3m32 › Citations

Structural insight into methyl-coenzyme M reductase chemistry using coenzyme B analogues .

Cedervall PE, Dey M, Pearson AR, Ragsdale SW, Wilmot CM
Biochemistry 49 7683-93 (2010)
Related entries: 3m1v, 3m2r, 3m2u, 3m2v, 3m30

Cited: 21 times
EuropePMC logo PMID: 20707311

Abstract

Methyl-coenzyme M reductase (MCR) catalyzes the final and rate-limiting step in methane biogenesis: the reduction of methyl-coenzyme M (methyl-SCoM) by coenzyme B (CoBSH) to methane and a heterodisulfide (CoBS-SCoM). Crystallographic studies show that the active site is deeply buried within the enzyme and contains a highly reduced nickel-tetrapyrrole, coenzyme F(430). Methyl-SCoM must enter the active site prior to CoBSH, as species derived from methyl-SCoM are always observed bound to the F(430) nickel in the deepest part of the 30 A long substrate channel that leads from the protein surface to the active site. The seven-carbon mercaptoalkanoyl chain of CoBSH binds within a 16 A predominantly hydrophobic part of the channel close to F(430), with the CoBSH thiolate lying closest to the nickel at a distance of 8.8 A. It has previously been suggested that binding of CoBSH initiates catalysis by inducing a conformational change that moves methyl-SCoM closer to the nickel promoting cleavage of the C-S bond of methyl-SCoM. In order to better understand the structural role of CoBSH early in the MCR mechanism, we have determined crystal structures of MCR in complex with four different CoBSH analogues: pentanoyl, hexanoyl, octanoyl, and nonanoyl derivatives of CoBSH (CoB(5)SH, CoB(6)SH, CoB(8)SH, and CoB(9)SH, respectively). The data presented here reveal that the shorter CoB(5)SH mercaptoalkanoyl chain overlays with that of CoBSH but terminates two units short of the CoBSH thiolate position. In contrast, the mercaptoalkanoyl chain of CoB(6)SH adopts a different conformation, such that its thiolate is coincident with the position of the CoBSH thiolate. This is consistent with the observation that CoB(6)SH is a slow substrate. A labile water in the substrate channel was found to be a sensitive indicator for the presence of CoBSH and HSCoM. The longer CoB(8)SH and CoB(9)SH analogues can be accommodated in the active site through exclusion of this water. These analogues react with Ni(III)-methyl, a proposed MCR catalytic intermediate of methanogenesis. The CoB(8)SH thiolate is 2.6 A closer to the nickel than that of CoBSH, but the additional carbon of CoB(9)SH only decreases the nickel thiolate distance a further 0.3 A. Although the analogues do not induce any structural changes in the substrate channel, the thiolates appear to preferentially bind at two distinct positions in the channel, one being the previously observed CoBSH thiolate position and the other being at a hydrophobic annulus of residues that lines the channel proximal to the nickel.

Articles - 3m32 mentioned but not cited (2)

  1. Structural insight into methyl-coenzyme M reductase chemistry using coenzyme B analogues . Cedervall PE, Dey M, Pearson AR, Ragsdale SW, Wilmot CM. Biochemistry 49 7683-7693 (2010)
  2. Early chordate origin of the vertebrate integrin αI domains. Chouhan BS, Käpylä J, Denessiouk K, Denesyuk A, Heino J, Johnson MS. PLoS ONE 9 e112064 (2014)


Reviews citing this publication (2)

  1. Fundamentals of methanogenic pathways that are key to the biomethanation of complex biomass. Ferry JG. Curr. Opin. Biotechnol. 22 351-357 (2011)
  2. Methyl (Alkyl)-Coenzyme M Reductases: Nickel F-430-Containing Enzymes Involved in Anaerobic Methane Formation and in Anaerobic Oxidation of Methane or of Short Chain Alkanes. Thauer RK. Biochemistry 58 5198-5220 (2019)

Articles citing this publication (17)

  1. Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome. Shi W, Moon CD, Leahy SC, Kang D, Froula J, Kittelmann S, Fan C, Deutsch S, Gagic D, Seedorf H, Kelly WJ, Atua R, Sang C, Soni P, Li D, Pinares-Patiño CS, McEwan JC, Janssen PH, Chen F, Visel A, Wang Z, Attwood GT, Rubin EM. Genome Res. 24 1517-1525 (2014)
  2. Conformational control of cofactors in nature - the influence of protein-induced macrocycle distortion on the biological function of tetrapyrroles. Senge MO, MacGowan SA, O'Brien JM. Chem. Commun. (Camb.) 51 17031-17063 (2015)
  3. Didehydroaspartate Modification in Methyl-Coenzyme M Reductase Catalyzing Methane Formation. Wagner T, Kahnt J, Ermler U, Shima S. Angew. Chem. Int. Ed. Engl. 55 10630-10633 (2016)
  4. Structural analysis of a Ni-methyl species in methyl-coenzyme M reductase from Methanothermobacter marburgensis. Cedervall PE, Dey M, Li X, Sarangi R, Hedman B, Ragsdale SW, Wilmot CM. J. Am. Chem. Soc. 133 5626-5628 (2011)
  5. Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions. Angle JC, Morin TH, Solden LM, Narrowe AB, Smith GJ, Borton MA, Rey-Sanchez C, Daly RA, Mirfenderesgi G, Hoyt DW, Riley WJ, Miller CS, Bohrer G, Wrighton KC. Nat Commun 8 1567 (2017)
  6. The reaction mechanism of methyl-coenzyme M reductase: how an enzyme enforces strict binding order. Wongnate T, Ragsdale SW. J. Biol. Chem. 290 9322-9334 (2015)
  7. In vivo activation of methyl-coenzyme M reductase by carbon monoxide. Zhou Y, Dorchak AE, Ragsdale SW. Front Microbiol 4 69 (2013)
  8. Gut Microbiota of Wild and Captive Alpine Musk Deer (Moschus chrysogaster). Sun Y, Sun Y, Shi Z, Liu Z, Zhao C, Lu T, Gao H, Zhu F, Chen R, Zhang J, Pan R, Li B, Teng L, Guo S. Front Microbiol 10 3156 (2019)
  9. Response of the Anaerobic Methanotroph "Candidatus Methanoperedens nitroreducens" to Oxygen Stress. Guerrero-Cruz S, Cremers G, van Alen TA, Op den Camp HJM, Jetten MSM, Rasigraf O, Vaksmaa A. Appl. Environ. Microbiol. 84 (2018)
  10. Functional capacities of microbial communities to carry out large scale geochemical processes are maintained during ex situ anaerobic incubation. Wilson RM, Zayed AA, Crossen KB, Woodcroft B, Tfaily MM, Emerson J, Raab N, Hodgkins SB, Verbeke B, Tyson G, Crill P, Saleska S, Chanton JP, Rich VI, IsoGenie Project Coordinators, IsoGenie Project Field Team. PLoS One 16 e0245857 (2021)
  11. Characterization of the protein fraction of the extracellular polymeric substances of three anaerobic granular sludges. Dubé CD, Guiot SR. AMB Express 9 23 (2019)
  12. Genome Analyses and Genome-Centered Metatranscriptomics of Methanothermobacter wolfeii Strain SIV6, Isolated from a Thermophilic Production-Scale Biogas Fermenter. Hassa J, Wibberg D, Maus I, Pühler A, Schlüter A. Microorganisms 8 (2019)
  13. Implication of O2 dynamics for both N2O and CH4 emissions from soil during biological soil disinfestation. Wang C, Ma X, Wang G, Li G, Zhu K. Sci Rep 11 6590 (2021)
  14. Sediment Disturbance Negatively Impacts Methanogen Abundance but Has Variable Effects on Total Methane Emissions. Rowe A, Urbanic M, Trutschel L, Shukle J, Druschel G, Booth M. Front Microbiol 13 796018 (2022)
  15. Structural Insights into the Methane-Generating Enzyme from a Methoxydotrophic Methanogen Reveal a Restrained Gallery of Post-Translational Modifications. Kurth JM, Müller MC, Welte CU, Wagner T. Microorganisms 9 837 (2021)
  16. The effect of 3-nitrooxypropanol, a potent methane inhibitor, on ruminal microbial gene expression profiles in dairy cows. Pitta DW, Indugu N, Melgar A, Hristov A, Challa K, Vecchiarelli B, Hennessy M, Narayan K, Duval S, Kindermann M, Walker N. Microbiome 10 146 (2022)
  17. XFEL serial crystallography reveals the room temperature structure of methyl-coenzyme M reductase. Ohmer CJ, Dasgupta M, Patwardhan A, Bogacz I, Kaminsky C, Doyle MD, Chen PY, Keable SM, Makita H, Simon PS, Massad R, Fransson T, Chatterjee R, Bhowmick A, Paley DW, Moriarty NW, Brewster AS, Gee LB, Alonso-Mori R, Moss F, Fuller FD, Batyuk A, Sauter NK, Bergmann U, Drennan CL, Yachandra VK, Yano J, Kern JF, Ragsdale SW. J Inorg Biochem 230 111768 (2022)


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