NADPH-dependent sulfite reductase flavoprotein adopts an extended conformation unique to this diflavin reductase

Tavolieri, Angela M.; Murray, Daniel T.; Askenasy, Isabel; Pennington, Joseph M.; McGarry, Lauren; Stanley, Christopher B.; Stroupe, Margaret Elizabeth

doi:10.1016/j.jsb.2019.01.001

Title: NADPH-dependent sulfite reductase flavoprotein adopts an extended conformation unique to this diflavin reductase

Journal Article · Tue Jan 15 00:00:00 EST 2019 · Journal of Structural Biology

DOI:https://doi.org/10.1016/j.jsb.2019.01.001· OSTI ID:1545231

Tavolieri, Angela M. ^[1]; Murray, Daniel T. ^[1]; Askenasy, Isabel ^[2]; Pennington, Joseph M. ^[1]; McGarry, Lauren ^[1];

^[3]; Stroupe, Margaret Elizabeth ^[1]

Dept. of Biological Science and Institute of Molecular Biophysics, Tallahassee, FL (United States)
Dept. of Biological Science and Institute of Molecular Biophysics, Tallahassee, FL (United States); Univ. of Wisconsin, Madison, WI (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

This is the first X-ray crystal structure of the monomeric form of sulfite reductase (SiR) flavoprotein (SiRFP-60) that shows the relationship between its major domains in an extended position not seen before in any homologous diflavin reductases. Small angle neutron scattering confirms this novel domain orientation also occurs in solution. Activity measurements of SiR and SiRFP variants allow us to propose a novel mechanism for electron transfer from the SiRFP reductase subunit to its oxidase metalloenzyme partner that, together, make up the SiR holoenzyme. Specifically, we propose that SiR performs its 6-electron reduction via intramolecular or intermolecular electron transfer. Furthermore, our model explains both the significance of the stoichiometric mismatch between reductase and oxidase subunits in the holoenzyme and how SiR can handle such a large volume electron reduction reaction that is at the heart of the sulfur bio-geo cycle.

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Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1545231

Journal Information:: Journal of Structural Biology, Vol. 205, Issue 2; ISSN 1047-8477

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 6 works

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References (57)

PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Structure of the open conformation of a functional chimeric NADPH cytochrome P450 reductase Aigrain, Louise; Pompon, Denis; Moréra, Solange EMBO reports, Vol. 10, Issue 7 https://doi.org/10.1038/embor.2009.82	journal	May 2009
Mantid—Data analysis and visualization package for neutron scattering and $μ$ SR experiments Arnold, O.; Bilheux, J. C.; Borreguero, J. M. Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 764 https://doi.org/10.1016/j.nima.2014.07.029	journal	November 2014
Structure–Function Relationships in the Oligomeric NADPH-Dependent Assimilatory Sulfite Reductase Askenasy, Isabel; Murray, Daniel T.; Andrews, Rachel M. Biochemistry, Vol. 57, Issue 26 https://doi.org/10.1021/acs.biochem.8b00446	journal	May 2018
The N-terminal Domain of Escherichia coli Assimilatory NADPH-Sulfite Reductase Hemoprotein Is an Oligomerization Domain That Mediates Holoenzyme Assembly Askenasy, Isabel; Pennington, Joseph M.; Tao, Yeqing Journal of Biological Chemistry, Vol. 290, Issue 31 https://doi.org/10.1074/jbc.M115.662379	journal	July 2015
Sulfur Cycling and the Intestinal Microbiome Barton, Larry L.; Ritz, Nathaniel L.; Fauque, Guy D. Digestive Diseases and Sciences, Vol. 62, Issue 9 https://doi.org/10.1007/s10620-017-4689-5	journal	August 2017
The relationship between structure and function for the sulfite reductases Crane, Brian R.; Getzoff, Elizabeth D. Current Opinion in Structural Biology, Vol. 6, Issue 6 https://doi.org/10.1016/S0959-440X(96)80003-0	journal	December 1996
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
NADPH-sulfite reductase flavoprotein from Escherichia coli : Contribution to the flavin content and subunit interaction Eschenbrenner, Michel; Covès, Jacques; Fontecave, Marc FEBS Letters, Vol. 374, Issue 1 https://doi.org/10.1016/0014-5793(95)01081-O	journal	October 1995
The Flavin Reductase Activity of the Flavoprotein Component of Sulfite Reductase from Escherichia coli Eschenbrenner, Michel; Covès, Jacques; Fontecave, Marc Journal of Biological Chemistry, Vol. 270, Issue 35 https://doi.org/10.1074/jbc.270.35.20550	journal	September 1995
Orchestrated Domain Movement in Catalysis by Cytochrome P450 Reductase Freeman, Samuel L.; Martel, Anne; Raven, Emma L. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-09840-8	journal	August 2017
Solution structure of the cytochrome P450 reductase–cytochrome c complex determined by neutron scattering Freeman, Samuel L.; Martel, Anne; Devos, Juliette M. Journal of Biological Chemistry, Vol. 293, Issue 14 https://doi.org/10.1074/jbc.RA118.001941	journal	April 2018
Four crystal structures of the 60 kDa flavoprotein monomer of the sulfite reductase indicate a disordered flavodoxin-like module 1 1Edited by R. Huber Gruez, Arnaud; Pignol, David; Zeghouf, Mahel Journal of Molecular Biology, Vol. 299, Issue 1 https://doi.org/10.1006/jmbi.2000.3748	journal	May 2000
Structure and Function of an NADPH-Cytochrome P450 Oxidoreductase in an Open Conformation Capable of Reducing Cytochrome P450 Hamdane, Djemel; Xia, Chuanwu; Im, Sang-Choul Journal of Biological Chemistry, Vol. 284, Issue 17 https://doi.org/10.1074/jbc.M807868200	journal	January 2009
Control of Electron Transfer and Catalysis in Neuronal Nitric-oxide Synthase (nNOS) by a Hinge Connecting Its FMN and FAD-NADPH Domains Haque, Mohammad Mahfuzul; Fadlalla, Mohammed A.; Aulak, Kulwant S. Journal of Biological Chemistry, Vol. 287, Issue 36 https://doi.org/10.1074/jbc.M112.339697	journal	August 2012
Distinct conformational behaviors of four mammalian dual-flavin reductases (cytochrome P450 reductase, methionine synthase reductase, neuronal nitric oxide synthase, endothelial nitric oxide synthase) determine their unique catalytic profiles Haque, Mohammad M.; Bayachou, Mekki; Tejero, Jesus FEBS Journal, Vol. 281, Issue 23 https://doi.org/10.1111/febs.13073	journal	October 2014
Structural insights into the enzyme catalysis from comparison of three forms of dissimilatory sulphite reductase from Desulfovibrio gigas: Structures of D. gigas dissimilatory sulphite reductases Hsieh, Yin-Cheng; Liu, Ming-Yih; Wang, Vincent C. -C. Molecular Microbiology, Vol. 78, Issue 5 https://doi.org/10.1111/j.1365-2958.2010.07390.x	journal	September 2010
Hydrogen sulfide and its roles in Saccharomyces cerevisiae in a winemaking context Huang, Chien-Wei; Walker, Michelle E.; Fedrizzi, Bruno FEMS Yeast Research, Vol. 17, Issue 6 https://doi.org/10.1093/femsyr/fox058	journal	July 2017
Redox-Linked Domain Movements in the Catalytic Cycle of Cytochrome P450 Reductase Huang, Wei-Cheng; Ellis, Jacqueline; Moody, Peter C. E. Structure, Vol. 21, Issue 9 https://doi.org/10.1016/j.str.2013.06.022	journal	September 2013
NADPH-Cytochrome P450 Oxidoreductase Hubbard, Paul A.; Shen, Anna L.; Paschke, Rosemary Journal of Biological Chemistry, Vol. 276, Issue 31 https://doi.org/10.1074/jbc.M101731200	journal	August 2001
The interaction of microsomal cytochrome P450 2B4 with its redox partners, cytochrome P450 reductase and cytochrome b5 Im, Sang-Choul; Waskell, Lucy Archives of Biochemistry and Biophysics, Vol. 507, Issue 1 https://doi.org/10.1016/j.abb.2010.10.023	journal	March 2011
Biochemical Distinctions between the Nuclear and Microsomal Membranes from Rat Hepatocytes Kasper, Charles B. Journal of Biological Chemistry, Vol. 246, Issue 3 https://doi.org/10.1016/S0021-9258(18)62453-6	journal	February 1971
PRIMUS: a Windows PC-based system for small-angle scattering data analysis Konarev, Petr V.; Volkov, Vladimir V.; Sokolova, Anna V. Journal of Applied Crystallography, Vol. 36, Issue 5, p. 1277-1282 https://doi.org/10.1107/S0021889803012779	journal	September 2003
A designed heme-[4Fe-4S] metalloenzyme catalyzes sulfite reduction like the native enzyme Mirts, Evan N.; Petrik, Igor D.; Hosseinzadeh, Parisa Science, Vol. 361, Issue 6407 https://doi.org/10.1126/science.aat8474	journal	September 2018
Siroheme and Sirohydrochlorin Murphy, Matthew J.; Siegel, Lewis M. Journal of Biological Chemistry, Vol. 248, Issue 19 https://doi.org/10.1016/S0021-9258(19)43436-4	journal	October 1973
The Crystal Structure of Desulfovibrio vulgaris Dissimilatory Sulfite Reductase Bound to DsrC Provides Novel Insights into the Mechanism of Sulfate Respiration Oliveira, Tânia F.; Vonrhein, Clemens; Matias, Pedro M. Journal of Biological Chemistry, Vol. 283, Issue 49 https://doi.org/10.1074/jbc.M805643200	journal	September 2008
Human Methionine Synthase Reductase, a Soluble P-450 Reductase-like Dual Flavoprotein, Is Sufficient for NADPH-dependent Methionine Synthase Activation Olteanu, Horatiu; Banerjee, Ruma Journal of Biological Chemistry, Vol. 276, Issue 38 https://doi.org/10.1074/jbc.M103707200	journal	July 2001
Kinetic and Thermodynamic Characterization of the Common Polymorphic Variants of Human Methionine Synthase Reductase Olteanu, Horatiu; Wolthers, Kirsten R.; Munro, Andrew W. Biochemistry, Vol. 43, Issue 7 https://doi.org/10.1021/bi035910i	journal	January 2004
Calmodulin Activates Intersubunit Electron Transfer in the Neuronal Nitric-oxide Synthase Dimer Panda, Koustubh; Ghosh, Sanjay; Stuehr, Dennis J. Journal of Biological Chemistry, Vol. 276, Issue 26 https://doi.org/10.1074/jbc.M100687200	journal	June 2001
Distinct Dimer Interaction and Regulation in Nitric-oxide Synthase Types I, II, and III Panda, Koustubh; Rosenfeld, Robin J.; Ghosh, Sanjay Journal of Biological Chemistry, Vol. 277, Issue 34 https://doi.org/10.1074/jbc.M203749200	journal	August 2002
Reaction Cycle of the Dissimilatory Sulfite Reductase from Archaeoglobus fulgidus , Parey, Kristian; Warkentin, Eberhard; Kroneck, Peter M. H. Biochemistry, Vol. 49, Issue 41 https://doi.org/10.1021/bi100781f	journal	October 2010
New developments in the ATSAS program package for small-angle scattering data analysis Petoukhov, Maxim V.; Franke, Daniel; Shkumatov, Alexander V. Journal of Applied Crystallography, Vol. 45, Issue 2 https://doi.org/10.1107/S0021889812007662	journal	March 2012
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Structure of the Dissimilatory Sulfite Reductase from the Hyperthermophilic Archaeon Archaeoglobus fulgidus Schiffer, Alexander; Parey, Kristian; Warkentin, Eberhard Journal of Molecular Biology, Vol. 379, Issue 5 https://doi.org/10.1016/j.jmb.2008.04.027	journal	June 2008
Solution Structure of the Sulfite Reductase Flavodoxin-like Domain from Escherichia coli ^† ^, ^‡ Sibille, Nathalie; Blackledge, Martin; Brutscher, Bernhard Biochemistry, Vol. 44, Issue 25 https://doi.org/10.1021/bi050437p	journal	June 2005
Heme Iron Reduction and Catalysis by a Nitric Oxide Synthase Heterodimer Containing One Reductase and Two Oxygenase Domains Siddhanta, Uma; Wu, Chaoqun; Abu-Soud, Husam M. Journal of Biological Chemistry, Vol. 271, Issue 13 https://doi.org/10.1074/jbc.271.13.7309	journal	March 1996
Domain Swapping in Inducible Nitric-oxide Synthase Siddhanta, Uma; Presta, Anthony; Fan, Baochen Journal of Biological Chemistry, Vol. 273, Issue 30 https://doi.org/10.1074/jbc.273.30.18950	journal	July 1998
Reduced Nicotinamide Adenine Dinucleotide Phosphate-Sulfite Reductase of Enterobacteria Siegel, Lewis M.; Davis, Patricia S. Journal of Biological Chemistry, Vol. 249, Issue 5 https://doi.org/10.1016/S0021-9258(19)42922-0	journal	March 1974
Reduced Nicotinamide Adenine Dinucleotide Phosphate-Sulfite Reductase of Enterobacteria Siegel, Lewis M.; Murphy, Matthew J.; Kamin, Henry Journal of Biological Chemistry, Vol. 248, Issue 1 https://doi.org/10.1016/S0021-9258(19)44469-4	journal	January 1973
Hydrogen Sulfide in Physiology and Diseases of the Digestive Tract Singh, Sudha; Lin, Henry Microorganisms, Vol. 3, Issue 4 https://doi.org/10.3390/microorganisms3040866	journal	November 2015
Mutational Analysis of Sulfite Reductase Hemoprotein Reveals the Mechanism for Coordinated Electron and Proton Transfer Smith, Kyle W.; Stroupe, M. Elizabeth Biochemistry, Vol. 51, Issue 49 https://doi.org/10.1021/bi300947a	journal	November 2012
Structural basis for the electron transfer from an open form of NADPH-cytochrome P450 oxidoreductase to heme oxygenase Sugishima, M.; Sato, H.; Higashimoto, Y. Proceedings of the National Academy of Sciences, Vol. 111, Issue 7 https://doi.org/10.1073/pnas.1322034111	journal	February 2014
Determination of the regularization parameter in indirect-transform methods using perceptual criteria Svergun, D. I. Journal of Applied Crystallography, Vol. 25, Issue 4, p. 495-503 https://doi.org/10.1107/S0021889892001663	journal	August 1992
Protein hydration in solution: Experimental observation by x-ray and neutron scattering Svergun, D. I.; Richard, S.; Koch, M. H. J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 5 https://doi.org/10.1073/pnas.95.5.2267	journal	March 1998
Reductive dehalogenation and mineralization of 3-chlorobenzoate in the presence of sulfate by microorganisms from a methanogenic aquifer Townsend, G. T.; Ramanand, K.; Suflita, J. M. Applied and Environmental Microbiology, Vol. 63, Issue 7 https://doi.org/10.1128/AEM.63.7.2785-2791.1997	journal	July 1997
Three-dimensional structure of NADPH-cytochrome P450 reductase: Prototype for FMN- and FAD-containing enzymes Wang, M.; Roberts, D. L.; Paschke, R. Proceedings of the National Academy of Sciences, Vol. 94, Issue 16 https://doi.org/10.1073/pnas.94.16.8411	journal	August 1997
The life sulfuric: microbial ecology of sulfur cycling in marine sediments: Microbial sulfur cycling in marine sediments Wasmund, Kenneth; Mußmann, Marc; Loy, Alexander Environmental Microbiology Reports, Vol. 9, Issue 4 https://doi.org/10.1111/1758-2229.12538	journal	May 2017
Absolute calibration of small-angle neutron scattering data Wignall, G. D.; Bates, F. S. Journal of Applied Crystallography, Vol. 20, Issue 1 https://doi.org/10.1107/S0021889887087181	journal	February 1987
Protein Interactions in the Human Methionine Synthase−Methionine Synthase Reductase Complex and Implications for the Mechanism of Enzyme Reactivation ^† Wolthers, Kirsten R.; Scrutton, Nigel S. Biochemistry, Vol. 46, Issue 23 https://doi.org/10.1021/bi700339v	journal	June 2007
Molecular Dissection of Human Methionine Synthase Reductase: Determination of the Flavin Redox Potentials in Full-Length Enzyme and Isolated Flavin-Binding Domains ^† Wolthers, Kirsten R.; Basran, Jaswir; Munro, Andrew W. Biochemistry, Vol. 42, Issue 13 https://doi.org/10.1021/bi027290b	journal	April 2003
Crystal structure and solution characterization of the activation domain of human methionine synthase: Human MS activation domain structure Wolthers, Kirsten R.; Toogood, Helen S.; Jowitt, Thomas A. FEBS Journal, Vol. 274, Issue 3 https://doi.org/10.1111/j.1742-4658.2006.05618.x	journal	December 2006
Conformational Changes of NADPH-Cytochrome P450 Oxidoreductase Are Essential for Catalysis and Cofactor Binding Xia, Chuanwu; Hamdane, Djemel; Shen, Anna L. Journal of Biological Chemistry, Vol. 286, Issue 18 https://doi.org/10.1074/jbc.M111.230532	journal	February 2011
Architecture of the Nitric-oxide Synthase Holoenzyme Reveals Large Conformational Changes and a Calmodulin-driven Release of the FMN Domain Yokom, Adam L.; Morishima, Yoshihiro; Lau, Miranda Journal of Biological Chemistry, Vol. 289, Issue 24 https://doi.org/10.1074/jbc.M114.564005	journal	June 2014
A Simplifed Functional Version of the Escherichia coli Sulfite Reductase Zeghouf, Mahel; Fontecave, Marc; Covès, Jacques Journal of Biological Chemistry, Vol. 275, Issue 48 https://doi.org/10.1074/jbc.M005619200	journal	September 2000
The Flavoprotein Component of the Escherichia coli Sulfite Reductase: Expression, Purification, and Spectral and Catalytic Properties of a Monomeric Form Containing both the Flavin Adenine Dinucleotide and the Flavin Mononucleotide Cofactors Zeghouf, Mahel; Fontecave, Marc; Macherel, David Biochemistry, Vol. 37, Issue 17 https://doi.org/10.1021/bi9728699	journal	April 1998
The full-length cytochrome P450 enzyme CYP102A1 dimerizes at its reductase domains and has flexible heme domains for efficient catalysis Zhang, Haoming; Yokom, Adam L.; Cheng, Shen Journal of Biological Chemistry, Vol. 293, Issue 20 https://doi.org/10.1074/jbc.RA117.000600	journal	May 2018
The extended Q -range small-angle neutron scattering diffractometer at the SNS Zhao, J. K.; Gao, C. Y.; Liu, D. Journal of Applied Crystallography, Vol. 43, Issue 5 https://doi.org/10.1107/S002188981002217X	journal	July 2010

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Flavoprotein
Diflavin reductase
Cytochrome p450 reductase
Electron transfer
X-ray crystallography
SANS

Data for: NADPH-dependent sulfite reductase flavoprotein adopts an extended conformation unique to this diflavin reductase. Stroupe, M. E. https://doi.org/10.17632/cfyh6vs5jh.1 The current record is supplemented by this dataset	dataset	January 2020
Data for: NADPH-dependent sulfite reductase flavoprotein adopts an extended conformation unique to this diflavin reductase. Stroupe, M. E. https://doi.org/10.17632/cfyh6vs5jh The current record is supplemented by this dataset	dataset	January 2020

Title: NADPH-dependent sulfite reductase flavoprotein adopts an extended conformation unique to this diflavin reductase

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