Characterization of metabolism in the Fe(III)-reducing organism Geobacter sulfurreducens by constraint-based modeling

R Mahadevan, D R Bond, J E Butler, A Esteve-Nuñez, M V Coppi, B O Palsson, C H Schilling, D R Lovley

Research output: Contribution to journalArticle

219 Citations (Scopus)

Abstract

Geobacter sulfurreducens is a well-studied representative of the Geobacteraceae, which play a critical role in organic matter oxidation coupled to Fe(III) reduction, bioremediation of groundwater contaminated with organics or metals, and electricity production from waste organic matter. In order to investigate G. sulfurreducens central metabolism and electron transport, a metabolic model which integrated genome-based predictions with available genetic and physiological data was developed via the constraint-based modeling approach. Evaluation of the rates of proton production and consumption in the extracellular and cytoplasmic compartments revealed that energy conservation with extracellular electron acceptors, such as Fe(III), was limited relative to that associated with intracellular acceptors. This limitation was attributed to lack of cytoplasmic proton consumption during reduction of extracellular electron acceptors. Model-based analysis of the metabolic cost of producing an extracellular electron shuttle to promote electron transfer to insoluble Fe(III) oxides demonstrated why Geobacter species, which do not produce shuttles, have an energetic advantage over shuttle-producing Fe(III) reducers in subsurface environments. In silico analysis also revealed that the metabolic network of G. sulfurreducens could synthesize amino acids more efficiently than that of Escherichia coli due to the presence of a pyruvate-ferredoxin oxidoreductase, which catalyzes synthesis of pyruvate from acetate and carbon dioxide in a single step. In silico phenotypic analysis of deletion mutants demonstrated the capability of the model to explore the flexibility of G. sulfurreducens central metabolism and correctly predict mutant phenotypes. These results demonstrate that iterative modeling coupled with experimentation can accelerate the understanding of the physiology of poorly studied but environmentally relevant organisms and may help optimize their practical applications.

Original languageEnglish
Pages (from-to)1558-68
Number of pages11
JournalApplied and Environmental Microbiology
Volume72
Issue number2
DOIs
Publication statusPublished - Feb 2006

Fingerprint

Geobacter sulfurreducens
Geobacter
metabolism
Electrons
electron
organisms
Computer Simulation
modeling
electrons
Protons
Pyruvate Synthase
protons
electron transfer
Geobacteraceae
pyruvate synthase
Electricity
Environmental Biodegradation
organic matter
Groundwater
Electron Transport

Keywords

  • Amino Acids
  • Electron Transport
  • Escherichia coli
  • Fumarates
  • Geobacter
  • Iron
  • Models, Biological
  • Mutation
  • Oxidation-Reduction
  • Phenotype
  • Protons
  • Quinones
  • Species Specificity

Cite this

Characterization of metabolism in the Fe(III)-reducing organism Geobacter sulfurreducens by constraint-based modeling. / Mahadevan, R; Bond, D R; Butler, J E; Esteve-Nuñez, A; Coppi, M V; Palsson, B O; Schilling, C H; Lovley, D R.

In: Applied and Environmental Microbiology, Vol. 72, No. 2, 02.2006, p. 1558-68.

Research output: Contribution to journalArticle

Mahadevan, R ; Bond, D R ; Butler, J E ; Esteve-Nuñez, A ; Coppi, M V ; Palsson, B O ; Schilling, C H ; Lovley, D R. / Characterization of metabolism in the Fe(III)-reducing organism Geobacter sulfurreducens by constraint-based modeling. In: Applied and Environmental Microbiology. 2006 ; Vol. 72, No. 2. pp. 1558-68.
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AU - Coppi, M V

AU - Palsson, B O

AU - Schilling, C H

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AB - Geobacter sulfurreducens is a well-studied representative of the Geobacteraceae, which play a critical role in organic matter oxidation coupled to Fe(III) reduction, bioremediation of groundwater contaminated with organics or metals, and electricity production from waste organic matter. In order to investigate G. sulfurreducens central metabolism and electron transport, a metabolic model which integrated genome-based predictions with available genetic and physiological data was developed via the constraint-based modeling approach. Evaluation of the rates of proton production and consumption in the extracellular and cytoplasmic compartments revealed that energy conservation with extracellular electron acceptors, such as Fe(III), was limited relative to that associated with intracellular acceptors. This limitation was attributed to lack of cytoplasmic proton consumption during reduction of extracellular electron acceptors. Model-based analysis of the metabolic cost of producing an extracellular electron shuttle to promote electron transfer to insoluble Fe(III) oxides demonstrated why Geobacter species, which do not produce shuttles, have an energetic advantage over shuttle-producing Fe(III) reducers in subsurface environments. In silico analysis also revealed that the metabolic network of G. sulfurreducens could synthesize amino acids more efficiently than that of Escherichia coli due to the presence of a pyruvate-ferredoxin oxidoreductase, which catalyzes synthesis of pyruvate from acetate and carbon dioxide in a single step. In silico phenotypic analysis of deletion mutants demonstrated the capability of the model to explore the flexibility of G. sulfurreducens central metabolism and correctly predict mutant phenotypes. These results demonstrate that iterative modeling coupled with experimentation can accelerate the understanding of the physiology of poorly studied but environmentally relevant organisms and may help optimize their practical applications.

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KW - Electron Transport

KW - Escherichia coli

KW - Fumarates

KW - Geobacter

KW - Iron

KW - Models, Biological

KW - Mutation

KW - Oxidation-Reduction

KW - Phenotype

KW - Protons

KW - Quinones

KW - Species Specificity

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VL - 72

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JO - Applied and Environmental Microbiology

JF - Applied and Environmental Microbiology

SN - 0099-2240

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ER -