The Solution Structure of a Tetraheme Cytochrome from Shewanella frigidimarina Reveals a Novel Family Structural Motif†‡
- Vitor B. Paixão ,
- Carlos A. Salgueiro ,
- Lorraine Brennan ,
- Graeme A. Reid ,
- Stephen K. Chapman , and
- David L. Turner
View Author Information
Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Rua da Quinta Grande 6, 2780-156 Oeiras, Portugal, Requimte, CQFB, Requimte, CQFB, Departamento de Química da Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa, Quinta da Torre, 2829-516 Caparica, Portugal, UCD Conway Institute, UCD School of Agriculture, Food Science and Veterinary Medicine, UCD, Belfield, Dublin 4, Ireland, Institute of Structural and Molecular Biology, University of Edinburgh, Mayfield Road, Edinburgh EH9 3JR, U.K., EaStCHEM, School of Chemistry, University of Edinburgh, West Mains Road, Edinburgh EH9 3JJ, U.K., and School of Chemistry, University of Southampton, Southampton SO17 1BJ, U.K.
†This work was supported by Grants POCI/QUI/58985/2004, POCI/QUI/60060/2004, and PPCDT/QUI/60060/2004 from Fundação para a Ciência e Tecnologia (Portugal). V.B.P. was supported by Grant BD/5830/2001 from Fundação para a Ciência e Tecnologia (Portugal).
‡The structure data and the chemical shifts are deposited in the Protein Data Bank as entry 2k3v and in the BioMagResBank as entry 15765, respectively.
* To whom correspondence should be addressed: Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Rua da Quinta Grande 6, 2780-156 Oeiras, Portugal. Telephone: 351 21 4469821. Fax: 351 21 4428766. E-mail: [email protected]
§Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa.
∥Departamento de Química da Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa.
⊥UCD.
#Institute of Structural and Molecular Biology, University of Edinburgh.
+School of Chemistry, University of Edinburgh.
@University of Southampton.
Abstract
The bacteria belonging to the genus Shewanella are facultative anaerobes that utilize a variety of terminal electron acceptors which includes soluble and insoluble metal oxides. The tetraheme c-type cytochrome isolated during anaerobic growth of Shewanella frigidimarina NCIMB400 (Sfc) contains 86 residues and is involved in the Fe(III) reduction pathways. Although the functional properties of Sfc redox centers are quite well described, no structures are available for this protein. In this work, we report the solution structure of the reduced form of Sfc. The overall fold is completely different from those of the tetraheme cytochromes c3 and instead has similarities with the tetraheme cytochrome recently isolated from Shewanella oneidensis (Soc). Comparison of the tetraheme cytochromes from Shewanella shows a considerable diversity in their primary structure and heme reduction potentials, yet they have highly conserved heme geometry, as is the case for the family of tetraheme cytochromes isolated from Desulfovibrio spp.
Cited By
This article is cited by 17 publications.
- Zdenek Futera, Ichiro Ide, Ben Kayser, Kavita Garg, Xiuyun Jiang, Jessica H. van Wonderen, Julea N. Butt, Hisao Ishii, Israel Pecht, Mordechai Sheves, David Cahen, Jochen Blumberger. Coherent Electron Transport across a 3 nm Bioelectronic Junction Made of Multi-Heme Proteins. The Journal of Physical Chemistry Letters 2020, 11 (22) , 9766-9774. https://doi.org/10.1021/acs.jpclett.0c02686
- Yufeng Qian, Catarina M. Paquete, Ricardo O. Louro, Daniel E. Ross, Edward LaBelle, Daniel R. Bond, and Ming Tien . Mapping the Iron Binding Site(s) on the Small Tetraheme Cytochrome of Shewanella oneidensis MR-1. Biochemistry 2011, 50 (28) , 6217-6224. https://doi.org/10.1021/bi2005015
- Vitor B. Paixão, Hans Vis, and David L. Turner. Redox Linked Conformational Changes in Cytochrome c3 from Desulfovibrio desulfuricans ATCC 27774. Biochemistry 2010, 49 (44) , 9620-9629. https://doi.org/10.1021/bi101237w
- Bruno M. Fonseca, Ricardo M. Soares, Catarina M. Paquete, Ricardo O. Louro. Bacterial Power: An Alternative Energy Source. 2021,,, 215-246. https://doi.org/10.1007/978-3-030-58315-6_8
- Olivier N Lemaire, Vincent Méjean, Chantal Iobbi-Nivol. The Shewanella genus: ubiquitous organisms sustaining and preserving aquatic ecosystems. FEMS Microbiology Reviews 2020, 44 (2) , 155-170. https://doi.org/10.1093/femsre/fuz031
- Xiuyun Jiang, Bastian Burger, Fruzsina Gajdos, C. Bortolotti, Zdenek Futera, Marian Breuer, Jochen Blumberger. Kinetics of trifurcated electron flow in the decaheme bacterial proteins MtrC and MtrF. Proceedings of the National Academy of Sciences 2019, 116 (9) , 3425-3430. https://doi.org/10.1073/pnas.1818003116
- Bruno M. Fonseca, Luís Silva, Inês B. Trindade, Elin Moe, Pedro M. Matias, Ricardo O. Louro, Catarina M. Paquete. Optimizing Electroactive Organisms: The Effect of Orthologous Proteins. Frontiers in Energy Research 2019, 7 https://doi.org/10.3389/fenrg.2019.00002
- Ricardo O. Louro, Nazua L. Costa, Ana P. Fernandes, Ana V. Silva, Inês B. Trindade, Bruno M. Fonseca, Catarina M. Paquete. Exploring the Molecular Mechanisms of Extracellular Electron Transfer for Harnessing Reducing Power in METs. 2019,,, 261-293. https://doi.org/10.1016/B978-0-444-64052-9.00010-8
- Catarina M. Paquete, Giovanni Rusconi, Ana V. Silva, Ricardo Soares, Ricardo O. Louro. A brief survey of the “cytochromome”. 2019,,, 69-135. https://doi.org/10.1016/bs.ampbs.2019.07.005
- Jochen Blumberger. Electron transfer and transport through multi-heme proteins: recent progress and future directions. Current Opinion in Chemical Biology 2018, 47 , 24-31. https://doi.org/10.1016/j.cbpa.2018.06.021
- Joana M. Dantas, Marta A. Silva, David Pantoja-Uceda, David L. Turner, Marta Bruix, Carlos A. Salgueiro. Solution structure and dynamics of the outer membrane cytochrome OmcF from Geobacter sulfurreducens. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2017, 1858 (9) , 733-741. https://doi.org/10.1016/j.bbabio.2017.03.007
- Leonor Morgado, Vítor B. Paixão, Marianne Schiffer, P. Raj Pokkuluri, Marta Bruix, Carlos A. Salgueiro. Revealing the structural origin of the redox-Bohr effect: the first solution structure of a cytochrome from Geobacter sulfurreducens. Biochemical Journal 2012, 441 (1) , 179-187. https://doi.org/10.1042/BJ20111103
- Jeffery A Mayfield, Carolyn A Dehner, Jennifer L DuBois. Recent advances in bacterial heme protein biochemistry. Current Opinion in Chemical Biology 2011, 15 (2) , 260-266. https://doi.org/10.1016/j.cbpa.2011.02.002
- Catarina M. Paquete, Ivo H. Saraiva, Eduardo Calçada, Ricardo O. Louro. Molecular Basis for Directional Electron Transfer. Journal of Biological Chemistry 2010, 285 (14) , 10370-10375. https://doi.org/10.1074/jbc.M109.078337
- 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
- Catarina M. Paquete, Ricardo O. Louro. Molecular details of multielectron transfer: the case of multiheme cytochromes from metal respiring organisms. Dalton Trans. 2010, 39 (18) , 4259-4266. https://doi.org/10.1039/B917952F
- Miguel Pessanha, Emma L. Rothery, Caroline S. Miles, Graeme A. Reid, Stephen K. Chapman, Ricardo O. Louro, David L. Turner, Carlos A. Salgueiro, António V. Xavier. Tuning of functional heme reduction potentials in Shewanella fumarate reductases. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2009, 1787 (2) , 113-120. https://doi.org/10.1016/j.bbabio.2008.11.007