Crystal structure of manganese catalase from Lactobacillus plantarum

V. V. Barynin, M. M. Whittaker, S. V. Antonyuk, V. S. Lamzin, P. M. Harrison, P. J. Artymiuk, James Whittaker

Research output: Contribution to journalArticle

246 Citations (Scopus)

Abstract

Background: Catalases are important antioxidant metalloenzymes that catalyze disproportionation of hydrogen peroxide, forming dioxygen and water. Two families of catalases are known, one having a heme cofactor, and the other, a structurally distinct family containing nonheme manganese. We have solved the structure of the mesophilic manganese catalase from Lactobacillus plantarum and its azide-inhibited complex. Results: The crystal structure of the native enzyme has been solved at 1.8 Å resolution by molecular replacement, and the azide complex of the native protein has been solved at 1.4 Å resolution. The hexameric structure of the holoenzyme is stabilized by extensive intersubunit contacts, including a β zipper and a structural calcium ion crosslinking neighboring subunits. Each subunit contains a dimanganese active site, accessed by a single substrate channel lined by charged residues. The manganese ions are linked by a μ1,3-bridging glutamate carboxylate and two μ-bridging solvent oxygens that electronically couple the metal centers. The active site region includes two residues (Arg147 and Glu178) that appear to be unique to the Lactobacillus plantarum catalase. Conclusions: A comparison of L. plantarum and T. thermophilus catalase structures reveals the existence of two distinct structural classes, differing in monomer design and the organization of their active sites, within the manganese catalase family. These differences have important implications for catalysis and may reflect distinct biological functions for the two enzymes, with the L. plantarum enzyme serving as a catalase, while the T. thermophilus enzyme may function as a catalase/peroxidase.

Original languageEnglish (US)
Pages (from-to)725-738
Number of pages14
JournalStructure
Volume9
Issue number8
DOIs
StatePublished - 2001

Fingerprint

Lactobacillus plantarum
Catalase
Catalytic Domain
Azides
Enzymes
Manganese
Ions
Oxygen
Holoenzymes
Catalysis
Heme
Hydrogen Peroxide
Peroxidase
Glutamic Acid
Antioxidants
Metals
Calcium
Water

Keywords

  • Antioxidant
  • Catalase
  • Dimanganese
  • Metalloenzyme
  • Nonheme
  • Structure

ASJC Scopus subject areas

  • Molecular Biology
  • Structural Biology

Cite this

Barynin, V. V., Whittaker, M. M., Antonyuk, S. V., Lamzin, V. S., Harrison, P. M., Artymiuk, P. J., & Whittaker, J. (2001). Crystal structure of manganese catalase from Lactobacillus plantarum. Structure, 9(8), 725-738. https://doi.org/10.1016/S0969-2126(01)00628-1

Crystal structure of manganese catalase from Lactobacillus plantarum. / Barynin, V. V.; Whittaker, M. M.; Antonyuk, S. V.; Lamzin, V. S.; Harrison, P. M.; Artymiuk, P. J.; Whittaker, James.

In: Structure, Vol. 9, No. 8, 2001, p. 725-738.

Research output: Contribution to journalArticle

Barynin, VV, Whittaker, MM, Antonyuk, SV, Lamzin, VS, Harrison, PM, Artymiuk, PJ & Whittaker, J 2001, 'Crystal structure of manganese catalase from Lactobacillus plantarum', Structure, vol. 9, no. 8, pp. 725-738. https://doi.org/10.1016/S0969-2126(01)00628-1
Barynin VV, Whittaker MM, Antonyuk SV, Lamzin VS, Harrison PM, Artymiuk PJ et al. Crystal structure of manganese catalase from Lactobacillus plantarum. Structure. 2001;9(8):725-738. https://doi.org/10.1016/S0969-2126(01)00628-1
Barynin, V. V. ; Whittaker, M. M. ; Antonyuk, S. V. ; Lamzin, V. S. ; Harrison, P. M. ; Artymiuk, P. J. ; Whittaker, James. / Crystal structure of manganese catalase from Lactobacillus plantarum. In: Structure. 2001 ; Vol. 9, No. 8. pp. 725-738.
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abstract = "Background: Catalases are important antioxidant metalloenzymes that catalyze disproportionation of hydrogen peroxide, forming dioxygen and water. Two families of catalases are known, one having a heme cofactor, and the other, a structurally distinct family containing nonheme manganese. We have solved the structure of the mesophilic manganese catalase from Lactobacillus plantarum and its azide-inhibited complex. Results: The crystal structure of the native enzyme has been solved at 1.8 {\AA} resolution by molecular replacement, and the azide complex of the native protein has been solved at 1.4 {\AA} resolution. The hexameric structure of the holoenzyme is stabilized by extensive intersubunit contacts, including a β zipper and a structural calcium ion crosslinking neighboring subunits. Each subunit contains a dimanganese active site, accessed by a single substrate channel lined by charged residues. The manganese ions are linked by a μ1,3-bridging glutamate carboxylate and two μ-bridging solvent oxygens that electronically couple the metal centers. The active site region includes two residues (Arg147 and Glu178) that appear to be unique to the Lactobacillus plantarum catalase. Conclusions: A comparison of L. plantarum and T. thermophilus catalase structures reveals the existence of two distinct structural classes, differing in monomer design and the organization of their active sites, within the manganese catalase family. These differences have important implications for catalysis and may reflect distinct biological functions for the two enzymes, with the L. plantarum enzyme serving as a catalase, while the T. thermophilus enzyme may function as a catalase/peroxidase.",
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AU - Whittaker, M. M.

AU - Antonyuk, S. V.

AU - Lamzin, V. S.

AU - Harrison, P. M.

AU - Artymiuk, P. J.

AU - Whittaker, James

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N2 - Background: Catalases are important antioxidant metalloenzymes that catalyze disproportionation of hydrogen peroxide, forming dioxygen and water. Two families of catalases are known, one having a heme cofactor, and the other, a structurally distinct family containing nonheme manganese. We have solved the structure of the mesophilic manganese catalase from Lactobacillus plantarum and its azide-inhibited complex. Results: The crystal structure of the native enzyme has been solved at 1.8 Å resolution by molecular replacement, and the azide complex of the native protein has been solved at 1.4 Å resolution. The hexameric structure of the holoenzyme is stabilized by extensive intersubunit contacts, including a β zipper and a structural calcium ion crosslinking neighboring subunits. Each subunit contains a dimanganese active site, accessed by a single substrate channel lined by charged residues. The manganese ions are linked by a μ1,3-bridging glutamate carboxylate and two μ-bridging solvent oxygens that electronically couple the metal centers. The active site region includes two residues (Arg147 and Glu178) that appear to be unique to the Lactobacillus plantarum catalase. Conclusions: A comparison of L. plantarum and T. thermophilus catalase structures reveals the existence of two distinct structural classes, differing in monomer design and the organization of their active sites, within the manganese catalase family. These differences have important implications for catalysis and may reflect distinct biological functions for the two enzymes, with the L. plantarum enzyme serving as a catalase, while the T. thermophilus enzyme may function as a catalase/peroxidase.

AB - Background: Catalases are important antioxidant metalloenzymes that catalyze disproportionation of hydrogen peroxide, forming dioxygen and water. Two families of catalases are known, one having a heme cofactor, and the other, a structurally distinct family containing nonheme manganese. We have solved the structure of the mesophilic manganese catalase from Lactobacillus plantarum and its azide-inhibited complex. Results: The crystal structure of the native enzyme has been solved at 1.8 Å resolution by molecular replacement, and the azide complex of the native protein has been solved at 1.4 Å resolution. The hexameric structure of the holoenzyme is stabilized by extensive intersubunit contacts, including a β zipper and a structural calcium ion crosslinking neighboring subunits. Each subunit contains a dimanganese active site, accessed by a single substrate channel lined by charged residues. The manganese ions are linked by a μ1,3-bridging glutamate carboxylate and two μ-bridging solvent oxygens that electronically couple the metal centers. The active site region includes two residues (Arg147 and Glu178) that appear to be unique to the Lactobacillus plantarum catalase. Conclusions: A comparison of L. plantarum and T. thermophilus catalase structures reveals the existence of two distinct structural classes, differing in monomer design and the organization of their active sites, within the manganese catalase family. These differences have important implications for catalysis and may reflect distinct biological functions for the two enzymes, with the L. plantarum enzyme serving as a catalase, while the T. thermophilus enzyme may function as a catalase/peroxidase.

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KW - Metalloenzyme

KW - Nonheme

KW - Structure

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