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Glycerol dehydrogenase: Structure, specificity, and mechanism of a family III polyol dehydrogenase

Glycerol dehydrogenase: Structure, specificity, and mechanism of a family III polyol dehydrogenase
Glycerol dehydrogenase: Structure, specificity, and mechanism of a family III polyol dehydrogenase
Background: Bacillus stearothermophilus glycerol dehydrogenase (GlyDH) (glycerol:NAD+ 2-oxidoreductase, EC 1.1.1.6) catalyzes the oxidation of glycerol to dihydroxyacetone (1,3-dihydroxypropanone) with concomitant reduction of NAD+ to NADH. Analysis of the sequence of this enzyme indicates that it is a member of the so-called iron-containing alcohol dehydrogenase family. Despite this sequence similarity, GlyDH shows a strict dependence on zinc for activity. On the basis of this, we propose to rename this group the family III metal-dependent polyol dehydrogenases. To date, no structural data have been reported for any enzyme in this group.
Results: The crystal structure of B. stearothermophilus glycerol dehydrogenase has been determined at 1.7 Å resolution to provide structural insights into the mechanistic features of this family. The enzyme has 370 amino acid residues, has a molecular mass of 39.5 kDa, and is a homooctamer in solution.
Conclusions: Analysis of the crystal structures of the free enzyme and of the binary complexes with NAD+ and glycerol show that the active site of GlyDH lies in the cleft between the enzyme's two domains, with the catalytic zinc ion playing a role in stabilizing an alkoxide intermediate. In addition, the specificity of this enzyme for a range of diols can be understood, as both hydroxyls of the glycerol form ligands to the enzyme-bound Zn2+ ion at the active site. The structure further reveals a previously unsuspected similarity to dehydroquinate synthase, an enzyme whose more complex chemistry shares a common chemical step with that catalyzed by glycerol dehydrogenase, providing a striking example of divergent evolution. Finally, the structure suggests that the NAD+ binding domain of GlyDH may be related to that of the classical Rossmann fold by switching the sequence order of the two mononucleotide binding folds that make up this domain.
crystal structure, metallo-enzyme, glycerol dehydrogenase, EC 1.1.1.6, glycerol oxidation, Bacillus stearothermophilus
0969-2126
789-802
Ruzheinikov, Sergey N.
3fdcb935-f0b4-48f8-aa57-dd779b963fcd
Burke, Jacky
3b45e665-0f11-4825-b807-0fb5ce1131e6
Sedelnikova, Sveta
f258f0df-abad-4e60-8beb-19bdbf296dd0
Baker, Patrick J.
1230622a-cc9b-41b9-94b9-1ca47be5aa9b
Taylor, Robert
2ef87af4-171a-42de-a37c-51b3b13bd73b
Bullough, Per A.
bdcbc26f-632d-41f2-b0a0-2a95a74973e6
Muir, Nicola M.
da9adda2-83de-44df-8213-62b0dfedf6c1
Gore, Michael G.
7bd6db4b-c5a2-4206-8666-b92208ba7979
Rice, David W.
a795d967-0041-4bd1-aa5a-38cb50cdfc9e
Ruzheinikov, Sergey N.
3fdcb935-f0b4-48f8-aa57-dd779b963fcd
Burke, Jacky
3b45e665-0f11-4825-b807-0fb5ce1131e6
Sedelnikova, Sveta
f258f0df-abad-4e60-8beb-19bdbf296dd0
Baker, Patrick J.
1230622a-cc9b-41b9-94b9-1ca47be5aa9b
Taylor, Robert
2ef87af4-171a-42de-a37c-51b3b13bd73b
Bullough, Per A.
bdcbc26f-632d-41f2-b0a0-2a95a74973e6
Muir, Nicola M.
da9adda2-83de-44df-8213-62b0dfedf6c1
Gore, Michael G.
7bd6db4b-c5a2-4206-8666-b92208ba7979
Rice, David W.
a795d967-0041-4bd1-aa5a-38cb50cdfc9e

Ruzheinikov, Sergey N., Burke, Jacky, Sedelnikova, Sveta, Baker, Patrick J., Taylor, Robert, Bullough, Per A., Muir, Nicola M., Gore, Michael G. and Rice, David W. (2001) Glycerol dehydrogenase: Structure, specificity, and mechanism of a family III polyol dehydrogenase. Structure, 9 (9), 789-802. (doi:10.1016/S0969-2126(01)00645-1).

Record type: Article

Abstract

Background: Bacillus stearothermophilus glycerol dehydrogenase (GlyDH) (glycerol:NAD+ 2-oxidoreductase, EC 1.1.1.6) catalyzes the oxidation of glycerol to dihydroxyacetone (1,3-dihydroxypropanone) with concomitant reduction of NAD+ to NADH. Analysis of the sequence of this enzyme indicates that it is a member of the so-called iron-containing alcohol dehydrogenase family. Despite this sequence similarity, GlyDH shows a strict dependence on zinc for activity. On the basis of this, we propose to rename this group the family III metal-dependent polyol dehydrogenases. To date, no structural data have been reported for any enzyme in this group.
Results: The crystal structure of B. stearothermophilus glycerol dehydrogenase has been determined at 1.7 Å resolution to provide structural insights into the mechanistic features of this family. The enzyme has 370 amino acid residues, has a molecular mass of 39.5 kDa, and is a homooctamer in solution.
Conclusions: Analysis of the crystal structures of the free enzyme and of the binary complexes with NAD+ and glycerol show that the active site of GlyDH lies in the cleft between the enzyme's two domains, with the catalytic zinc ion playing a role in stabilizing an alkoxide intermediate. In addition, the specificity of this enzyme for a range of diols can be understood, as both hydroxyls of the glycerol form ligands to the enzyme-bound Zn2+ ion at the active site. The structure further reveals a previously unsuspected similarity to dehydroquinate synthase, an enzyme whose more complex chemistry shares a common chemical step with that catalyzed by glycerol dehydrogenase, providing a striking example of divergent evolution. Finally, the structure suggests that the NAD+ binding domain of GlyDH may be related to that of the classical Rossmann fold by switching the sequence order of the two mononucleotide binding folds that make up this domain.

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Submitted date: 29 January 2001
Published date: September 2001
Keywords: crystal structure, metallo-enzyme, glycerol dehydrogenase, EC 1.1.1.6, glycerol oxidation, Bacillus stearothermophilus

Identifiers

Local EPrints ID: 25142
URI: http://eprints.soton.ac.uk/id/eprint/25142
ISSN: 0969-2126
PURE UUID: cf624fca-0110-4e4d-ad98-ccf0d53e0d8d

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Date deposited: 06 Apr 2006
Last modified: 15 Mar 2024 07:00

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Contributors

Author: Sergey N. Ruzheinikov
Author: Jacky Burke
Author: Sveta Sedelnikova
Author: Patrick J. Baker
Author: Robert Taylor
Author: Per A. Bullough
Author: Nicola M. Muir
Author: Michael G. Gore
Author: David W. Rice

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