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Redox Characterization of Geobacter sulfurreducens Cytochrome c7:  Physiological Relevance of the Conserved Residue F15 Probed by Site-Specific Mutagenesis†

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Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Rua da Quinta Grande 6, 2780-156 Oeiras, Portugal, Biosciences Division, Argonne National Laboratory, Argonne, Illinois 60439, and Departamento de Química da Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa, Quinta da Torre, 2829-516, Portugal
Cite this: Biochemistry 2004, 43, 30, 9909–9917
Publication Date (Web):July 9, 2004
https://doi.org/10.1021/bi0492859
Copyright © 2004 American Chemical Society
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Abstract

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The complete genome sequence of the δ-proteobacterium Geobacter sulfurreducens reveals a large abundance of multiheme cytochromes. Cytochrome c7, isolated from this metal ion-reducing bacterium, is a triheme periplasmic electron-transfer protein with Mr 9.6 kDa. This protein is involved in metal ion-reducing pathways and shares 56% sequence identity with a triheme cytochrome isolated from the closely related δ-proteobacterium Desulfuromonas acetoxidans (Dac7). In this work, two-dimensional NMR was used to monitor the heme core and the general folding in solution of the G. sulfurreducens triheme cytochrome c7 (PpcA). NMR signals obtained for the three hemes of PpcA at different stages of oxidation were cross-assigned to the crystal structure [Pokkuluri, P. R., Londer, Y. Y., Duke, N. E. C., Long, W. C., and Schiffer, M. (2004) Biochemistry 43, 849−859] using the complete network of chemical exchange connectivities, and the order in which each heme becomes oxidized was determined at pH 6.0 and 8.2. Redox titrations followed by visible spectroscopy were also performed in order to monitor the macroscopic redox behavior of PpcA. The results obtained showed that PpcA and Dac7 have different redox properties:  (i) the order in which each heme becomes oxidized is different; (ii) the reduction potentials of the heme groups and the global redox behavior of PpcA are pH dependent (redox−Bohr effect) in the physiological pH range, which is not observed with Dac7. The differences observed in the redox behavior of PpcA and Dac7 may account for the different functions of these proteins and constitute an excellent example of how homologous proteins can perform different physiological functions. The redox titrations followed by visible spectroscopy of PpcA and two mutants of the conserved residue F15 (PpcAF15Y and PpcAF15W) lead to the conclusion that F15 modulates the redox behavior of PpcA, thus having an important physiological role.

†

 This work is supported by FCT-Portugal Grant POCTI/42902/QUI/2001 (approved by FCT and POCTI and cofinanced by FEDER) and by the U.S. Department of Energy's Office of Science, Biological and Environmental Research, Structural Biology and NABIR programs, under Contract W-31-109-Eng-38. Miguel Pessanha acknowledges Fundação para a Ciência e Tecnologia (FCT), Portugal, for a doctoral fellowship (SFRH/5229/2001).

‡

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

§

 Argonne National Laboratory.

*

 To whom correspondence should be addressed. Telephone:  (351) 214 469 848. Fax:  (351) 214 428 766. E-mail:  [email protected]

‖

 Departamento de Química da Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa.

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Total correlation spectroscopy NMR spectra for PpcA and PpcAF15Y in the reduced form, exchange spectroscopy NMR spectra for PpcA at pH 8.2 illustrating the cross-peaks between heme signals in several different oxidation stages, and a plot with the α-band region of the visible spectra used for the PpcA potentiometric titration carried out at pH 6.9. This material is available free of charge via the Internet at http://pubs.acs.org.

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This article is cited by 32 publications.

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  2. Oleksandr Kokhan, Nina S. Ponomarenko, P. Raj Pokkuluri, Marianne Schiffer, Karen L. Mulfort, and David. M. Tiede . Bidirectional Photoinduced Electron Transfer in Ruthenium(II)-Tris-bipyridyl-Modified PpcA, a Multi-heme c-Type Cytochrome from Geobacter sulfurreducens. The Journal of Physical Chemistry B 2015, 119 (24) , 7612-7624. https://doi.org/10.1021/jp511558f
  3. Jincheng Wei, Peng Liang, Xiaoxin Cao and Xia Huang. A New Insight into Potential Regulation on Growth and Power Generation of Geobacter sulfurreducens in Microbial Fuel Cells Based on Energy Viewpoint. Environmental Science & Technology 2010, 44 (8) , 3187-3191. https://doi.org/10.1021/es903758m
  4. Vitor B. Paixão, Carlos A. Salgueiro, Lorraine Brennan, Graeme A. Reid, Stephen K. Chapman and David L. Turner . The Solution Structure of a Tetraheme Cytochrome from Shewanella frigidimarina Reveals a Novel Family Structural Motif. Biochemistry 2008, 47 (46) , 11973-11980. https://doi.org/10.1021/bi801326j
  5. Gérard Simonneaux and, Arnaud Bondon. Mechanism of Electron Transfer in Heme Proteins and Models:  The NMR Approach. Chemical Reviews 2005, 105 (6) , 2627-2646. https://doi.org/10.1021/cr030731s
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  8. Marisa R. Ferreira, Carlos A. Salgueiro. Biomolecular Interaction Studies Between Cytochrome PpcA From Geobacter sulfurreducens and the Electron Acceptor Ferric Nitrilotriacetate (Fe-NTA). Frontiers in Microbiology 2018, 9 https://doi.org/10.3389/fmicb.2018.02741
  9. Leonor Morgado, Marta Bruix, P. Raj Pokkuluri, Carlos A. Salgueiro, David L. Turner. Redox- and pH-linked conformational changes in triheme cytochrome PpcA from Geobacter sulfurreducens. Biochemical Journal 2017, 474 (2) , 231-246. https://doi.org/10.1042/BCJ20160932
  10. Marisa R. Ferreira, Joana M. Dantas, Carlos A. Salgueiro. Molecular interactions between Geobacter sulfurreducens triheme cytochromes and the electron acceptor Fe( iii ) citrate studied by NMR. Dalton Transactions 2017, 46 (7) , 2350-2359. https://doi.org/10.1039/C6DT04129A
  11. Carlos A. Salgueiro, Joana M. Dantas. Multiheme Cytochromes. 2016,,, 1-39. https://doi.org/10.1007/978-3-642-44961-1_1
  12. Joana M. Dantas, Leonor Morgado, Muktak Aklujkar, Marta Bruix, Yuri Y. Londer, Marianne Schiffer, P. Raj Pokkuluri, Carlos A. Salgueiro. Rational engineering of Geobacter sulfurreducens electron transfer components: a foundation for building improved Geobacter-based bioelectrochemical technologies. Frontiers in Microbiology 2015, 6 https://doi.org/10.3389/fmicb.2015.00752
  13. Leonor Morgado, Sílvia Lourenço, Yuri Y. Londer, Marianne Schiffer, P. Raj Pokkuluri, Carlos A. Salgueiro, . 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. PLoS ONE 2014, 9 (8) , e105566. https://doi.org/10.1371/journal.pone.0105566
  14. Marta A. Silva, Raquel C. Valente, P. Raj Pokkuluri, David L. Turner, Carlos A. Salgueiro, Teresa Catarino. Thermodynamic and kinetic characterization of two methyl-accepting chemotaxis heme sensors from Geobacter sulfurreducens reveals the structural origin of their functional difference. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2014, 1837 (6) , 920-928. https://doi.org/10.1016/j.bbabio.2014.01.008
  15. Joana M. Dantas, Leonor Morgado, Teresa Catarino, Oleksandr Kokhan, P. Raj Pokkuluri, Carlos A. Salgueiro. 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. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2014, 1837 (6) , 750-760. https://doi.org/10.1016/j.bbabio.2014.02.004
  16. Leonor Morgado, Joana M. Dantas, Telma Simões, Yuri Y. Londer, P. Raj Pokkuluri, Carlos A. Salgueiro. Role of Met58 in the regulation of electron/proton transfer in trihaem cytochrome PpcA from Geobacter sulfurreducens. Bioscience Reports 2013, 33 (1) https://doi.org/10.1042/BSR20120086
  17. Leonor Morgado, Ana P. Fernandes, Joana M. Dantas, Marta A. Silva, Carlos A. Salgueiro. On the road to improve the bioremediation and electricity-harvesting skills of Geobacter sulfurreducens: functional and structural characterization of multihaem cytochromes. Biochemical Society Transactions 2012, 40 (6) , 1295-1301. https://doi.org/10.1042/BST20120099
  18. Daniel R. Bond, Sarah M. Strycharz-Glaven, Leonard M. Tender, César I. Torres. On Electron Transport through Geobacter Biofilms. ChemSusChem 2012, 5 (6) , 1099-1105. https://doi.org/10.1002/cssc.201100748
  19. Joana M. Dantas, Leonor Morgado, Yuri Y. Londer, Ana P. Fernandes, Ricardo O. Louro, P. Raj Pokkuluri, Marianne Schiffer, Carlos A. Salgueiro. Pivotal role of the strictly conserved aromatic residue F15 in the cytochrome c 7 family. JBIC Journal of Biological Inorganic Chemistry 2012, 17 (1) , 11-24. https://doi.org/10.1007/s00775-011-0821-8
  20. Fang Qian, Daniel E. Morse. Miniaturizing microbial fuel cells. Trends in Biotechnology 2011, 29 (2) , 62-69. https://doi.org/10.1016/j.tibtech.2010.10.003
  21. Derek R. Lovley, Toshiyuki Ueki, Tian Zhang, Nikhil S. Malvankar, Pravin M. Shrestha, Kelly A. Flanagan, Muktak Aklujkar, Jessica E. Butler, Ludovic Giloteaux, Amelia-Elena Rotaru, Dawn E. Holmes, Ashley E. Franks, Roberto Orellana, Carla Risso, Kelly P. Nevin. Geobacter. 2011,,, 1-100. https://doi.org/10.1016/B978-0-12-387661-4.00004-5
  22. 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
  23. Krishna P. Katuri, Paul Kavanagh, Saravanan Rengaraj, Dónal Leech. Geobacter sulfurreducens biofilms developed under different growth conditions on glassy carbon electrodes: insights using cyclic voltammetry. Chemical Communications 2010, 46 (26) , 4758. https://doi.org/10.1039/c003342a
  24. 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
  25. O. V. Arkhipova, M. S. Chuvochina, S. M. Trutko. Cytochromes c of the anaerobic methacrylate reducer Geobacter sulfurreducens AM-1. Microbiology 2009, 78 (3) , 296-303. https://doi.org/10.1134/S0026261709030060
  26. 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
  27. 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
  28. Shweta Srikanth, Enrico Marsili, Michael C. Flickinger, Daniel R. Bond. Electrochemical characterization ofGeobacter sulfurreducens cells immobilized on graphite paper electrodes. Biotechnology and Bioengineering 2008, 99 (5) , 1065-1073. https://doi.org/10.1002/bit.21671
  29. Abraham Esteve-Núñez, Julian Sosnik, Pablo Visconti, Derek R. Lovley. Fluorescent properties of c-type cytochromes reveal their potential role as an extracytoplasmic electron sink in Geobacter sulfurreducens. Environmental Microbiology 2008, 10 (2) , 497-505. https://doi.org/10.1111/j.1462-2920.2007.01470.x
  30. Teresa Santos-Silva, João Miguel Dias, Alain Dolla, Marie-Claire Durand, Luísa L. Gonçalves, Jorge Lampreia, Isabel Moura, Maria João Romão. Crystal Structure of the 16 Heme Cytochrome from Desulfovibrio gigas: A Glycosylated Protein in a Sulphate-reducing Bacterium. Journal of Molecular Biology 2007, 370 (4) , 659-673. https://doi.org/10.1016/j.jmb.2007.04.055
  31. Christopher G. Mowat, Stephen K. Chapman. Multi-heme cytochromes—new structures, new chemistry. Dalton Transactions 2005, 302 (21) , 3381. https://doi.org/10.1039/b505184c
  32. Miguel Pessanha, Emma L. Rothery, Ricardo O. Louro, David L. Turner, Caroline S. Miles, Graeme A. Reid, Stephen K. Chapman, António V. Xavier, Carlos A. Salgueiro. Redox behaviour of the haem domain of flavocytochrome c 3 from Shewanella frigidimarina probed by NMR. FEBS Letters 2004, 578 (1-2) , 185-190. https://doi.org/10.1016/j.febslet.2004.10.098

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