Recovery of particulate methane monooxygenase structure and activity in a lipid bilayer

Koo, Christopher W.; Tucci, Frank J.; He, Yuan; Rosenzweig, Amy C.

doi:10.1126/science.abm3282

Recovery of particulate methane monooxygenase structure and activity in a lipid bilayer

Journal Article · Fri Mar 18 04:00:00 EDT 2022 · Science

DOI:https://doi.org/10.1126/science.abm3282· OSTI ID:1982957

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Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA.
Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA.; Department of Chemistry, Northwestern University, Evanston, IL 60208, USA.

Bacterial methane oxidation using the enzyme particulate methane monooxygenase (pMMO) contributes to the removal of environmental methane, a potent greenhouse gas. Crystal structures determined using inactive, detergent-solubilized pMMO lack several conserved regions neighboring the proposed active site. We show that reconstituting pMMO in nanodiscs with lipids extracted from the native organism restores methane oxidation activity. Multiple nanodisc-embedded pMMO structures determined by cryo–electron microscopy to 2.14- to 2.46-angstrom resolution reveal the structure of pMMO in a lipid environment. The resulting model includes stabilizing lipids, regions of the PmoA and PmoC subunits not observed in prior structures, and a previously undetected copper-binding site in the PmoC subunit with an adjacent hydrophobic cavity. These structures provide a revised framework for understanding and engineering pMMO function.

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Sponsoring Organization:: USDOE

DOE Contract Number:: AC05-76RL01830

OSTI ID:: 1982957

Journal Information:: Science, Journal Name: Science Journal Issue: 6586 Vol. 375; ISSN 0036-8075

Publisher:: AAAS

Country of Publication:: United States

Language:: English

References (58)

Crystal structure of a membrane-bound metalloenzyme that catalyses the biological oxidation of methane Lieberman, Raquel L.; Rosenzweig, Amy C. Nature, Vol. 434, Issue 7030 https://doi.org/10.1038/nature03311	journal	January 2005
A tale of two methane monooxygenases Ross, Matthew O.; Rosenzweig, Amy C. JBIC Journal of Biological Inorganic Chemistry, Vol. 22, Issue 2-3 https://doi.org/10.1007/s00775-016-1419-y	journal	November 2016
Deciphering the oxygen activation mechanism at the CuC site of particulate methane monooxygenase Peng, Wei; Qu, Xiaoyang; Shaik, Sason Nature Catalysis, Vol. 4, Issue 4 https://doi.org/10.1038/s41929-021-00591-4	journal	April 2021
A Rapid Method of Total Lipid Extraction and Purification Bligh, E. G.; Dyer, W. J. Canadian Journal of Biochemistry and Physiology, Vol. 37, Issue 1 https://doi.org/10.1139/y59-099	journal	January 1959
Coordination of the Copper Centers in Particulate Methane Monooxygenase: Comparison between Methanotrophs and Characterization of the Cu_C Site by EPR and ENDOR Spectroscopies Jodts, Richard J.; Ross, Matthew O.; Koo, Christopher W. Journal of the American Chemical Society, Vol. 143, Issue 37 https://doi.org/10.1021/jacs.1c07018	journal	September 2021
The PmoB subunit of particulate methane monooxygenase (pMMO) in Methylococcus capsulatus (Bath): The CuI sponge and its function Lu, Yu-Jhang; Hung, Mu-Cheng; Chang, Brian T. -A. Journal of Inorganic Biochemistry, Vol. 196 https://doi.org/10.1016/j.jinorgbio.2019.04.005	journal	July 2019
Jalview Version 2--a multiple sequence alignment editor and analysis workbench Waterhouse, A. M.; Procter, J. B.; Martin, D. M. A. Bioinformatics, Vol. 25, Issue 9 https://doi.org/10.1093/bioinformatics/btp033	journal	January 2009
Role of Arginine Residues in the Active Site of the Membrane-Bound Lytic Transglycosylase B from Pseudomonas aeruginosa Reid, Christopher W.; Blackburn, Neil T.; Clarke, Anthony J. Biochemistry, Vol. 45, Issue 7 https://doi.org/10.1021/bi052342t	journal	January 2006
Metalloprotein Crystallography: More than a Structure Bowman, Sarah E. J.; Bridwell-Rabb, Jennifer; Drennan, Catherine L. Accounts of Chemical Research, Vol. 49, Issue 4 https://doi.org/10.1021/acs.accounts.5b00538	journal	March 2016
Engineered Methanotrophy: A Sustainable Solution for Methane-Based Industrial Biomanufacturing Nguyen, Anh Duc; Lee, Eun Yeol Trends in Biotechnology, Vol. 39, Issue 4 https://doi.org/10.1016/j.tibtech.2020.07.007	journal	April 2021
Membrane protein assembly into Nanodiscs Bayburt, Timothy H.; Sligar, Stephen G. FEBS Letters, Vol. 584, Issue 9 https://doi.org/10.1016/j.febslet.2009.10.024	journal	October 2009
UCSF ChimeraX : Structure visualization for researchers, educators, and developers Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Protein Science, Vol. 30, Issue 1 https://doi.org/10.1002/pro.3943	journal	October 2020
Particulate methane monooxygenase contains only mononuclear copper centers Ross, Matthew O.; MacMillan, Fraser; Wang, Jingzhou Science, Vol. 364, Issue 6440 https://doi.org/10.1126/science.aav2572	journal	May 2019
MAFFT: Iterative Refinement and Additional Methods Katoh, Kazutaka; Standley, Daron M. Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-646-7_8	book	January 2013
Towards a unified understanding of the copper sites in particulate methane monooxygenase: an X-ray absorption spectroscopic investigation Cutsail, George E.; Ross, Matthew O.; Rosenzweig, Amy C. Chemical Science, Vol. 12, Issue 17 https://doi.org/10.1039/D1SC00676B	journal	January 2021
Modeling the soil consumption of atmospheric methane at the global scale: SOIL CONSUMPTION OF ATMOSPHERIC METHANE Curry, Charles L. Global Biogeochemical Cycles, Vol. 21, Issue 4 https://doi.org/10.1029/2006GB002818	journal	November 2007
Appion: An integrated, database-driven pipeline to facilitate EM image processing Lander, Gabriel C.; Stagg, Scott M.; Voss, Neil R. Journal of Structural Biology, Vol. 166, Issue 1 https://doi.org/10.1016/j.jsb.2009.01.002	journal	April 2009
Native top-down mass spectrometry provides insights into the copper centers of membrane-bound methane monooxygenase Ro, Soo Y.; Schachner, Luis F.; Koo, Christopher W. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10590-6	journal	June 2019
Copper Centers in the Cryo-EM Structure of Particulate Methane Monooxygenase Reveal the Catalytic Machinery of Methane Oxidation Chang, W. -H.; Lin, H. -H.; Tsai, I-K. Journal of the American Chemical Society, Vol. 143, Issue 26 https://doi.org/10.1021/jacs.1c04082	journal	June 2021
Mössbauer Studies of the Membrane-Associated Methane Monooxygenase from Methylococcus capsulatus Bath: Evidence for a Diiron Center Martinho, Marlène; Choi, Dong W.; DiSpirito, Alan A. Journal of the American Chemical Society, Vol. 129, Issue 51 https://doi.org/10.1021/ja077682b	journal	December 2007
Structural Reorganization of the Copper Binding Site Involving Thr15 of Mavicyanin from Cucurbita pepo medullosa (Zucchini) upon Reduction Xie, Y. Journal of Biochemistry, Vol. 137, Issue 4 https://doi.org/10.1093/jb/mvi062	journal	April 2005
Biochemistry of aerobic biological methane oxidation Koo, Christopher W.; Rosenzweig, Amy C. Chemical Society Reviews, Vol. 50, Issue 5 https://doi.org/10.1039/D0CS01291B	journal	January 2021
Evidence That a Type-2 NADH:Quinone Oxidoreductase Mediates Electron Transfer to Particulate Methane Monooxygenase in Methylococcus capsulatus Cook, Scott A.; Shiemke, Andrew K. Archives of Biochemistry and Biophysics, Vol. 398, Issue 1 https://doi.org/10.1006/abbi.2001.2628	journal	February 2002
The Active-Site Structure of Umecyanin, the Stellacyanin from Horseradish Roots Dennison, Christopher; Harrison, Mark D. Journal of the American Chemical Society, Vol. 126, Issue 8 https://doi.org/10.1021/ja0375378	journal	February 2004
Arginine residues at internal positions in a protein are always charged Harms, M. J.; Schlessman, J. L.; Sue, G. R. Proceedings of the National Academy of Sciences, Vol. 108, Issue 47 https://doi.org/10.1073/pnas.1104808108	journal	November 2011
Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix Liebschner, Dorothee; Afonine, Pavel V.; Baker, Matthew L. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10 https://doi.org/10.1107/S2059798319011471	journal	October 2019
Methane-Oxidizing Enzymes: An Upstream Problem in Biological Gas-to-Liquids Conversion Lawton, Thomas J.; Rosenzweig, Amy C. Journal of the American Chemical Society, Vol. 138, Issue 30 https://doi.org/10.1021/jacs.6b04568	journal	July 2016
Oxidation of methane by a biological dicopper centre Balasubramanian, Ramakrishnan; Smith, Stephen M.; Rawat, Swati Nature, Vol. 465, Issue 7294 https://doi.org/10.1038/nature08992	journal	April 2010
New tools for automated high-resolution cryo-EM structure determination in RELION-3 Zivanov, Jasenko; Nakane, Takanori; Forsberg, Björn O. eLife, Vol. 7 https://doi.org/10.7554/eLife.42166	journal	November 2018
CTFFIND4: Fast and accurate defocus estimation from electron micrographs Rohou, Alexis; Grigorieff, Nikolaus Journal of Structural Biology, Vol. 192, Issue 2 https://doi.org/10.1016/j.jsb.2015.08.008	journal	November 2015
Estimation of high-order aberrations and anisotropic magnification from cryo-EM data sets in RELION -3.1 Zivanov, Jasenko; Nakane, Takanori; Scheres, Sjors H. W. IUCrJ, Vol. 7, Issue 2 https://doi.org/10.1107/S2052252520000081	journal	February 2020
Genetic Systems for Moderately Halo(alkali)philic Bacteria of the Genus Methylomicrobium Ojala, David S.; Beck, David A. C.; Kalyuzhnaya, Marina G. Methods in Methane Metabolism, Part B: Methanotrophy https://doi.org/10.1016/B978-0-12-386905-0.00007-3	book	January 2011
Characterization of the Particulate Methane Monooxygenase Metal Centers in Multiple Redox States by X-ray Absorption Spectroscopy Lieberman, Raquel L.; Kondapalli, Kalyan C.; Shrestha, Deepak B. Inorganic Chemistry, Vol. 45, Issue 20 https://doi.org/10.1021/ic060739v	journal	October 2006
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
DeepEMhancer: a deep learning solution for cryo-EM volume post-processing Sanchez-Garcia, Ruben; Gomez-Blanco, Josue; Cuervo, Ana Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-02399-1	journal	July 2021
UCSF ChimeraX: Meeting modern challenges in visualization and analysis: UCSF ChimeraX Visualization System Goddard, Thomas D.; Huang, Conrad C.; Meng, Elaine C. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3235	journal	September 2017
Redox Potentiometry Studies of Particulate Methane Monooxygenase: Support for a Trinuclear Copper Cluster Active Site Chan, Sunney I.; Wang, Vincent C. -C.; Lai, Jeff C. -H. Angewandte Chemie International Edition, Vol. 46, Issue 12 https://doi.org/10.1002/anie.200604647	journal	March 2007
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
CASTp 3.0: computed atlas of surface topography of proteins Tian, Wei; Chen, Chang; Lei, Xue Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky473	journal	June 2018
Bacterial cytosolic proteins with a high capacity for Cu(I) that protect against copper toxicity Vita, Nicolas; Landolfi, Gianpiero; Baslé, Arnaud Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep39065	journal	December 2016
The Metal Centers of Particulate Methane Monooxygenase from Methylosinus trichosporium OB3b ^† ^‡ Hakemian, Amanda S.; Kondapalli, Kalyan C.; Telser, Joshua Biochemistry, Vol. 47, Issue 26 https://doi.org/10.1021/bi800598h	journal	July 2008
Methane emissions as energy reservoir: Context, scope, causes and mitigation strategies Chai, Xiaoli; Tonjes, David J.; Mahajan, Devinder Progress in Energy and Combustion Science, Vol. 56 https://doi.org/10.1016/j.pecs.2016.05.001	journal	September 2016
The Membrane-Associated Methane Monooxygenase (pMMO) and pMMO-NADH:Quinone Oxidoreductase Complex from Methylococcus capsulatus Bath Choi, Dong-W.; Kunz, Ryan C.; Boyd, Eric S. Journal of Bacteriology, Vol. 185, Issue 19 https://doi.org/10.1128/JB.185.19.5755-5764.2003	journal	September 2003
Nanodiscs: A Controlled Bilayer Surface for the Study of Membrane Proteins McLean, Mark A.; Gregory, Michael C.; Sligar, Stephen G. Annual Review of Biophysics, Vol. 47, Issue 1 https://doi.org/10.1146/annurev-biophys-070816-033620	journal	May 2018
Automated molecular microscopy: The new Leginon system Suloway, Christian; Pulokas, James; Fellmann, Denis Journal of Structural Biology, Vol. 151, Issue 1 https://doi.org/10.1016/j.jsb.2005.03.010	journal	July 2005
Probing the Hydrophobic Pocket of the Active Site in the Particulate Methane Monooxygenase (pMMO) fromMethylococcus capsulatus (Bath) by Variable Stereoselective Alkane Hydroxylation and Olefin Epoxidation Ng, Kok-Yaoh; Tu, Li-Chun; Wang, Yane-Shih ChemBioChem, Vol. 9, Issue 7 https://doi.org/10.1002/cbic.200700628	journal	May 2008
From micelles to bicelles: Effect of the membrane on particulate methane monooxygenase activity Ro, Soo Y.; Ross, Matthew O.; Deng, Yue Wen Journal of Biological Chemistry, Vol. 293, Issue 27 https://doi.org/10.1074/jbc.RA118.003348	journal	May 2018
A Simple Method for the Isolation and Purification of Total Lipides from Animal Tissues Folch, Jordi; Lees, M.; Stanley, G. H. Sloane Journal of Biological Chemistry, Vol. 226, Issue 1 https://doi.org/10.1016/S0021-9258(18)64849-5	journal	May 1957
Purified particulate methane monooxygenase from Methylococcus capsulatus (Bath) is a dimer with both mononuclear copper and a copper-containing cluster Lieberman, R. L.; Shrestha, D. B.; Doan, P. E. Proceedings of the National Academy of Sciences, Vol. 100, Issue 7 https://doi.org/10.1073/pnas.0536703100	journal	March 2003
Crystal Structure and Characterization of Particulate Methane Monooxygenase from Methylocystis species Strain M Smith, Stephen M.; Rawat, Swati; Telser, Joshua Biochemistry, Vol. 50, Issue 47 https://doi.org/10.1021/bi200801z	journal	November 2011
A missing link in cupredoxins: Crystal structure of cucumber stellacyanin at 1.6 Å resolution Hart, P. John; Eisenberg, David; Nersissian, Aram M. Protein Science, Vol. 5, Issue 11 https://doi.org/10.1002/pro.5560051104	journal	November 1996
Detergents as Tools in Membrane Biochemistry Garavito, R. Michael; Ferguson-Miller, Shelagh Journal of Biological Chemistry, Vol. 276, Issue 35 https://doi.org/10.1074/jbc.R100031200	journal	June 2001
Feeling the hidden mechanical forces in lipid bilayer is an original sense Anishkin, A.; Loukin, S. H.; Teng, J. Proceedings of the National Academy of Sciences, Vol. 111, Issue 22 https://doi.org/10.1073/pnas.1313364111	journal	May 2014
Climate change, human health, and epidemiological transition Barrett, Bruce; Charles, Joel W.; Temte, Jonathan L. Preventive Medicine, Vol. 70 https://doi.org/10.1016/j.ypmed.2014.11.013	journal	January 2015
Quantum Refinement Does Not Support Dinuclear Copper Sites in Crystal Structures of Particulate Methane Monooxygenase Cao, Lili; Caldararu, Octav; Rosenzweig, Amy C. Angewandte Chemie International Edition, Vol. 57, Issue 1 https://doi.org/10.1002/anie.201708977	journal	December 2017
Effects of Zinc on Particulate Methane Monooxygenase Activity and Structure Sirajuddin, Sarah; Barupala, Dulmini; Helling, Stefan Journal of Biological Chemistry, Vol. 289, Issue 31 https://doi.org/10.1074/jbc.M114.581363	journal	June 2014
Biological conversion of methane to chemicals and fuels: technical challenges and issues Hwang, In Yeub; Nguyen, Anh Duc; Nguyen, Thu Thi Applied Microbiology and Biotechnology, Vol. 102, Issue 7 https://doi.org/10.1007/s00253-018-8842-7	journal	February 2018
Methane and Trichloroethylene Degradation byMethylosinus trichosporium OB3b Expressing Particulate Methane Monooxygenase Lontoh, Sonny; Semrau, Jeremy D. Applied and Environmental Microbiology, Vol. 64, Issue 3 https://doi.org/10.1128/AEM.64.3.1106-1114.1998	journal	March 1998

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