The reaction mechanism of methyl-coenzyme M reductase: How an enzyme enforces strict binding order
Abstract
Methyl-coenzyme M reductase (MCR) is a nickel tetrahydrocorphinoid (coenzyme F430) containing enzyme involved in the biological synthesis and anaerobic oxidation of methane. MCR catalyzes the conversion of methyl-2-mercaptoethanesulfonate (methyl-SCoM) and N-7-mercaptoheptanoylthreonine phosphate (CoB7SH) to CH4 and the mixed disulfide CoBS-SCoM. In this study, the reaction of MCR from Methanothermobacter marburgensis, with its native substrates was investigated using static binding, chemical quench, and stopped-flow techniques. Rate constants were measured for each step in this strictly ordered ternary complex catalytic mechanism. Surprisingly, in the absence of the other substrate, MCR can bind either substrate; however, only one binary complex (MCR·methyl-SCoM) is productive whereas the other (MCR·CoB7SH) is inhibitory. Moreover, the kinetic data demonstrate that binding of methyl-SCoM to the inhibitory MCR·CoB7SH complex is highly disfavored (Kd = 56 mM). However, binding of CoB7SH to the productive MCR·methyl-SCoM complex to form the active ternary complex (CoB7SH·MCR(NiI)·CH3SCoM) is highly favored (Kd = 79 μM). Only then can the chemical reaction occur (kobs = 20 s-1 at 25 °C), leading to rapid formation and dissociation of CH4 leaving the binary product complex (MCR(NiII)·CoB7S-·SCoM), which undergoes electron transfer to regenerate Ni(I) and the final product CoBS-SCoM. In conclusion, this first rapid kinetics study of MCR withmore »
- Authors:
-
- Univ. of Michigan, Ann Arbor, MI (United States)
- Publication Date:
- Research Org.:
- Univ. of Michigan, Ann Arbor, MI (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1348414
- Grant/Contract Number:
- FG02-08ER15931
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 290; Journal Issue: 15; Journal ID: ISSN 0021-9258
- Publisher:
- American Society for Biochemistry and Molecular Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; electron paramagnetic resonance (EPR); enzyme inhibitor; enzyme kinetics; enzyme mechanism; metalloenzyme; nickel; pre-steady-state kinetics
Citation Formats
Wongnate, Thanyaporn, and Ragsdale, Stephen W. The reaction mechanism of methyl-coenzyme M reductase: How an enzyme enforces strict binding order. United States: N. p., 2015.
Web. doi:10.1074/jbc.m115.636761.
Wongnate, Thanyaporn, & Ragsdale, Stephen W. The reaction mechanism of methyl-coenzyme M reductase: How an enzyme enforces strict binding order. United States. https://doi.org/10.1074/jbc.m115.636761
Wongnate, Thanyaporn, and Ragsdale, Stephen W. Tue .
"The reaction mechanism of methyl-coenzyme M reductase: How an enzyme enforces strict binding order". United States. https://doi.org/10.1074/jbc.m115.636761. https://www.osti.gov/servlets/purl/1348414.
@article{osti_1348414,
title = {The reaction mechanism of methyl-coenzyme M reductase: How an enzyme enforces strict binding order},
author = {Wongnate, Thanyaporn and Ragsdale, Stephen W.},
abstractNote = {Methyl-coenzyme M reductase (MCR) is a nickel tetrahydrocorphinoid (coenzyme F430) containing enzyme involved in the biological synthesis and anaerobic oxidation of methane. MCR catalyzes the conversion of methyl-2-mercaptoethanesulfonate (methyl-SCoM) and N-7-mercaptoheptanoylthreonine phosphate (CoB7SH) to CH4 and the mixed disulfide CoBS-SCoM. In this study, the reaction of MCR from Methanothermobacter marburgensis, with its native substrates was investigated using static binding, chemical quench, and stopped-flow techniques. Rate constants were measured for each step in this strictly ordered ternary complex catalytic mechanism. Surprisingly, in the absence of the other substrate, MCR can bind either substrate; however, only one binary complex (MCR·methyl-SCoM) is productive whereas the other (MCR·CoB7SH) is inhibitory. Moreover, the kinetic data demonstrate that binding of methyl-SCoM to the inhibitory MCR·CoB7SH complex is highly disfavored (Kd = 56 mM). However, binding of CoB7SH to the productive MCR·methyl-SCoM complex to form the active ternary complex (CoB7SH·MCR(NiI)·CH3SCoM) is highly favored (Kd = 79 μM). Only then can the chemical reaction occur (kobs = 20 s-1 at 25 °C), leading to rapid formation and dissociation of CH4 leaving the binary product complex (MCR(NiII)·CoB7S-·SCoM), which undergoes electron transfer to regenerate Ni(I) and the final product CoBS-SCoM. In conclusion, this first rapid kinetics study of MCR with its natural substrates describes how an enzyme can enforce a strictly ordered ternary complex mechanism and serves as a template for identification of the reaction intermediates.},
doi = {10.1074/jbc.m115.636761},
journal = {Journal of Biological Chemistry},
number = 15,
volume = 290,
place = {United States},
year = {Tue Feb 17 00:00:00 EST 2015},
month = {Tue Feb 17 00:00:00 EST 2015}
}
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