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http://dx.doi.org/10.4014/jmb.2201.01029

Electron Transfer to Hydroxylase through Component Interactions in Soluble Methane Monooxygenase  

Lee, Chaemin (Department of Chemistry, Jeonbuk National University)
Hwang, Yunha (Department of Chemistry, Jeonbuk National University)
Kang, Hyun Goo (Department of Neurology, Research Institute of Clinical Medicine of Jeonbuk National University and Biomedical Research Institute of Jeonbuk National University Hospital)
Lee, Seung Jae (Department of Chemistry, Jeonbuk National University)
Publication Information
Journal of Microbiology and Biotechnology / v.32, no.3, 2022 , pp. 287-293 More about this Journal
Abstract
The hydroxylation of methane (CH4) is crucial to the field of environmental microbiology, owing to the heat capacity of methane, which is much higher than that of carbon dioxide (CO2). Soluble methane monooxygenase (sMMO), a member of the bacterial multicomponent monooxygenase (BMM) superfamily, is essential for the hydroxylation of specific substrates, including hydroxylase (MMOH), regulatory component (MMOB), and reductase (MMOR). The diiron active site positioned in the MMOH α-subunit is reduced through the interaction of MMOR in the catalytic cycle. The electron transfer pathway, however, is not yet fully understood due to the absence of complex structures with reductases. A type II methanotroph, Methylosinus sporium 5, successfully expressed sMMO and hydroxylase, which were purified for the study of the mechanisms. Studies on the MMOH-MMOB interaction have demonstrated that Tyr76 and Trp78 induce hydrophobic interactions through π-π stacking. Structural analysis and sequencing of the ferredoxin domain in MMOR (MMOR-Fd) suggested that Tyr93 and Tyr95 could be key residues for electron transfer. Mutational studies of these residues have shown that the concentrations of flavin adenine dinucleotide (FAD) and iron ions are changed. The measurements of dissociation constants (Kds) between hydroxylase and mutated reductases confirmed that the binding affinities were not significantly changed, although the specific enzyme activities were significantly reduced by MMOR-Y93A. This result shows that Tyr93 could be a crucial residue for the electron transfer route at the interface between hydroxylase and reductase.
Keywords
Soluble methane monooxygenase (sMMO); electron transfer; reductase; bacterial multicomponent monooxygenase (BMM); hydroxylation;
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1 Hanson RS, Hanson TE. 1996. Methanotrophic bacteria. Microbiol. Rev. 60: 439-471.   DOI
2 Stainthorpe AC, Lees V, Salmond GPC, Dalton H, Murrell JC. 1990. The Methane monooxygenase gene cluster of Methylococcus capsulatus (Bath). Gene 91: 27-34.   DOI
3 Ward N, Larsen O, Sakwa J, Bruseth L, Khouri H, Durkin AS, et al. 2004. Genomic insights into methanotrophy: The complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol. 2: e303.   DOI
4 Balasubramanian R, Smith SM, Rawat S, Yatsunyk LA, Stemmler TL, Rosenzweig AC. 2010. Oxidation of methane by a biological dicopper centre. Nature 465: 115-119.   DOI
5 Choi DW, Kunz RC, Boyd ES, Semrau JD, Antholine WE, Han JI, et al. 2003. The membrane-associated methane monooxygenase (pMMO) and pMMO-NADH : quinone oxidoreductase complex from Methylococcus capsulatus Bath. J. Bacteriol. 185: 5755-5764.   DOI
6 Wang VC, Maji S, Chen PP, Lee HK, Yu SS, Chan SI. 2017. Alkane oxidation: methane monooxygenases, related enzymes, and their biomimetics. Chem. Rev. 117: 8574-8621.   DOI
7 Leahy JG, Batchelor PJ, Morcomb SM. 2003. Evolution of the soluble diiron monooxygenases. FEMS Microbiol. Rev. 27: 449-479.   DOI
8 Lee SY, Lipscomb JD. 1999. Oxygen activation catalyzed by methane monooxygenase hydroxylase component: proton delivery during the O-O bond cleavage steps. Biochemistry 38: 4423-4432.   DOI
9 Lee C, Ha SC, Rao Z, Hwang Y, Kim DS, Kim SY, et al. 2021. Elucidation of the electron transfer environment in the MMOR FAD-binding domain from Methylosinus sporium 5. Dalton Trans. 50: 16493-16498.   DOI
10 Chang SL, Wallar BJ, Lipscomb JD, Mayo KH. 1999. Solution structure of component B from methane monooxygenase derived through heteronuclear NMR and molecular modeling. Biochemistry 38: 5799-5812.   DOI
11 Chatwood LL, Muller J, Gross JD, Wagner G, Lippard SJ. 2004. NMR structure of the flavin domain from soluble methane monooxygenase reductase from Methylococcus capsulatus (Bath). Biochemistry 43: 11983-11991.   DOI
12 Banerjee R, Proshlyakov Y, Lipscomb JD, Proshlyakov DA. 2015. Structure of the key species in the enzymatic oxidation of methane to methanol. Nature 518: 431-434.   DOI
13 Liu Y, Nesheim JC, Lee SK, Lipscomb JD. 1995. Gating effects of component B on oxygen activation by the methane monooxygenase hydroxylase component. J. Biol. Chem. 270: 24662-24665.   DOI
14 Lieberman RL, Rosenzweig AC. 2004. Biological methane oxidation: regulation, biochemistry, and active site structure of particulate methane monooxygenase. Crit. Rev. Biochem. Mol. 39: 147-164.   DOI
15 Merkx M, Kopp DA, Sazinsky MH, Blazyk JL, Muller J, Lippard SJ. 2001. Dioxygen activation and methane hydroxylation by soluble methane monooxygenase: a tale of two irons and three proteins. Angew. Chem. Int. Ed. Engl. 40: 2782-2807.   DOI
16 Elango N, Radhakrishnan R, Froland WA, Wallar BJ, Earhart CA, Lipscomb JD, et al. 1997. Crystal structure of the hydroxylase component of methane monooxygenase from Methylosinus trichosporium OB3b. Protein Sci. 6: 556-568.   DOI
17 Lee SJ, McCormick MS, Lippard SJ, Cho US. 2013. Control of substrate access to the active site in methane monooxygenase. Nature 494: 380-384.   DOI
18 Brandstetter H, Whittington DA, Lippard SJ, Frederick CA. 1999. Mutational and structural analyses of the regulatory protein B of soluble methane monooxygenase from Methylococcus capsulatus (Bath). Chem. Biol. 6: 441-449.   DOI
19 Wang WX, Lippard SJ. 2014. Diiron oxidation state control of substrate access to the active site of soluble methane monooxygenase mediated by the regulatory component. J. Am. Chem. Soc. 136: 2244-2247.   DOI
20 Liu Y, Nesheim JC, Paulsen KE, Stankovich MT, Lipscomb JD. 1997. Roles of the methane monooxygenase reductase component in the regulation of catalysis. Biochemistry 36: 5223-5233.   DOI
21 Cutsail GE 3rd, Banerjee R, Zhou A, Que L Jr., Lipscomb JD, DeBeer S. 2018. High-resolution extended X-ray absorption fine structure analysis provides evidence for a longer Fe...Fe distance in the Q intermediate of methane monooxygenase. J. Am. Chem. Soc. 140: 16807-16820.   DOI
22 Rosenzweig AC, Frederick CA, Lippard SJ, Nordlund P. 1993. Crystal structure of a bacterial nonheme iron hydroxylase that catalyzes the biological oxidation of methane. Nature 366: 537-543.   DOI
23 Muller J, Lugovskoy AA, Wagner G, Lippard SJ. 2002. NMR structure of the [2Fe-2S] ferredoxin domain from soluble methane monooxygenase reductase and interaction with its hydroxylase. Biochemistry 41: 42-51.   DOI
24 Tinberg CE, Lippard SJ. 2011. Dioxygen activation in soluble methane monooxygenase. Acct. Chem. Res. 44: 280-288.   DOI
25 Kopp DA, Gassner GT, Blazyk JL, Lippard SJ. 2001. Electron-transfer reactions of the reductase component of soluble methane monooxygenase from Methylococcus capsulatus (Bath). Biochemistry 40: 14932-14941.   DOI
26 Liu KE, Valentine AM, Wang DL, Huynh BH, Edmondson DE, Salifoglou A, et al. 1995. Kinetic and spectroscopic characterization of intermediates and component interactions in reactions of methane monooxygenase from Methylococcus capsulatus (Bath). J. Am. Chem. Soc. 117: 10174-10185.   DOI
27 Balasubramanian R, Rosenzweig AC. 2007. Structural and mechanistic insights into methane oxidation by particulate methane monooxygenase. Acct. Chem. Res. 40: 573-580.   DOI
28 Hakemian AS, Rosenzweig AC. 2007. The biochemistry of methane oxidation. Annu. Rev. Biochem. 76: 223-241.   DOI
29 Sullivan JP, Dickinson D, Chase HA. 1998. Methanotrophs, Methylosinus trichosporium OB3b, sMMO, and their application to bioremediation. Crit. Rev. Microbiol. 24: 335-373.   DOI
30 Baik MH, Newcomb M, Friesner RA, Lippard SJ. 2003. Mechanistic studies on the hydroxylation of methane by methane monooxygenase. Chem. Rev. 103: 2385-2419.   DOI
31 Wallar BJ, Lipscomb JD. 1996. Dioxygen activation by enzymes containing binuclear non-heme iron clusters. Chem. Rev. 96: 2625-2657.   DOI
32 Sazinsky MH, Lippard SJ. 2005. Product bound structures of the soluble methane monooxygenase hydroxylase from Methylococcus capsulatus (Bath): protein motion in the α-subunit. J. Am. Chem. Soc. 127: 5814-5825.   DOI
33 Kim H, An S, Park YR, Jang H, Yoo H, Park SH, et al. 2019. MMOD-induced structural changes of hydroxylase in soluble methane monooxygenase. Sci. Adv. 5: eaax0059.   DOI
34 Blazyk JL, Gassner GT, Lippard SJ. 2005. Intermolecular electron-transfer reactions in soluble methane monooxygenase: a role for hysteresis in protein function. J. Am. Chem. Soc. 127: 17364-17376.   DOI
35 Chang SL, Wallar BJ, Lipscomb JD, Mayo KH. 2001. Residues in Methylosinus trichosporium OB3b methane monooxygenase component B involved in molecular interactions with reduced- and oxidized-hydroxylase component: a role for the N-terminus. Biochemistry 40: 9539-9551.   DOI
36 Walters KJ, Gassner GT, Lippard SJ, Wagner G. 1999. Structure of the soluble methane monooxygenase regulatory protein B. Proc. Natl. Acad. Sci. USA 96: 7877-7882.   DOI
37 Gassner GT, Lippard SJ. 1999. Component interactions in the soluble methane monooxygenase system from Methylococcus capsulatus (Bath). Biochemistry 38: 12768-12785.   DOI
38 Schulz CE, Castillo RG, Pantazis DA, DeBeer S, Neese F. 2021. Structure-spectroscopy correlations for intermediate Q of soluble methane monooxygenase: insights from QM/MM calculations. J. Am. Chem. Soc. 143: 6560-6577.   DOI
39 Amaral JA, Knowles R. 1995. Growth of methanotrophs in methane and oxygen counter gradients. FEMS Microbiol. Lett. 126: 215-220.   DOI
40 Jacobs AB, Banerjee R, Deweese DE, Braun A, Babicz JT, Jr., Gee LB, et al. 2021. Nuclear resonance vibrational spectroscopic definition of the Fe(IV)2 intermediate Q in methane monooxygenase and its reactivity. J. Am. Chem. Soc. 143: 16007-16029.   DOI
41 Tinberg CE, Lippard SJ. 2009. Revisiting the mechanism of dioxygen activation in soluble methane monooxygenase from M. capsulatus (Bath): evidence for a multi-step, proton-dependent reaction pathway. Biochemistry 48: 12145-12158.   DOI
42 Shu L, Nesheim JC, Kauffmann K, Munck E, Lipscomb JD, Que L, Jr. 1997. An Fe2IVO2 diamond core structure for the key intermediate Q of methane monooxygenase. Science 275: 515-518.   DOI
43 Liang AD, Lippard SJ. 2014. Component interactions and electron transfer in toluene/o-xylene monooxygenase. Biochemistry 53: 7368-7375.   DOI
44 Lund J, Dalton H. 1985. Further characterization of the FAD and Fe2S2 redox centres of component C, the NADH: acceptor reductase of the soluble methane monooxygenase of Methylococcus capsulatus (Bath). Eur. J. Biochem. 147: 291-296.   DOI
45 Murray LJ, Lippard SJ. 2007. Substrate trafficking and dioxygen activation in bacterial multicomponent monooxygenases. Acct. Chem. Res. 40: 466-474.   DOI
46 Rosenzweig AC, Sazinsky MH. 2006. Structural insights into dioxygen-activating copper enzymes. Curr. Opin. Struc. Biol. 16: 729-735.   DOI