MMOD-induced structural changes of hydroxylase in soluble methane monooxygenase

Kim, Hanseong; An, Sojin; Park, Yeo Reum; Jang, Hara; Yoo, Heeseon; Park, Sang Ho; Lee, Seung Jae; Cho, Uhn-Soo

doi:10.1126/sciadv.aax0059

Title: MMOD-induced structural changes of hydroxylase in soluble methane monooxygenase

Journal Article · 02 October 2019 · Science Advances

DOI: https://doi.org/10.1126/sciadv.aax0059 · OSTI ID:1593446

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Univ. of Michigan, Ann Arbor, MI (United States)
Chonbuk National Univ., Jeonju (Republic of Korea)

Soluble methane monooxygenase in methanotrophs converts methane to methanol under ambient conditions. The maximum catalytic activity of hydroxylase (MMOH) is achieved through the interplay of its regulatory protein (MMOB) and reductase. An additional auxiliary protein, MMOD, functions as an inhibitor of MMOH; however, its inhibitory mechanism remains unknown. Here, we report the crystal structure of the MMOH-MMOD complex from Methylosinus sporium strain 5 (2.6 Å). Its structure illustrates that MMOD associates with the canyon region of MMOH where MMOB binds. Although MMOD and MMOB recognize the same binding site, each binding component triggers different conformational changes toward MMOH, which then respectively lead to the inhibition and activation of MMOH. Particularly, MMOD binding perturbs the di-iron geometry by inducing two major MMOH conformational changes, i.e., MMOH β subunit disorganization and subsequent His¹⁴⁷ dissociation with Fe1 coordination. Furthermore, 1,6-hexanediol, a mimic of the products of sMMO, reveals the substrate access route.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Research Foundation of Korea (NRF); The Biomedical Research Council (BMRC)

Grant/Contract Number:: NRF-2015M3D3A1A01064876; R01 DK111465

OSTI ID:: 1593446

Journal Information:: Science Advances, Vol. 5, Issue 10; ISSN 2375-2548

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 22 works

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References (62)

New findings in methane-utilizing bacteria highlight their importance in the biosphere and their commercial potential Higgins, I. J.; Best, D. J.; Hammond, R. C. Nature, Vol. 286, Issue 5773 https://doi.org/10.1038/286561a0	journal	August 1980
Oxidation-reduction potentials of the methane monooxygenase hydroxylase component from Methylosinus trichosporium OB3b Paulsen, Kim E.; Liu, Yi; Fox, Brian G. Biochemistry, Vol. 33, Issue 3 https://doi.org/10.1021/bi00169a013	journal	January 1994
Copper-dependent reciprocal transcriptional regulation of methane monooxygenase genes in Methylococcus capsulatus and Methylosinus trichosporium Nielsen, Allan K.; Gerdes, Kenn; Murrell, J. Colin Molecular Microbiology, Vol. 25, Issue 02 https://doi.org/10.1046/j.1365-2958.1997.4801846.x	journal	July 1997
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
NMR Structure of the Flavin Domain from Soluble Methane Monooxygenase Reductase from Methylococcus capsulatus (Bath) Chatwood, Lisa L.; Mueller, Jens; Gross, John D. Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr6295	dataset	January 2004
Preparation and X-ray Structures of Metal-Free, Dicobalt and Dimanganese Forms of Soluble Methane Monooxygenase Hydroxylase from Methylococcus capsulatus (Bath) † Sazinsky, Matthew H.; Merkx, Maarten; Cadieux, Elisabeth Biochemistry, Vol. 43, Issue 51 https://doi.org/10.1021/bi048140z	journal	December 2004
NMR Structure of the [2Fe-2S] Ferredoxin Domain from Soluble Methane Monooxygenase Reductase and Interaction with Its Hydroxylase † , ‡ Müller, Jens; Lugovskoy, Alexey A.; Wagner, Gerhard Biochemistry, Vol. 41, Issue 1 https://doi.org/10.1021/bi015668k	journal	January 2002
NMR Structure of the Amino-Terminal Domain of the Lambda Integrase Protein in Complex with DNA: Immobilization of a Flexible Tail Facilitates Beta-Sheet Recognition of the Major Groove Fadeev, Evgeny A.; Sam, My D.; Clubb, Robert T. Journal of Molecular Biology, Vol. 388, Issue 4 https://doi.org/10.1016/j.jmb.2009.03.041	journal	May 2009
Control of substrate access to the active site in methane monooxygenase Lee, Seung Jae; McCormick, Michael S.; Lippard, Stephen J. Nature, Vol. 494, Issue 7437 https://doi.org/10.1038/nature11880	journal	February 2013
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
NMR Structure of the [2Fe-2S] Ferredoxin Domain from Soluble Methane Monooxygenase Reductase and Interaction with its Hydroxylase Muller, J.; Lugovskoy, A. A.; Wagner, G. Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr5148	dataset	January 2002
Methanobactin and MmoD work in concert to act as the ‘copper-switch’ in methanotrophs: Copper-switch in methanotrophy Semrau, Jeremy D.; Jagadevan, Sheeja; DiSpirito, Alan A. Environmental Microbiology https://doi.org/10.1111/1462-2920.12150	journal	May 2013
NMR Structure of the Flavin Domain from Soluble Methane Monooxygenase Reductase from Methylococcus capsulatus (Bath) † , ‡ Chatwood, Lisa L.; Müller, Jens; Gross, John D. Biochemistry, Vol. 43, Issue 38 https://doi.org/10.1021/bi049066n	journal	September 2004
High-Energy-Resolution Fluorescence-Detected X-ray Absorption of the Q Intermediate of Soluble Methane Monooxygenase Castillo, Rebeca G.; Banerjee, Rahul; Allpress, Caleb J. Journal of the American Chemical Society, Vol. 139, Issue 49 https://doi.org/10.1021/jacs.7b09560	journal	November 2017
Crystal structure of a bacterial non-haem iron hydroxylase that catalyses the biological oxidation of methane Rosenzweig, Amy C.; Frederick, Christin A.; Lippard, Stephen J. Nature, Vol. 366, Issue 6455 https://doi.org/10.1038/366537a0	journal	December 1993
Structure of the soluble methane monooxygenase regulatory protein B Walters, K. J.; Gassner, G. T.; Lippard, S. J. Proceedings of the National Academy of Sciences, Vol. 96, Issue 14 https://doi.org/10.1073/pnas.96.14.7877	journal	July 1999
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
Protein production by auto-induction in high-density shaking cultures Studier, F. William Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234 https://doi.org/10.1016/j.pep.2005.01.016	journal	May 2005
Structure of the key species in the enzymatic oxidation of methane to methanol Banerjee, Rahul; Proshlyakov, Yegor; Lipscomb, John D. Nature, Vol. 518, Issue 7539 https://doi.org/10.1038/nature14160	journal	January 2015
Dioxygen Activation by Enzymes Containing Binuclear Non-Heme Iron Clusters Wallar, Bradley J.; Lipscomb, John D. Chemical Reviews, Vol. 96, Issue 7 https://doi.org/10.1021/cr9500489	journal	January 1996
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6 https://doi.org/10.1007/s00775-020-01814-y	journal	August 2020
Methane monooxygenase component B and reductase alter the regioselectivity of the hydroxylase component-catalyzed reactions. A novel role for protein-protein interactions in an oxygenase mechanism. Froland, W. A.; Andersson, K. K.; Lee, S. K. Journal of Biological Chemistry, Vol. 267, Issue 25 https://doi.org/10.1016/S0021-9258(19)37083-8	journal	September 1992
Why OrfY?: CHARACTERIZATION OF MMOD, A LONG OVERLOOKED COMPONENT OF THE SOLUBLE METHANE MONOOXYGENASE FROM Merkx, Maarten; Lippard, Stephen J. Journal of Biological Chemistry, Vol. 277, Issue 8 https://doi.org/10.1074/jbc.M107712200	journal	November 2001
Methanobactin and the Link between Copper and Bacterial Methane Oxidation DiSpirito, Alan A.; Semrau, Jeremy D.; Murrell, J. Colin Microbiology and Molecular Biology Reviews, Vol. 80, Issue 2 https://doi.org/10.1128/MMBR.00058-15	journal	March 2016
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
Product Bound Structures of the Soluble Methane Monooxygenase Hydroxylase from Methylococcus capsulatus (Bath): Protein Motion in the α-Subunit Sazinsky, Matthew H.; Lippard, Stephen J. Journal of the American Chemical Society, Vol. 127, Issue 16 https://doi.org/10.1021/ja044099b	journal	April 2005
The relationship of biomass, polysaccharide and H2 formation in the wild-type and nifA/nifB mutants of Rhodobacter capsulatus Klein, G.; Klipp, W.; Jahn, A. Archives of Microbiology, Vol. 155, Issue 5 https://doi.org/10.1007/BF00244965	journal	April 1991
Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Krissinel, E.; Henrick, K. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904026460	journal	November 2004
Dioxygen Activation and Methane Hydroxylation by Soluble Methane Monooxygenase: A Tale of Two Irons and Three Proteins Merkx, Maarten; Kopp, Daniel A.; Sazinsky, Matthew H. Angewandte Chemie International Edition, Vol. 40, Issue 15 https://doi.org/10.1002/1521-3773(20010803)40:15<2782::AID-ANIE2782>3.0.CO;2-P	journal	August 2001
Electron Transfer Control in Soluble Methane Monooxygenase Wang, Weixue; Iacob, Roxana E.; Luoh, Rebecca P. Journal of the American Chemical Society, Vol. 136, Issue 27 https://doi.org/10.1021/ja504688z	journal	June 2014
Electron-Transfer Reactions of the Reductase Component of Soluble Methane Monooxygenase from Methylococcus capsulatus (Bath) † Kopp, Daniel A.; Gassner, George T.; Blazyk, Jessica L. Biochemistry, Vol. 40, Issue 49 https://doi.org/10.1021/bi015556t	journal	December 2001
Enzymatic Oxidation of Methane Sirajuddin, Sarah; Rosenzweig, Amy C. Biochemistry, Vol. 54, Issue 14 https://doi.org/10.1021/acs.biochem.5b00198	journal	March 2015
Sequencing and analysis of the Methylococcus capsulatus (Bath) soluble methane monooxygenase genes: Sequencing and analysis of sMMO genes Coufal, David E.; Blazyk, Jessica L.; Whittington, Douglas A. European Journal of Biochemistry, Vol. 267, Issue 8 https://doi.org/10.1046/j.1432-1327.2000.01210.x	journal	April 2000
Crystal structure of the hydroxylase component of methane monooxygenase from Methylosinus trichosporium OB3b Elango, Nates An; Radhakrishnan, Ramaswamy; Froland, Wayne A. Protein Science, Vol. 6, Issue 3 https://doi.org/10.1002/pro.5560060305	journal	March 1997
Alkane Oxidation: Methane Monooxygenases, Related Enzymes, and Their Biomimetics Wang, Vincent C. -C.; Maji, Suman; Chen, Peter P. -Y. Chemical Reviews, Vol. 117, Issue 13 https://doi.org/10.1021/acs.chemrev.6b00624	journal	February 2017
Dioxygen Activation by Nonheme Diiron Enzymes: Diverse Dioxygen Adducts, High-Valent Intermediates, and Related Model Complexes Jasniewski, Andrew J.; Que, Lawrence Chemical Reviews, Vol. 118, Issue 5 https://doi.org/10.1021/acs.chemrev.7b00457	journal	December 2017
FEM: feature-enhanced map Afonine, Pavel V.; Moriarty, Nigel W.; Mustyakimov, Marat Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 3 https://doi.org/10.1107/S1399004714028132	journal	February 2015
Reactions of the Peroxo Intermediate of Soluble Methane Monooxygenase Hydroxylase with Ethers Beauvais, Laurance G.; Lippard, Stephen J. Journal of the American Chemical Society, Vol. 127, Issue 20 https://doi.org/10.1021/ja050865i	journal	May 2005
Methanotrophic bacteria. Hanson, R. S.; Hanson, T. E. Microbiological reviews, Vol. 60, Issue 2 https://doi.org/10.1128/MR.60.2.439-471.1996	journal	January 1996
An optimized growth medium for increased recombinant protein secretion titer via the type III secretion system Burdette, Lisa Ann; Wong, Han Teng; Tullman-Ercek, Danielle Microbial Cell Factories, Vol. 20, Issue 1 https://doi.org/10.1186/s12934-021-01536-z	journal	February 2021
Dioxygen Activation in Soluble Methane Monooxygenase Tinberg, Christine E.; Lippard, Stephen J. Accounts of Chemical Research, Vol. 44, Issue 4 https://doi.org/10.1021/ar1001473	journal	April 2011
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Structure of the Soluble Methane Monooxygenase Regulatory Protein B Walters, K. J.; Gassner, G. T.; Lippard, S. J. Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr4431	dataset	January 2003
The methane monooxygenase gene cluster of Methylosinus trichosporium: cloning and sequencing of the mmoC gene Cardy, D. L. N.; Laidler, V.; Salmond, G. P. C. Archives of Microbiology, Vol. 156, Issue 6 https://doi.org/10.1007/bf00245395	journal	November 1991
NMR Structure of the Amino-Terminal Domain of the Lambda Integrase Protein in Complex with DNA: Immobilization of a Flexible Tail Facilitates Beta-Sheet Recognition of the Major Groove Fadeev, Evgeny A.; Sam, My D.; Clubb, Robert T. Journal of Molecular Biology, Vol. 388, Issue 4 https://doi.org/10.1016/j.jmb.2009.03.041	journal	May 2009
Protein production by auto-induction in high-density shaking cultures Studier, F. William Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234 https://doi.org/10.1016/j.pep.2005.01.016	journal	May 2005
Mutational and structural analyses of the regulatory protein B of soluble methane monooxygenase from Methylococcus capsulatus (Bath) Brandstetter, Hans; Whittington, Douglas A.; Lippard, Stephen J. Chemistry & Biology, Vol. 6, Issue 7 https://doi.org/10.1016/s1074-5521(99)80062-3	journal	July 1999
Enzymatic Oxidation of Methane Sirajuddin, Sarah; Rosenzweig, Amy C. Biochemistry, Vol. 54, Issue 14 https://doi.org/10.1021/acs.biochem.5b00198	journal	March 2015
Alkane Oxidation: Methane Monooxygenases, Related Enzymes, and Their Biomimetics Wang, Vincent C. -C.; Maji, Suman; Chen, Peter P. -Y. Chemical Reviews, Vol. 117, Issue 13 https://doi.org/10.1021/acs.chemrev.6b00624	journal	February 2017
Dioxygen Activation by Nonheme Diiron Enzymes: Diverse Dioxygen Adducts, High-Valent Intermediates, and Related Model Complexes Jasniewski, Andrew J.; Que, Lawrence Chemical Reviews, Vol. 118, Issue 5 https://doi.org/10.1021/acs.chemrev.7b00457	journal	December 2017
Dioxygen Activation in Soluble Methane Monooxygenase Tinberg, Christine E.; Lippard, Stephen J. Accounts of Chemical Research, Vol. 44, Issue 4 https://doi.org/10.1021/ar1001473	journal	April 2011
Oxidation-reduction potentials of the methane monooxygenase hydroxylase component from Methylosinus trichosporium OB3b Paulsen, Kim E.; Liu, Yi; Fox, Brian G. Biochemistry, Vol. 33, Issue 3 https://doi.org/10.1021/bi00169a013	journal	January 1994
NMR Structure of the Flavin Domain from Soluble Methane Monooxygenase Reductase from Methylococcus capsulatus (Bath) † , ‡ Chatwood, Lisa L.; Müller, Jens; Gross, John D. Biochemistry, Vol. 43, Issue 38 https://doi.org/10.1021/bi049066n	journal	September 2004
Dioxygen Activation by Enzymes Containing Binuclear Non-Heme Iron Clusters Wallar, Bradley J.; Lipscomb, John D. Chemical Reviews, Vol. 96, Issue 7 https://doi.org/10.1021/cr9500489	journal	January 1996
Product Bound Structures of the Soluble Methane Monooxygenase Hydroxylase from Methylococcus capsulatus (Bath): Protein Motion in the α-Subunit Sazinsky, Matthew H.; Lippard, Stephen J. Journal of the American Chemical Society, Vol. 127, Issue 16 https://doi.org/10.1021/ja044099b	journal	April 2005
Reactions of the Peroxo Intermediate of Soluble Methane Monooxygenase Hydroxylase with Ethers Beauvais, Laurance G.; Lippard, Stephen J. Journal of the American Chemical Society, Vol. 127, Issue 20 https://doi.org/10.1021/ja050865i	journal	May 2005
Electron Transfer Control in Soluble Methane Monooxygenase Wang, Weixue; Iacob, Roxana E.; Luoh, Rebecca P. Journal of the American Chemical Society, Vol. 136, Issue 27 https://doi.org/10.1021/ja504688z	journal	June 2014
High-Energy-Resolution Fluorescence-Detected X-ray Absorption of the Q Intermediate of Soluble Methane Monooxygenase Castillo, Rebeca G.; Banerjee, Rahul; Allpress, Caleb J. Journal of the American Chemical Society, Vol. 139, Issue 49 https://doi.org/10.1021/jacs.7b09560	journal	November 2017
New findings in methane-utilizing bacteria highlight their importance in the biosphere and their commercial potential Higgins, I. J.; Best, D. J.; Hammond, R. C. Nature, Vol. 286, Issue 5773 https://doi.org/10.1038/286561a0	journal	August 1980
Copper-dependent reciprocal transcriptional regulation of methane monooxygenase genes in Methylococcus capsulatus and Methylosinus trichosporium Nielsen, Allan K.; Gerdes, Kenn; Murrell, J. Colin Molecular Microbiology, Vol. 25, Issue 02 https://doi.org/10.1046/j.1365-2958.1997.4801846.x	journal	July 1997
Structure of the soluble methane monooxygenase regulatory protein B Walters, K. J.; Gassner, G. T.; Lippard, S. J. Proceedings of the National Academy of Sciences, Vol. 96, Issue 14 https://doi.org/10.1073/pnas.96.14.7877	journal	July 1999
Domain Engineering of the Reductase Component of Soluble Methane Monooxygenase from Methylococcus capsulatus (Bath) Blazyk, Jessica L.; Lippard, Stephen J. Journal of Biological Chemistry, Vol. 279, Issue 7 https://doi.org/10.1074/jbc.m308940200	journal	November 2003

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