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

Morgado, Leonor; Dantas, Joana M.; Bruix, Marta; Londer, Yuri Y.; Salgueiro, Carlos A.

doi:10.1155/2012/298739

Title: Fine Tuning of Redox Networks on Multiheme Cytochromes from Geobacter sulfurreducens Drives Physiological Electron/Proton Energy Transduction

Journal Article · Sun Jan 01 00:00:00 EST 2012 · Bioinorganic Chemistry and Applications

DOI:https://doi.org/10.1155/2012/298739· OSTI ID:1626203

Morgado, Leonor ^[1]; Dantas, Joana M. ^[1]; Bruix, Marta ^[2]; Londer, Yuri Y. ^[3]; Salgueiro, Carlos A. ^[1]

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)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1626203

Journal Information:: Bioinorganic Chemistry and Applications, Vol. 2012; ISSN 1565-3633

Publisher:: HindawiCopyright Statement

Country of Publication:: United States

Language:: English

References (26)

The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions Ding, Yan-Huai R.; Hixson, Kim K.; Giometti, Carol S. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1764, Issue 7 https://doi.org/10.1016/j.bbapap.2006.04.017	journal	July 2006
OmcF, a Putative c-Type Monoheme Outer Membrane Cytochrome Required for the Expression of Other Outer Membrane Cytochromes in Geobacter sulfurreducens Kim, B. -C.; Leang, C.; Ding, Y. -H. R. Journal of Bacteriology, Vol. 187, Issue 13 https://doi.org/10.1128/JB.187.13.4505-4513.2005	journal	June 2005
Bug juice: harvesting electricity with microorganisms Lovley, Derek R. Nature Reviews Microbiology, Vol. 4, Issue 7, p. 497-508 https://doi.org/10.1038/nrmicro1442	journal	July 2006
Proton thrusters: overview of the structural and functional features of soluble tetrahaem cytochromes c 3 Louro, Ricardo O. JBIC Journal of Biological Inorganic Chemistry, Vol. 12, Issue 1 https://doi.org/10.1007/s00775-006-0165-y	journal	September 2006
Carbonate Species as OH ⁻ Carriers for Decreasing the pH Gradient between Cathode and Anode in Biological Fuel Cells Torres, César I.; Lee, Hyung-Sool; Rittmann, Bruce E. Environmental Science & Technology, Vol. 42, Issue 23 https://doi.org/10.1021/es8019353	journal	December 2008
Optimization of culture conditions and electricity generation using Geobacter sulfurreducens in a dual-chambered microbial fuel-cell Kim, Mi-Sun; Lee, Yu-jin International Journal of Hydrogen Energy, Vol. 35, Issue 23 https://doi.org/10.1016/j.ijhydene.2010.04.061	journal	December 2010
pH, redox potential and local biofilm potential microenvironments within Geobacter sulfurreducens biofilms and their roles in electron transfer Babauta, Jerome T.; Nguyen, Hung Duc; Harrington, Timothy D. Biotechnology and Bioengineering, Vol. 109, Issue 10 https://doi.org/10.1002/bit.24538	journal	May 2012
Proton transport inside the biofilm limits electrical current generation by anode-respiring bacteria Torres, César I.; Kato Marcus, Andrew; Rittmann, Bruce E. Biotechnology and Bioengineering, Vol. 100, Issue 5 https://doi.org/10.1002/bit.21821	journal	August 2008
Microbial Biofilm Voltammetry: Direct Electrochemical Characterization of Catalytic Electrode-Attached Biofilms Marsili, E.; Rollefson, J. B.; Baron, D. B. Applied and Environmental Microbiology, Vol. 74, Issue 23 https://doi.org/10.1128/AEM.00177-08	journal	October 2008
Redox-Bohr effect in electron/proton energy transduction: cytochrome c 3 coupled to hydrogenase works as a 'proton thruster' in Desulfovibrio vulgaris Louro, Ricardo O.; Catarino, Teresa; LeGall, Jean JBIC Journal of Biological Inorganic Chemistry, Vol. 2, Issue 4 https://doi.org/10.1007/s007750050160	journal	August 1997
Family of Cytochrome c ₇ -Type Proteins from Geobacter sulfurreducens : Structure of One Cytochrome c ₇ at 1.45 Å Resolution ^† ^, ^‡ Pokkuluri, P. Raj; Londer, Yuri Y.; Duke, Norma E. C. Biochemistry, Vol. 43, Issue 4 https://doi.org/10.1021/bi0301439	journal	February 2004
Characterization of Proton Production and Consumption Associated with Microbial Metabolism Srinivasan, Karthikeyan; Mahadevan, Radhakrishnan BMC Biotechnology, Vol. 10, Issue 1 https://doi.org/10.1186/1472-6750-10-2	journal	January 2010
Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens Shelobolina, Evgenya S.; Coppi, Maddalena V.; Korenevsky, Anton A. BMC Microbiology, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2180-7-16	journal	January 2007
Proteome of Geobacter sulfurreducens grown with Fe(III) oxide or Fe(III) citrate as the electron acceptor Ding, Yan-Huai R.; Hixson, Kim K.; Aklujkar, Muktak A. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1784, Issue 12 https://doi.org/10.1016/j.bbapap.2008.06.011	journal	December 2008
Evidence that OmcB and OmpB of Geobacter sulfurreducens are outer membrane surface proteins Qian, Xinlei; Reguera, Gemma; Mester, TÃ¼nde FEMS Microbiology Letters, Vol. 277, Issue 1 https://doi.org/10.1111/j.1574-6968.2007.00915.x	journal	December 2007
Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes Butler, Jessica E.; Young, Nelson D.; Lovley, Derek R. BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-40	journal	January 2010
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 Richter, Hanno; Nevin, Kelly P.; Jia, Hongfei Energy & Environmental Science, Vol. 2, Issue 5 https://doi.org/10.1039/b816647a	journal	January 2009
Characterization of Metabolism in the Fe(III)-Reducing Organism Geobacter sulfurreducens by Constraint-Based Modeling Mahadevan, R.; Bond, D. R.; Butler, J. E. Applied and Environmental Microbiology, Vol. 72, Issue 2 https://doi.org/10.1128/AEM.72.2.1558-1568.2006	journal	February 2006
Linking Spectral and Electrochemical Analysis to Monitor c-type Cytochrome Redox Status in Living Geobacter sulfurreducens Biofilms Liu, Ying; Kim, Hoseang; Franklin, Rhonda R. ChemPhysChem, Vol. 12, Issue 12 https://doi.org/10.1002/cphc.201100246	journal	June 2011
Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe(III) reduction in Geobacter sulfurreducens Qian, Xinlei; Mester, Tünde; Morgado, Leonor Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 4 https://doi.org/10.1016/j.bbabio.2011.01.003	journal	April 2011
The history and the hypotheses concerning ATP-formation by energised protons Williams, R. J. P. FEBS Letters, Vol. 85, Issue 1 https://doi.org/10.1016/0014-5793(78)81238-1	journal	January 1978
Thermodynamic Characterization of a Triheme Cytochrome Family from Geobacter sulfurreducens Reveals Mechanistic and Functional Diversity Morgado, Leonor; Bruix, Marta; Pessanha, Miguel Biophysical Journal, Vol. 99, Issue 1 https://doi.org/10.1016/j.bpj.2010.04.017	journal	July 2010
Structural characterization of a family of cytochromes c7 involved in Fe(III) respiration by Geobacter sulfurreducens Pokkuluri, P. R.; Londer, Y. Y.; Yang, X. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 2 https://doi.org/10.1016/j.bbabio.2009.10.007	journal	February 2010
Electrochemical characterization ofGeobacter sulfurreducens cells immobilized on graphite paper electrodes Srikanth, Shweta; Marsili, Enrico; Flickinger, Michael C. Biotechnology and Bioengineering, Vol. 99, Issue 5 https://doi.org/10.1002/bit.21671	journal	January 2008
Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens Lloyd, Jon R.; Leang, Ching; Myerson, Allison L. HODGES Biochemical Journal, Vol. 369, Issue 1 https://doi.org/10.1042/bj20020597	journal	January 2003
Purification and Characterization of OmcZ, an Outer-Surface, Octaheme c-Type Cytochrome Essential for Optimal Current Production by Geobacter sulfurreducens Inoue, K.; Qian, X.; Morgado, L. Applied and Environmental Microbiology, Vol. 76, Issue 12 https://doi.org/10.1128/aem.00027-10	journal	April 2010

Cited By (2)

Rational engineering of Geobacter sulfurreducens electron transfer components: a foundation for building improved Geobacter-based bioelectrochemical technologies Dantas, Joana M.; Morgado, Leonor; Aklujkar, Muktak Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00752	journal	July 2015
Biomolecular Interaction Studies Between Cytochrome PpcA From Geobacter sulfurreducens and the Electron Acceptor Ferric Nitrilotriacetate (Fe-NTA) Ferreira, Marisa R.; Salgueiro, Carlos A. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02741	journal	November 2018

Similar Records

Unveiling the Structural Basis That Regulates the Energy Transduction Properties within a Family of Triheme Cytochromes from Geobacter sulfurreducens

Journal Article · Thu Oct 06 00:00:00 EDT 2016 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1626203

Dantas, Joana M.; Simões, Telma; Morgado, Leonor; +6 more

Unveiling the Structural Basis That Regulates the Energy Transduction Properties within a Family of Triheme Cytochromes from Geobacter sulfurreducens

Journal Article · Tue Sep 27 00:00:00 EDT 2016 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1626203

Dantas, Joana M.; Simões, Telma; Morgado, Leonor; +6 more

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

Journal Article · Thu Jul 30 00:00:00 EDT 2015 · Frontiers in Microbiology · OSTI ID:1626203

Dantas, Joana M.; Morgado, Leonor; Aklujkar, Muktak; +5 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Biochemistry & Molecular Biology
Chemistry

Title: Fine Tuning of Redox Networks on Multiheme Cytochromes from Geobacter sulfurreducens Drives Physiological Electron/Proton Energy Transduction

Citation Formats

References (26)

Cited By (2)

Similar Records

Related Subjects