Fine Tuning of Redox Networks on Multiheme Cytochromes from Geobacter sulfurreducens Drives Physiological Electron/Proton Energy Transduction
Abstract
The bacteriumGeobacter sulfurreducens (Gs)can grow in the presence of extracellular terminal acceptors, a property that is currently explored to harvest electricity from aquatic sediments and waste organic matter into microbial fuel cells. A family composed of five triheme cytochromes (PpcA-E) was identified inGs. These cytochromes play a crucial role by bridging the electron transfer from oxidation of cytoplasmic donors to the cell exterior and assisting the reduction of extracellular terminal acceptors. The detailed thermodynamic characterization of such proteins showed that PpcA and PpcD have an important redox-Bohr effect that might implicate these proteins in the e-/H+coupling mechanisms to sustain cellular growth. The physiological relevance of the redox-Bohr effect in these proteins was studied by determining the fractional contribution of each individual redox-microstate at different pH values. For both proteins, oxidation progresses from a particular protonated microstate to a particular deprotonated one, over specific pH ranges. The preferred e-/H+transfer pathway established by the selected microstates indicates that both proteins are functionally designed to couple e-/H+transfer at the physiological pH range for cellular growth.
- Authors:
-
- Universidade Nova de Lisboa, Campus Caparica, Caparica (Portugal). Faculdade de Ciências e Tecnologia. Departamento de Química. Requimte-CQFB
- Instituto de Química-Física “Rocasolano”, Madrid (Spain). CSIC. Departamento de Espectroscopía y Estructura Molecular
- Argonne National Lab. (ANL), Argonne, 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). Biological Systems Science Division
- OSTI Identifier:
- 1626203
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Bioinorganic Chemistry and Applications
- Additional Journal Information:
- Journal Volume: 2012; Journal ID: ISSN 1565-3633
- Publisher:
- Hindawi
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Biochemistry & Molecular Biology; Chemistry
Citation Formats
Morgado, Leonor, Dantas, Joana M., Bruix, Marta, Londer, Yuri Y., and Salgueiro, Carlos A. Fine Tuning of Redox Networks on Multiheme Cytochromes from Geobacter sulfurreducens Drives Physiological Electron/Proton Energy Transduction. United States: N. p., 2012.
Web. doi:10.1155/2012/298739.
Morgado, Leonor, Dantas, Joana M., Bruix, Marta, Londer, Yuri Y., & Salgueiro, Carlos A. Fine Tuning of Redox Networks on Multiheme Cytochromes from Geobacter sulfurreducens Drives Physiological Electron/Proton Energy Transduction. United States. https://doi.org/10.1155/2012/298739
Morgado, Leonor, Dantas, Joana M., Bruix, Marta, Londer, Yuri Y., and Salgueiro, Carlos A. Sun .
"Fine Tuning of Redox Networks on Multiheme Cytochromes from Geobacter sulfurreducens Drives Physiological Electron/Proton Energy Transduction". United States. https://doi.org/10.1155/2012/298739. https://www.osti.gov/servlets/purl/1626203.
@article{osti_1626203,
title = {Fine Tuning of Redox Networks on Multiheme Cytochromes from Geobacter sulfurreducens Drives Physiological Electron/Proton Energy Transduction},
author = {Morgado, Leonor and Dantas, Joana M. and Bruix, Marta and Londer, Yuri Y. and Salgueiro, Carlos A.},
abstractNote = {The bacteriumGeobacter sulfurreducens (Gs)can grow in the presence of extracellular terminal acceptors, a property that is currently explored to harvest electricity from aquatic sediments and waste organic matter into microbial fuel cells. A family composed of five triheme cytochromes (PpcA-E) was identified inGs. These cytochromes play a crucial role by bridging the electron transfer from oxidation of cytoplasmic donors to the cell exterior and assisting the reduction of extracellular terminal acceptors. The detailed thermodynamic characterization of such proteins showed that PpcA and PpcD have an important redox-Bohr effect that might implicate these proteins in the e-/H+coupling mechanisms to sustain cellular growth. The physiological relevance of the redox-Bohr effect in these proteins was studied by determining the fractional contribution of each individual redox-microstate at different pH values. For both proteins, oxidation progresses from a particular protonated microstate to a particular deprotonated one, over specific pH ranges. The preferred e-/H+transfer pathway established by the selected microstates indicates that both proteins are functionally designed to couple e-/H+transfer at the physiological pH range for cellular growth.},
doi = {10.1155/2012/298739},
journal = {Bioinorganic Chemistry and Applications},
number = ,
volume = 2012,
place = {United States},
year = {Sun Jan 01 00:00:00 EST 2012},
month = {Sun Jan 01 00:00:00 EST 2012}
}
Works referenced in this record:
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
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
Bug juice: harvesting electricity with microorganisms
journal, July 2006
- Lovley, Derek R.
- Nature Reviews Microbiology, Vol. 4, Issue 7, p. 497-508
Proton thrusters: overview of the structural and functional features of soluble tetrahaem cytochromes c 3
journal, September 2006
- Louro, Ricardo O.
- JBIC Journal of Biological Inorganic Chemistry, Vol. 12, Issue 1
Carbonate Species as OH − Carriers for Decreasing the pH Gradient between Cathode and Anode in Biological Fuel Cells
journal, December 2008
- Torres, César I.; Lee, Hyung-Sool; Rittmann, Bruce E.
- Environmental Science & Technology, Vol. 42, Issue 23
Optimization of culture conditions and electricity generation using Geobacter sulfurreducens in a dual-chambered microbial fuel-cell
journal, December 2010
- Kim, Mi-Sun; Lee, Yu-jin
- International Journal of Hydrogen Energy, Vol. 35, Issue 23
pH, redox potential and local biofilm potential microenvironments within Geobacter sulfurreducens biofilms and their roles in electron transfer
journal, May 2012
- Babauta, Jerome T.; Nguyen, Hung Duc; Harrington, Timothy D.
- Biotechnology and Bioengineering, Vol. 109, Issue 10
Proton transport inside the biofilm limits electrical current generation by anode-respiring bacteria
journal, August 2008
- Torres, César I.; Kato Marcus, Andrew; Rittmann, Bruce E.
- Biotechnology and Bioengineering, Vol. 100, Issue 5
Microbial Biofilm Voltammetry: Direct Electrochemical Characterization of Catalytic Electrode-Attached Biofilms
journal, October 2008
- Marsili, E.; Rollefson, J. B.; Baron, D. B.
- Applied and Environmental Microbiology, Vol. 74, Issue 23
Redox-Bohr effect in electron/proton energy transduction: cytochrome c
3 coupled to hydrogenase works as a 'proton thruster' in Desulfovibrio vulgaris
journal, August 1997
- Louro, Ricardo O.; Catarino, Teresa; LeGall, Jean
- JBIC Journal of Biological Inorganic Chemistry, Vol. 2, Issue 4
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
Characterization of Proton Production and Consumption Associated with Microbial Metabolism
journal, January 2010
- Srinivasan, Karthikeyan; Mahadevan, Radhakrishnan
- BMC Biotechnology, Vol. 10, Issue 1
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
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
Evidence that OmcB and OmpB of Geobacter sulfurreducens are outer membrane surface proteins
journal, December 2007
- Qian, Xinlei; Reguera, Gemma; Mester, Tünde
- FEMS Microbiology Letters, Vol. 277, Issue 1
Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes
journal, January 2010
- Butler, Jessica E.; Young, Nelson D.; Lovley, Derek R.
- BMC Genomics, Vol. 11, Issue 1
Cyclic voltammetry of biofilms of wild type and mutant Geobacter sulfurreducens on fuel cell anodes indicates possible roles of OmcB, OmcZ, type IV pili, and protons in extracellular electron transfer
journal, January 2009
- Richter, Hanno; Nevin, Kelly P.; Jia, Hongfei
- Energy & Environmental Science, Vol. 2, Issue 5
Characterization of Metabolism in the Fe(III)-Reducing Organism Geobacter sulfurreducens by Constraint-Based Modeling
journal, February 2006
- Mahadevan, R.; Bond, D. R.; Butler, J. E.
- Applied and Environmental Microbiology, Vol. 72, Issue 2
Linking Spectral and Electrochemical Analysis to Monitor c-type Cytochrome Redox Status in Living Geobacter sulfurreducens Biofilms
journal, June 2011
- Liu, Ying; Kim, Hoseang; Franklin, Rhonda R.
- ChemPhysChem, Vol. 12, Issue 12
Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe(III) reduction in Geobacter sulfurreducens
journal, April 2011
- Qian, Xinlei; Mester, Tünde; Morgado, Leonor
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 4
The history and the hypotheses concerning ATP-formation by energised protons
journal, January 1978
- Williams, R. J. P.
- FEBS Letters, Vol. 85, Issue 1
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
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
Electrochemical characterization ofGeobacter sulfurreducens cells immobilized on graphite paper electrodes
journal, January 2008
- Srikanth, Shweta; Marsili, Enrico; Flickinger, Michael C.
- Biotechnology and Bioengineering, Vol. 99, Issue 5
Electrochemical characterization ofGeobacter sulfurreducens cells immobilized on graphite paper electrodes
journal, January 2008
- Srikanth, Shweta; Marsili, Enrico; Flickinger, Michael C.
- Biotechnology and Bioengineering, Vol. 99, Issue 5
Proton transport inside the biofilm limits electrical current generation by anode-respiring bacteria
journal, August 2008
- Torres, César I.; Kato Marcus, Andrew; Rittmann, Bruce E.
- Biotechnology and Bioengineering, Vol. 100, Issue 5
Linking Spectral and Electrochemical Analysis to Monitor c-type Cytochrome Redox Status in Living Geobacter sulfurreducens Biofilms
journal, June 2011
- Liu, Ying; Kim, Hoseang; Franklin, Rhonda R.
- ChemPhysChem, Vol. 12, Issue 12
The history and the hypotheses concerning ATP-formation by energised protons
journal, January 1978
- Williams, R. J. P.
- FEBS Letters, Vol. 85, 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
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
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
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
Carbonate Species as OH − Carriers for Decreasing the pH Gradient between Cathode and Anode in Biological Fuel Cells
journal, December 2008
- Torres, César I.; Lee, Hyung-Sool; Rittmann, Bruce E.
- Environmental Science & Technology, Vol. 42, Issue 23
Bug juice: harvesting electricity with microorganisms
journal, July 2006
- Lovley, Derek R.
- Nature Reviews Microbiology, Vol. 4, Issue 7, p. 497-508
Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens
journal, January 2003
- Lloyd, Jon R.; Leang, Ching; Myerson, Allison L. HODGES
- Biochemical Journal, Vol. 369, Issue 1
Evidence that OmcB and OmpB of Geobacter sulfurreducens are outer membrane surface proteins
journal, December 2007
- Qian, Xinlei; Reguera, Gemma; Mester, Tünde
- FEMS Microbiology Letters, Vol. 277, Issue 1
Purification and Characterization of OmcZ, an Outer-Surface, Octaheme c-Type Cytochrome Essential for Optimal Current Production by Geobacter sulfurreducens
journal, April 2010
- Inoue, K.; Qian, X.; Morgado, L.
- Applied and Environmental Microbiology, Vol. 76, Issue 12
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
Works referencing / citing this record:
Rational engineering of Geobacter sulfurreducens electron transfer components: a foundation for building improved Geobacter-based bioelectrochemical technologies
journal, July 2015
- Dantas, Joana M.; Morgado, Leonor; Aklujkar, Muktak
- Frontiers in Microbiology, Vol. 6
Rational engineering of Geobacter sulfurreducens electron transfer components: a foundation for building improved Geobacter-based bioelectrochemical technologies
journal, July 2015
- Dantas, Joana M.; Morgado, Leonor; Aklujkar, Muktak
- Frontiers in Microbiology, Vol. 6
Biomolecular Interaction Studies Between Cytochrome PpcA From Geobacter sulfurreducens and the Electron Acceptor Ferric Nitrilotriacetate (Fe-NTA)
journal, November 2018
- Ferreira, Marisa R.; Salgueiro, Carlos A.
- Frontiers in Microbiology, Vol. 9