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 designmore »
- 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 Lab. (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
- OSTI Identifier:
- 1224905
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- 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. doi: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. Thu .
"Rational engineering of Geobacter sulfurreducens electron transfer components: A foundation for building improved Geobacter-based bioelectrochemical technologies". United States. doi: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},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {2015},
month = {7}
}
Web of Science
Works referenced in this record:
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
- Dantas, Joana M.; Kokhan, Oleksandr; Pokkuluri, P. Raj
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 10
Evidence for interaction between the triheme cytochrome PpcA from Geobacter sulfurreducens and anthrahydroquinone-2,6-disulfonate, an analog of the redox active components of humic substances
journal, June 2014
- Dantas, Joana M.; Morgado, Leonor; Catarino, Teresa
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 6
Pivotal role of the strictly conserved aromatic residue F15 in the cytochrome c 7 family
journal, July 2011
- Dantas, Joana M.; Morgado, Leonor; Londer, Yuri Y.
- JBIC Journal of Biological Inorganic Chemistry, Vol. 17, Issue 1
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
- Dantas, Joana M.; Morgado, Leonor; Pokkuluri, P. Raj
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 4
Backbone, side chain and heme resonance assignments of the triheme cytochrome PpcD from Geobacter sulfurreducens
journal, September 2014
- Dantas, Joana M.; Salgueiro, Carlos A.; Bruix, Marta
- Biomolecular NMR Assignments, Vol. 9, Issue 1
Orientation of the axial ligands and magnetic properties of the hemes in the cytochrome c7 family from Geobacter sulfurreducens determined by paramagnetic NMR
journal, January 2011
- Dantas, Joana M.; Saraiva, Ivo H.; Morgado, Leonor
- Dalton Transactions, Vol. 40, Issue 47
Proteome of Geobacter sulfurreducens grown with Fe(III) oxide or Fe(III) citrate as the electron acceptor
journal, December 2008
- Ding, Yan-Huai R.; Hixson, Kim K.; Aklujkar, Muktak A.
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1784, Issue 12
The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions
journal, July 2006
- Ding, Yan-Huai R.; Hixson, Kim K.; Giometti, Carol S.
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1764, Issue 7
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
Isotopic labeling of c-type multiheme cytochromes overexpressed in E. coli
journal, May 2008
- Fernandes, Ana P.; Couto, Isabel; Morgado, Leonor
- Protein Expression and Purification, Vol. 59, Issue 1
The role of intramolecular interactions in the functional control of multiheme cytochromes c
journal, August 2011
- Fonseca, Bruno M.; Paquete, Catarina M.; Salgueiro, Carlos A.
- FEBS Letters, Vol. 586, Issue 5
Efficient and selective isotopic labeling of hemes to facilitate the study of multiheme proteins
journal, April 2012
- Fonseca, Bruno; Tien, Ming; Rivera, Mario
- BioTechniques
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
OmcF, a Putative c-Type Monoheme Outer Membrane Cytochrome Required for the Expression of Other Outer Membrane Cytochromes in Geobacter sulfurreducens
journal, June 2005
- Kim, B. -C.; Leang, C.; Ding, Y. -H. R.
- Journal of Bacteriology, Vol. 187, Issue 13
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
Insights into genes involved in electricity generation in Geobacter sulfurreducens via whole genome microarray analysis of the OmcF-deficient mutant
journal, June 2008
- Kim, Byoung-Chan; Postier, Bradley L.; DiDonato, Raymond J.
- Bioelectrochemistry, Vol. 73, Issue 1
OmcB, a c-Type Polyheme Cytochrome, Involved in Fe(III) Reduction in Geobacter sulfurreducens
journal, April 2003
- Leang, C.; Coppi, M. V.; Lovley, D. R.
- Journal of Bacteriology, Vol. 185, Issue 7
An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors
journal, November 2014
- Levar, Caleb E.; Chan, Chi Ho; Mehta-Kolte, Misha G.
- mBio, Vol. 5, Issue 6
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
- Liu, Yimo; Wang, Zheming; Liu, Juan
- Environmental Microbiology Reports, Vol. 6, Issue 6
Heterologous expression of hexaheme fragments of a multidomain cytochrome from Geobacter sulfurreducens representing a novel class of cytochromes c
journal, February 2005
- Londer, Yuri Y.; Raj Pokkuluri, P.; Erickson, Jill
- Protein Expression and Purification, Vol. 39, Issue 2
Heterologous expression of dodecaheme “nanowire” cytochromes c from Geobacter sulfurreducens
journal, May 2006
- Londer, Yuri Y.; Pokkuluri, P. Raj; Orshonsky, Valerie
- Protein Expression and Purification, Vol. 47, Issue 1
Production and preliminary characterization of a recombinant triheme cytochrome c7 from Geobacter sulfurreducens in Escherichia coli
journal, July 2002
- Londer, Yuri Y.; Pokkuluri, P. Raj; Tiede, David M.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1554, Issue 3
Microbial reduction of uranium
journal, April 1991
- Lovley, Derek R.; Phillips, Elizabeth J. P.; Gorby, Yuri A.
- Nature, Vol. 350, Issue 6317
Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism
journal, November 1987
- Lovley, Derek R.; Stolz, John F.; Nord, Gordon L.
- Nature, Vol. 330, Issue 6145
Outer Membrane c-Type Cytochromes Required for Fe(III) and Mn(IV) Oxide Reduction in Geobacter sulfurreducens
journal, December 2005
- Mehta, T.; Coppi, M. V.; Childers, S. E.
- Applied and Environmental Microbiology, Vol. 71, Issue 12
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
Redox-linked conformational changes of a multiheme cytochrome from Geobacter sulfurreducens
journal, August 2007
- Morgado, Leonor; Bruix, Marta; Londer, Yuri Y.
- Biochemical and Biophysical Research Communications, Vol. 360, Issue 1
Structural insights into the modulation of the redox properties of two Geobacter sulfurreducens homologous triheme cytochromes
journal, September 2008
- Morgado, Leonor; Bruix, Marta; Orshonsky, Valerie
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1777, Issue 9
Thermodynamic Characterization of a Triheme Cytochrome Family from Geobacter sulfurreducens Reveals Mechanistic and Functional Diversity
journal, July 2010
- Morgado, Leonor; Bruix, Marta; Pessanha, Miguel
- Biophysical Journal, Vol. 99, Issue 1
Fine Tuning of Redox Networks on Multiheme Cytochromes from Geobacter sulfurreducens Drives Physiological Electron/Proton Energy Transduction
journal, January 2012
- Morgado, Leonor; Dantas, Joana M.; Bruix, Marta
- Bioinorganic Chemistry and Applications, Vol. 2012
Role of Met58 in the regulation of electron/proton transfer in trihaem cytochrome PpcA from Geobacter sulfurreducens
journal, November 2012
- Morgado, Leonor; Dantas, Joana M.; Simões, Telma
- Bioscience Reports, Vol. 33, Issue 1
One simple step in the identification of the cofactors signals, one giant leap for the solution structure determination of multiheme proteins
journal, March 2010
- Morgado, Leonor; Fernandes, Ana P.; Londer, Yuri Y.
- Biochemical and Biophysical Research Communications, Vol. 393, Issue 3
Dissecting the Functional Role of Key Residues in Triheme Cytochrome PpcA: A Path to Rational Design of G. sulfurreducens Strains with Enhanced Electron Transfer Capabilities
journal, August 2014
- Morgado, Leonor; Lourenço, Sílvia; Londer, Yuri Y.
- PLoS ONE, Vol. 9, Issue 8
Backbone, side chain and heme resonance assignments of the triheme cytochrome PpcA from Geobacter sulfurreducens
journal, November 2010
- Morgado, Leonor; Paixão, Vitor B.; Salgueiro, Carlos A.
- Biomolecular NMR Assignments, Vol. 5, Issue 1
Revealing the structural origin of the redox-Bohr effect: the first solution structure of a cytochrome from Geobacter sulfurreducens
journal, December 2011
- Morgado, Leonor; Paixão, Vítor B.; Schiffer, Marianne
- Biochemical Journal, Vol. 441, Issue 1
Orientation of the axial ligands and magnetic properties of the hemes in the triheme ferricytochrome PpcA from G. sulfurreducens determined by paramagnetic NMR
journal, July 2010
- Morgado, Leonor; Saraiva, Ivo H.; Louro, Ricardo O.
- FEBS Letters, Vol. 584, Issue 15
Nomenclature of tetrapyrroles. Recommendations 1986
journal, December 1988
- Moss, Gerard P.
- European Journal of Biochemistry, Vol. 178, Issue 2
Anode Biofilm Transcriptomics Reveals Outer Surface Components Essential for High Density Current Production in Geobacter sulfurreducens Fuel Cells
journal, May 2009
- Nevin, Kelly P.; Kim, Byoung-Chan; Glaven, Richard H.
- PLoS ONE, Vol. 4, Issue 5
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
Redox Linked Conformational Changes in Cytochrome c 3 from Desulfovibrio desulfuricans ATCC 27774
journal, November 2010
- Paixão, Vitor B.; Vis, Hans; Turner, David L.
- Biochemistry, Vol. 49, Issue 44
Redox Characterization of Geobacter sulfurreducens Cytochrome c 7 : Physiological Relevance of the Conserved Residue F15 Probed by Site-Specific Mutagenesis †
journal, August 2004
- Pessanha, Miguel; Londer, Yuri Y.; Long, W. Chris
- Biochemistry, Vol. 43, Issue 30
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.
- Biochemistry, Vol. 45, Issue 46
Structure of a novel c 7 -type three-heme cytochrome domain from a multidomain cytochrome c polymer
journal, June 2004
- Pokkuluri, P. Raj; Londer, Yuri Y.; Duke, Norma E. C.
- Protein Science, Vol. 13, Issue 6
Family of Cytochrome c 7 -Type Proteins from Geobacter sulfurreducens : Structure of One Cytochrome c 7 at 1.45 Å Resolution † , ‡
journal, February 2004
- Pokkuluri, P. Raj; Londer, Yuri Y.; Duke, Norma E. C.
- Biochemistry, Vol. 43, Issue 4
Outer membrane cytochrome c , OmcF, from Geobacter sulfurreducens : High structural similarity to an algal cytochrome c 6
journal, January 2009
- Pokkuluri, P. R.; Londer, Y. Y.; Wood, S. J.
- Proteins: Structure, Function, and Bioinformatics, Vol. 74, Issue 1
Structural characterization of a family of cytochromes c7 involved in Fe(III) respiration by Geobacter sulfurreducens
journal, February 2010
- Pokkuluri, P. R.; Londer, Y. Y.; Yang, X.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 2
Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens
journal, January 2007
- Shelobolina, Evgenya S.; Coppi, Maddalena V.; Korenevsky, Anton A.
- BMC Microbiology, Vol. 7, Issue 1
Overexpression of multi-heme C-type cytochromes
journal, February 2005
- Shi, Liang; Lin, Jiann-Trzwo; Markillie, Lye M.
- BioTechniques, Vol. 38, Issue 2
Going Wireless: Fe(III) Oxide Reduction without Pili by Geobacter sulfurreducens Strain JS-1
journal, May 2014
- Smith, Jessica A.; Tremblay, Pier-Luc; Shrestha, Pravin Malla
- Applied and Environmental Microbiology, Vol. 80, Issue 14
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
Role of Geobacter sulfurreducens Outer Surface c-Type Cytochromes in Reduction of Soil Humic Acid and Anthraquinone-2,6-Disulfonate
journal, February 2010
- Voordeckers, J. W.; Kim, B. -C.; Izallalen, M.
- Applied and Environmental Microbiology, Vol. 76, Issue 7
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
- Biosensors and Bioelectronics, Vol. 24, Issue 12, p. 3498-3503