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Title: Rational engineering of Geobacter sulfurreducens electron transfer components: A foundation for building improved Geobacter-based bioelectrochemical technologies

Abstract

Multiheme cytochromes have been implicated in Geobacter sulfurreducens extracellular electron transfer (EET). These proteins are potential targets to improve EET and enhance bioremediation and electrical current production by G. sulfurreducens. However, the functional characterization of multiheme cytochromes is particularly complex due to the co-existence of several microstates in solution, connecting the fully reduced and fully oxidized states. Throughout the last decade, new strategies have been developed to characterize multiheme redox proteins functionally and structurally. These strategies were used to reveal the functional mechanism of G. sulfurreducens multiheme cytochromes and also to identify key residues in these proteins for EET. In previous studies, we set the foundations for enhancement of the EET abilities of G. sulfurreducens by characterizing a family of five triheme cytochromes (PpcA-E). These periplasmic cytochromes are implicated in electron transfer between the oxidative reactions of metabolism in the cytoplasm and the reduction of extracellular terminal electron acceptors at the cell's outer surface. The results obtained suggested that PpcA can couple e-/H+ transfer, a property that might contribute to the proton electrochemical gradient across the cytoplasmic membrane for metabolic energy production. The structural and functional properties of PpcA were characterized in detail and used for rational design of amore » family of 23 single site PpcA mutants. In this review, we summarize the functional characterization of the native and mutant proteins. Mutants that retain the mechanistic features of PpcA and adopt preferential e-/H+ transfer pathways at lower reduction potential values compared to the wild-type protein were selected for in vivo studies as the best candidates to increase the electron transfer rate of G. sulfurreducens. For the first time G. sulfurreducens strains have been manipulated by the introduction of mutant forms of essential proteins with the aim to develop and improve bioelectrochemical technologies.« less

Authors:
 [1];  [1];  [2];  [3];  [4];  [4];  [4];  [1]
  1. Univ. Nova de Lisboa, Caparica (Portugal)
  2. Towson Univ., Towson, MD (United States)
  3. Instituto de Quimica-Fisica "Rocasolano", Madrid (Spain)
  4. Argonne National Lab. (ANL), Lemont, IL (United States)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1224905
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Geobacter; cytochrome c; multiheme; extracellular electron transfer; Geobacter mutant strains

Citation Formats

Dantas, Joana M., Morgado, Leonor, Aklujkar, Muktak, Bruix, Marta, Londer, Yuri Y., Schiffer, Marianne, Pokkuluri, P. Raj, and Salgueiro, Carlos A. Rational engineering of Geobacter sulfurreducens electron transfer components: A foundation for building improved Geobacter-based bioelectrochemical technologies. United States: N. p., 2015. Web. doi:10.3389/fmicb.2015.00752.
Dantas, Joana M., Morgado, Leonor, Aklujkar, Muktak, Bruix, Marta, Londer, Yuri Y., Schiffer, Marianne, Pokkuluri, P. Raj, & Salgueiro, Carlos A. Rational engineering of Geobacter sulfurreducens electron transfer components: A foundation for building improved Geobacter-based bioelectrochemical technologies. United States. https://doi.org/10.3389/fmicb.2015.00752
Dantas, Joana M., Morgado, Leonor, Aklujkar, Muktak, Bruix, Marta, Londer, Yuri Y., Schiffer, Marianne, Pokkuluri, P. Raj, and Salgueiro, Carlos A. 2015. "Rational engineering of Geobacter sulfurreducens electron transfer components: A foundation for building improved Geobacter-based bioelectrochemical technologies". United States. https://doi.org/10.3389/fmicb.2015.00752. https://www.osti.gov/servlets/purl/1224905.
@article{osti_1224905,
title = {Rational engineering of Geobacter sulfurreducens electron transfer components: A foundation for building improved Geobacter-based bioelectrochemical technologies},
author = {Dantas, Joana M. and Morgado, Leonor and Aklujkar, Muktak and Bruix, Marta and Londer, Yuri Y. and Schiffer, Marianne and Pokkuluri, P. Raj and Salgueiro, Carlos A.},
abstractNote = {Multiheme cytochromes have been implicated in Geobacter sulfurreducens extracellular electron transfer (EET). These proteins are potential targets to improve EET and enhance bioremediation and electrical current production by G. sulfurreducens. However, the functional characterization of multiheme cytochromes is particularly complex due to the co-existence of several microstates in solution, connecting the fully reduced and fully oxidized states. Throughout the last decade, new strategies have been developed to characterize multiheme redox proteins functionally and structurally. These strategies were used to reveal the functional mechanism of G. sulfurreducens multiheme cytochromes and also to identify key residues in these proteins for EET. In previous studies, we set the foundations for enhancement of the EET abilities of G. sulfurreducens by characterizing a family of five triheme cytochromes (PpcA-E). These periplasmic cytochromes are implicated in electron transfer between the oxidative reactions of metabolism in the cytoplasm and the reduction of extracellular terminal electron acceptors at the cell's outer surface. The results obtained suggested that PpcA can couple e-/H+ transfer, a property that might contribute to the proton electrochemical gradient across the cytoplasmic membrane for metabolic energy production. The structural and functional properties of PpcA were characterized in detail and used for rational design of a family of 23 single site PpcA mutants. In this review, we summarize the functional characterization of the native and mutant proteins. Mutants that retain the mechanistic features of PpcA and adopt preferential e-/H+ transfer pathways at lower reduction potential values compared to the wild-type protein were selected for in vivo studies as the best candidates to increase the electron transfer rate of G. sulfurreducens. For the first time G. sulfurreducens strains have been manipulated by the introduction of mutant forms of essential proteins with the aim to develop and improve bioelectrochemical technologies.},
doi = {10.3389/fmicb.2015.00752},
url = {https://www.osti.gov/biblio/1224905}, journal = {Frontiers in Microbiology},
issn = {1664-302X},
number = ,
volume = 6,
place = {United States},
year = {Thu Jul 30 00:00:00 EDT 2015},
month = {Thu Jul 30 00:00:00 EDT 2015}
}

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Cited by: 28 works
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Works referenced in this record:

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Structural insights into the modulation of the redox properties of two Geobacter sulfurreducens homologous triheme cytochromes
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Solution structure of a mutant of the triheme cytochrome PpcA from Geobacter sulfurreducens sheds light on the role of the conserved aromatic residue F15
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Microbial reduction of uranium
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Genome of Geobacter sulfurreducens: Metal Reduction in Subsurface Environments
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One simple step in the identification of the cofactors signals, one giant leap for the solution structure determination of multiheme proteins
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Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens
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Proteome of Geobacter sulfurreducens grown with Fe(III) oxide or Fe(III) citrate as the electron acceptor
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The role of intramolecular interactions in the functional control of multiheme cytochromes c
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Nomenclature of tetrapyrroles. Recommendations 1986
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Selection of a variant of Geobacter sulfurreducens with enhanced capacity for current production in microbial fuel cells
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Structural characterization of a family of cytochromes c7 involved in Fe(III) respiration by Geobacter sulfurreducens
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Pivotal role of the strictly conserved aromatic residue F15 in the cytochrome c 7 family
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Revealing the structural origin of the redox-Bohr effect: the first solution structure of a cytochrome from Geobacter sulfurreducens
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Outer membrane cytochrome c , OmcF, from Geobacter sulfurreducens : High structural similarity to an algal cytochrome c 6
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Molecular interaction studies revealed the bifunctional behavior of triheme cytochrome PpcA from Geobacter sulfurreducens toward the redox active analog of humic substances
journal, October 2015


The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions
journal, July 2006


Structure of a novel c 7 -type three-heme cytochrome domain from a multidomain cytochrome c polymer
journal, June 2004


Heterologous expression of dodecaheme “nanowire” cytochromes c from Geobacter sulfurreducens
journal, May 2006


Production and preliminary characterization of a recombinant triheme cytochrome c7 from Geobacter sulfurreducens in Escherichia coli
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Fine Tuning of Redox Networks on Multiheme Cytochromes from Geobacter sulfurreducens Drives Physiological Electron/Proton Energy Transduction
journal, January 2012


NMR Studies of Cooperativity in the Tetrahaem Cytochrome c3 from Desulfovibrio vulgaris
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Going Wireless: Fe(III) Oxide Reduction without Pili by Geobacter sulfurreducens Strain JS-1
journal, May 2014


Redox Linked Conformational Changes in Cytochrome c 3 from Desulfovibrio desulfuricans ATCC 27774
journal, November 2010


Heterologous expression of hexaheme fragments of a multidomain cytochrome from Geobacter sulfurreducens representing a novel class of cytochromes c
journal, February 2005


Backbone, side chain and heme resonance assignments of the triheme cytochrome PpcA from Geobacter sulfurreducens
journal, November 2010


Redox-linked conformational changes of a multiheme cytochrome from Geobacter sulfurreducens
journal, August 2007


Fluorescent properties of c-type cytochromes reveal their potential role as an extracytoplasmic electron sink in Geobacter sulfurreducens
journal, February 2008


Overexpression of multi-heme C-type cytochromes
journal, February 2005


Backbone, side chain and heme resonance assignments of the triheme cytochrome PpcD from Geobacter sulfurreducens
journal, September 2014


Isotopic labeling of c-type multiheme cytochromes overexpressed in E. coli
journal, May 2008


Role of Met58 in the regulation of electron/proton transfer in trihaem cytochrome PpcA from Geobacter sulfurreducens
journal, November 2012


Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens
journal, October 2006


Novel Mode of Microbial Energy Metabolism: Organic Carbon Oxidation Coupled to Dissimilatory Reduction of Iron or Manganese
journal, January 1988


Structure of a novel c 7-type three-heme cytochrome domain from a multidomain cytochrome c polymer
journal, February 2009


Backbone, side chain and heme resonance assignments of the triheme cytochrome PpcD from Geobacter sulfurreducens
dataset, January 2017


Outer membrane cytochrome c , OmcF, from Geobacter sulfurreducens : High structural similarity to an algal cytochrome c 6
journal, January 2009


Pivotal role of the strictly conserved aromatic residue F15 in the cytochrome c 7 family
journal, July 2011


Backbone, side chain and heme resonance assignments of the triheme cytochrome PpcA from Geobacter sulfurreducens
journal, November 2010


Backbone, side chain and heme resonance assignments of the triheme cytochrome PpcD from Geobacter sulfurreducens
journal, September 2014


Structural insights into the modulation of the redox properties of two Geobacter sulfurreducens homologous triheme cytochromes
journal, September 2008


Structural characterization of a family of cytochromes c7 involved in Fe(III) respiration by Geobacter sulfurreducens
journal, February 2010


Solution structure of a mutant of the triheme cytochrome PpcA from Geobacter sulfurreducens sheds light on the role of the conserved aromatic residue F15
journal, April 2013


Molecular interaction studies revealed the bifunctional behavior of triheme cytochrome PpcA from Geobacter sulfurreducens toward the redox active analog of humic substances
journal, October 2015


The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions
journal, July 2006


Proteome of Geobacter sulfurreducens grown with Fe(III) oxide or Fe(III) citrate as the electron acceptor
journal, December 2008


Redox-linked conformational changes of a multiheme cytochrome from Geobacter sulfurreducens
journal, August 2007


One simple step in the identification of the cofactors signals, one giant leap for the solution structure determination of multiheme proteins
journal, March 2010


Selection of a variant of Geobacter sulfurreducens with enhanced capacity for current production in microbial fuel cells
journal, August 2009


The role of intramolecular interactions in the functional control of multiheme cytochromes c
journal, August 2011


Heterologous expression of hexaheme fragments of a multidomain cytochrome from Geobacter sulfurreducens representing a novel class of cytochromes c
journal, February 2005


Isotopic labeling of c-type multiheme cytochromes overexpressed in E. coli
journal, May 2008


Redox Linked Conformational Changes in Cytochrome c 3 from Desulfovibrio desulfuricans ATCC 27774
journal, November 2010


Microbial reduction of uranium
journal, April 1991


Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens
journal, January 2003


Structure of a novel c 7 -type three-heme cytochrome domain from a multidomain cytochrome c polymer
journal, June 2004


Nomenclature of tetrapyrroles. Recommendations 1986
journal, December 1988


NMR Studies of Cooperativity in the Tetrahaem Cytochrome c3 from Desulfovibrio vulgaris
journal, November 1996


Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens
journal, October 2006


Fluorescent properties of c-type cytochromes reveal their potential role as an extracytoplasmic electron sink in Geobacter sulfurreducens
journal, February 2008


Genome of Geobacter sulfurreducens: Metal Reduction in Subsurface Environments
journal, December 2003


Role of Geobacter sulfurreducens Outer Surface c-Type Cytochromes in Reduction of Soil Humic Acid and Anthraquinone-2,6-Disulfonate
journal, February 2010


Outer Membrane c-Type Cytochromes Required for Fe(III) and Mn(IV) Oxide Reduction in Geobacter sulfurreducens
journal, December 2005


OmcB, a c-Type Polyheme Cytochrome, Involved in Fe(III) Reduction in Geobacter sulfurreducens
journal, April 2003


An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors
journal, November 2014


Fine Tuning of Redox Networks on Multiheme Cytochromes from Geobacter sulfurreducens Drives Physiological Electron/Proton Energy Transduction
journal, January 2012


Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens
journal, January 2007


Works referencing / citing this record:

Potential regulates metabolism and extracellular respiration of electroactive Geobacter biofilm
journal, February 2019


Silica immobilization of Geobacter sulfurreducens for constructing ready-to-use artificial bioelectrodes
journal, April 2017


Potential of Zymomonas mobilis as an electricity producer in ethanol production
journal, March 2020


The triheme cytochrome PpcF from Geobacter metallireducens exhibits distinct redox properties
journal, November 2018