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Thermodynamic Characterization of Triheme Cytochrome PpcA from Geobacter sulfurreducens:  Evidence for a Role Played in e-/H+ Energy Transduction†,‡

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Requimte, CQFB, Departamento de Química, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Quinta da Torre, 2829-516 Caparica, Portugal, Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Rua da Quinta Grande 6, 2780-156 Oeiras, Portugal, and Biosciences Division, Argonne National Laboratory, Argonne, Illinois 60439
Cite this: Biochemistry 2006, 45, 46, 13910–13917
Publication Date (Web):October 28, 2006
https://doi.org/10.1021/bi061394v
Copyright © 2006 American Chemical Society
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Abstract

Abstract Image

The facultative aerobic bacterium Geobacter sulfurreducens produces a small periplasmic c-type triheme cytochrome with 71 residues (PpcA) under anaerobic growth conditions, which is involved in the iron respiration. The thermodynamic properties of the PpcA redox centers and of a protonatable center were determined using NMR and visible spectroscopy techniques. The redox centers have negative and different reduction potentials (−162, −143, and −133 mV for heme I, III, and IV, respectively, for the fully reduced and protonated protein), which are modulated by redox interactions among the hemes (covering a range from 10 to 36 mV) and by redox−Bohr interactions (up to −62 mV) between the hemes and a protonatable center located in the proximity of heme IV. All the interactions between the four centers are dominated by electrostatic effects. The microscopic reduction potential of heme III is the one most affected by the oxidation of the other hemes, whereas heme IV is the most affected by the protonation state of the molecule. The thermodynamic properties of PpcA showed that pH strongly modulates the redox behavior of the individual heme groups. A preferred electron transfer pathway at physiologic pH is defined, showing that PpcA has the necessary thermodynamic properties to perform e-/H+ energy transduction, contributing to a H+ electrochemical potential gradient across the periplasmic membrane that drives ATP synthesis. PpcA is 46% identical in sequence to and shares a high degree of structural similarity with a periplasmic triheme cytochrome c7 isolated from Desulfuromonas acetoxidans, a bacterium closely related to the Geobacteracea family. However, the results obtained for PpcA are quite different from those published for D. acetoxidans c7, and the physiological consequences of these differences are discussed.

†

 This work is supported by Fundação para a Ciência e Tecnologia (FCT) by Project Grants POCI/QUI/60060/2004 and POCI/BIO/58652/2004 and by the U.S. Department of Energy's Office of Science, Biological and Environmental Research NABIR and GTL programs under Contract W-31-109-Eng-38. M.P. acknowledges Fundação para a Ciência e Tecnologia (FCT), Portugal, for Postdoctoral Grant BPD/20571/2004.

‡

 We dedicate this article to the memory of Professor António V. Xavier (1943−2006), who among many other important scientific achievements had an outstanding contribution to the understanding of the role played by multiheme cytochromes in energy transduction mechanisms.

§

 Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa.

‖

 Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa.

⊥

 Argonne National Laboratory.

*

 To whom correspondence should be addressed:  Departamento de Química, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Quinta da Torre, 2829-516 Caparica, Portugal. Telephone:  (351) 212 948 300. Fax:  (351) 212 948 385. E-mail:  [email protected]

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  27. Leonor Morgado, Marta Bruix, Miguel Pessanha, Yuri Y. Londer, Carlos A. Salgueiro. Thermodynamic Characterization of a Triheme Cytochrome Family from Geobacter sulfurreducens Reveals Mechanistic and Functional Diversity. Biophysical Journal 2010, 99 (1) , 293-301. https://doi.org/10.1016/j.bpj.2010.04.017
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  29. Leonor Morgado, Ana P. Fernandes, Yuri Y. Londer, Marta Bruix, Carlos A. Salgueiro. One simple step in the identification of the cofactors signals, one giant leap for the solution structure determination of multiheme proteins. Biochemical and Biophysical Research Communications 2010, 393 (3) , 466-470. https://doi.org/10.1016/j.bbrc.2010.02.024
  30. P.R. Pokkuluri, Y.Y. Londer, X. Yang, N.E.C. Duke, J. Erickson, V. Orshonsky, G. Johnson, M. Schiffer. Structural characterization of a family of cytochromes c7 involved in Fe(III) respiration by Geobacter sulfurreducens. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2010, 1797 (2) , 222-232. https://doi.org/10.1016/j.bbabio.2009.10.007
  31. Leonor Morgado, Ana P. Fernandes, Yuri Y. Londer, P. Raj Pokkuluri, Marianne Schiffer, Carlos A. Salgueiro. Thermodynamic characterization of the redox centres in a representative domain of a novel c-type multihaem cytochrome. Biochemical Journal 2009, 420 (3) , 485-492. https://doi.org/10.1042/BJ20082428
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  34. Leonor Morgado, Marta Bruix, Valerie Orshonsky, Yuri Y. Londer, Norma E.C. Duke, Xiaojing Yang, P. Raj Pokkuluri, Marianne Schiffer, Carlos A. Salgueiro. Structural insights into the modulation of the redox properties of two Geobacter sulfurreducens homologous triheme cytochromes. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2008, 1777 (9) , 1157-1165. https://doi.org/10.1016/j.bbabio.2008.04.043
  35. Ana P. Fernandes, Isabel Couto, Leonor Morgado, Yuri Y. Londer, Carlos A. Salgueiro. Isotopic labeling of c-type multiheme cytochromes overexpressed in E. coli. Protein Expression and Purification 2008, 59 (1) , 182-188. https://doi.org/10.1016/j.pep.2008.02.001
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  37. Leonor Morgado, Marta Bruix, Yuri Y. Londer, P. Raj Pokkuluri, Marianne Schiffer, Carlos A. Salgueiro. Redox-linked conformational changes of a multiheme cytochrome from Geobacter sulfurreducens. Biochemical and Biophysical Research Communications 2007, 360 (1) , 194-198. https://doi.org/10.1016/j.bbrc.2007.06.026

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