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 »
- Authors:
-
- Univ. Nova de Lisboa, Caparica (Portugal)
- Towson Univ., Towson, MD (United States)
- Instituto de Quimica-Fisica "Rocasolano", Madrid (Spain)
- 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}
}
Web of Science
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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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Molecular interaction studies revealed the bifunctional behavior of triheme cytochrome PpcA from Geobacter sulfurreducens toward the redox active analog of humic substances
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- Dantas, Joana M.; Kokhan, Oleksandr; Pokkuluri, P. Raj
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journal, March 2010
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Insights into genes involved in electricity generation in Geobacter sulfurreducens via whole genome microarray analysis of the OmcF-deficient mutant
journal, June 2008
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Selection of a variant of Geobacter sulfurreducens with enhanced capacity for current production in microbial fuel cells
journal, August 2009
- Yi, Hana; Nevin, Kelly P.; Kim, Byoung-Chan
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Thermodynamic Characterization of a Triheme Cytochrome Family from Geobacter sulfurreducens Reveals Mechanistic and Functional Diversity
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Heterologous expression of hexaheme fragments of a multidomain cytochrome from Geobacter sulfurreducens representing a novel class of cytochromes c
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Isotopic labeling of c-type multiheme cytochromes overexpressed in E. coli
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Redox Characterization of Geobacter sulfurreducens Cytochrome c 7 : Physiological Relevance of the Conserved Residue F15 Probed by Site-Specific Mutagenesis †
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- Pessanha, Miguel; Londer, Yuri Y.; Long, W. Chris
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Thermodynamic Characterization of Triheme Cytochrome PpcA from Geobacter sulfurreducens : Evidence for a Role Played in e - /H + Energy Transduction † , ‡
journal, November 2006
- Pessanha, Miguel; Morgado, Leonor; Louro, Ricardo O.
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Redox Linked Conformational Changes in Cytochrome c 3 from Desulfovibrio desulfuricans ATCC 27774
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Microbial reduction of uranium
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Orientation of the axial ligands and magnetic properties of the hemes in the cytochrome c7 family from Geobacter sulfurreducens determined by paramagnetic NMR
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A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by G eobacter sulfurreducens PCA : A trans-outer membrane electron transfer complex
journal, September 2014
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- European Journal of Biochemistry, Vol. 178, Issue 2
NMR Studies of Cooperativity in the Tetrahaem Cytochrome c3 from Desulfovibrio vulgaris
journal, November 1996
- Turner, David L.; Salgueiro, Carlos A.; Catarino, Teresa
- European Journal of Biochemistry, Vol. 241, Issue 3
Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens
journal, October 2006
- Holmes, Dawn E.; Chaudhuri, Swades K.; Nevin, Kelly P.
- Environmental Microbiology, Vol. 8, Issue 10
Fluorescent properties of c-type cytochromes reveal their potential role as an extracytoplasmic electron sink in Geobacter sulfurreducens
journal, February 2008
- Esteve-Núñez, Abraham; Sosnik, Julian; Visconti, Pablo
- Environmental Microbiology, Vol. 10, Issue 2
Power output and columbic efficiencies from biofilms of Geobacter sulfurreducens comparable to mixed community microbial fuel cells: High current production with a pure culture
journal, June 2008
- Nevin, K. P.; Richter, H.; Covalla, S. F.
- Environmental Microbiology, Vol. 10, Issue 10
Investigation of direct vs. indirect involvement of the c -type cytochrome MacA in Fe(III) reduction by Geobacter sulfurreducens
journal, September 2008
- Kim, Byoung-Chan; Lovley, Derek R.
- FEMS Microbiology Letters, Vol. 286, Issue 1
Genome of Geobacter sulfurreducens: Metal Reduction in Subsurface Environments
journal, December 2003
- Methe, B. A.; Nelson, K. E.; Eisen, J. A.
- Science, Vol. 302, Issue 5652, p. 1967-1969
Role of Geobacter sulfurreducens Outer Surface c-Type Cytochromes in Reduction of Soil Humic Acid and Anthraquinone-2,6-Disulfonate
journal, February 2010
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Outer Membrane c-Type Cytochromes Required for Fe(III) and Mn(IV) Oxide Reduction in Geobacter sulfurreducens
journal, December 2005
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OmcB, a c-Type Polyheme Cytochrome, Involved in Fe(III) Reduction in Geobacter sulfurreducens
journal, April 2003
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