinery of Geobacter metallireducens GS-15 to carry out CO2 fixation and direct electron transfer to iron. An updated metabolic reconstruction was generated, growth screens on targeted conditions of interest were performed, and constraint-based analysis was utilized to characterize and evaluate critical pathways and reactions in G. metallireducens. The novel capability of G. metallireducens to grow autotrophically with formate and Fe(III) was predicted and subsequently validated in vivo. Additionally, the energetic cost of transferring electrons to an external electron acceptor was determined through analysis of growth experiments carried out using three different electron acceptors (Fe(III), nitrate, and fumarate) by systematically isolating and examining different parts of the electron transport chain. The updated reconstruction will serve as a knowledgebase for understanding and engineering Geobacter and similar species. Author Summary The ability of microorganisms to exchange electrons directly with their environment has large implications for our knowledge of industrial and environmental processes. For decades, it has been known that microbesmore » can use electrodes as electron acceptors in microbial fuel cell settings. Geobacter metallireducens has been one of the model organisms for characterizing microbe-electrode interactions as well as environmental processes such as bioremediation. Here, we significantly expand the knowledge of metabolism and energetics of this model organism by employing constraint-based metabolic modeling. Through this analysis, we build the metabolic pathways necessary for carbon fixation, a desirable property for industrial chemical production. We further discover a novel growth condition which enables the characterization of autotrophic (i.e., carbon-fixing) metabolism in Geobacter. Importantly, our systems-level modeling approach helped elucidate the key metabolic pathways and the energetic cost associated with extracellular electron transfer. This model can be applied to characterize and engineer the metabolism and electron transfer capabilities of Geobacter for biotechnological applications.« less

Authors:
; ; ; ; ; ; ;
Publication Date:
Sponsoring Org.:
USDOE Advanced Research Projects Agency - Energy (ARPA-E)
OSTI Identifier:
1211508
DOE Contract Number:  
DE-AR0000087
Resource Type:
Journal Article
Journal Name:
PLOS COMPUTATIONAL BIOLOGY
Additional Journal Information:
Journal Volume: 10; Journal Issue: 4; Journal ID: ISSN 1553-734X
Country of Publication:
United States
Language:
English

Citation Formats

Feist, AM, Nagarajan, H, Rotaru, AE, Tremblay, PL, Zhang, T, Nevin, KP, Lovley, DR, and Zengler, K. Constraint-Based Modeling of Carbon Fixation and the Energetics of Electron Transfer in Geobacter metallireducens. United States: N. p., 2014. Web. doi:10.1371/journal.pcbi.1003575.
Feist, AM, Nagarajan, H, Rotaru, AE, Tremblay, PL, Zhang, T, Nevin, KP, Lovley, DR, & Zengler, K. Constraint-Based Modeling of Carbon Fixation and the Energetics of Electron Transfer in Geobacter metallireducens. United States. https://doi.org/10.1371/journal.pcbi.1003575
Feist, AM, Nagarajan, H, Rotaru, AE, Tremblay, PL, Zhang, T, Nevin, KP, Lovley, DR, and Zengler, K. 2014. "Constraint-Based Modeling of Carbon Fixation and the Energetics of Electron Transfer in Geobacter metallireducens". United States. https://doi.org/10.1371/journal.pcbi.1003575.
@article{osti_1211508,
title = {Constraint-Based Modeling of Carbon Fixation and the Energetics of Electron Transfer in Geobacter metallireducens},
author = {Feist, AM and Nagarajan, H and Rotaru, AE and Tremblay, PL and Zhang, T and Nevin, KP and Lovley, DR and Zengler, K},
abstractNote = {Geobacter species are of great interest for environmental and biotechnology applications as they can carry out direct electron transfer to insoluble metals or other microorganisms and have the ability to assimilate inorganic carbon. Here, we report on the capability and key enabling metabolic machinery of Geobacter metallireducens GS-15 to carry out CO2 fixation and direct electron transfer to iron. An updated metabolic reconstruction was generated, growth screens on targeted conditions of interest were performed, and constraint-based analysis was utilized to characterize and evaluate critical pathways and reactions in G. metallireducens. The novel capability of G. metallireducens to grow autotrophically with formate and Fe(III) was predicted and subsequently validated in vivo. Additionally, the energetic cost of transferring electrons to an external electron acceptor was determined through analysis of growth experiments carried out using three different electron acceptors (Fe(III), nitrate, and fumarate) by systematically isolating and examining different parts of the electron transport chain. The updated reconstruction will serve as a knowledgebase for understanding and engineering Geobacter and similar species. Author Summary The ability of microorganisms to exchange electrons directly with their environment has large implications for our knowledge of industrial and environmental processes. For decades, it has been known that microbes can use electrodes as electron acceptors in microbial fuel cell settings. Geobacter metallireducens has been one of the model organisms for characterizing microbe-electrode interactions as well as environmental processes such as bioremediation. Here, we significantly expand the knowledge of metabolism and energetics of this model organism by employing constraint-based metabolic modeling. Through this analysis, we build the metabolic pathways necessary for carbon fixation, a desirable property for industrial chemical production. We further discover a novel growth condition which enables the characterization of autotrophic (i.e., carbon-fixing) metabolism in Geobacter. Importantly, our systems-level modeling approach helped elucidate the key metabolic pathways and the energetic cost associated with extracellular electron transfer. This model can be applied to characterize and engineer the metabolism and electron transfer capabilities of Geobacter for biotechnological applications.},
doi = {10.1371/journal.pcbi.1003575},
url = {https://www.osti.gov/biblio/1211508}, journal = {PLOS COMPUTATIONAL BIOLOGY},
issn = {1553-734X},
number = 4,
volume = 10,
place = {United States},
year = {Thu Apr 24 00:00:00 EDT 2014},
month = {Thu Apr 24 00:00:00 EDT 2014}
}