Geometry of the soluble methane monooxygenase catalytic diiron center in two oxidation states

Amy C. Rosenzweig; Pär Nordlund; Patricia M. Takahara; Christin A. Frederick; Stephen J. Lippard

doi:10.1016/1074-5521(95)90222-8

Geometry of the soluble methane monooxygenase catalytic diiron center in two oxidation states

Amy C. Rosenzweig^*, Pär Nordlund, Patricia M. Takahara, Christin A. Frederick, Stephen J. Lippard

^*Corresponding author for this work

Molecular Biosciences

Research output: Contribution to journal › Article › peer-review

441 Scopus citations

Abstract

Background: The hydroxylase component of soluble methane monooxygenase (sMMO) contains a dinuclear iron center responsible for the oxidation of methane to methanol. As isolated, the center is in the oxidized, diiron(III) state. The 2.2 Å resolution X-ray structure of the oxidized hydroxylase, H_ox, from Methylococcus capsulatus (Bath) was previously determined at 4 °C. In this structure the two iron atoms are bridged by a glutamate, a hydroxide ion, and an acetate ion, and additionally coordinated to two His residues, three. Glu residues, and a water molecule. Results: The 1.7 Å resolution crystal structures of the sMMO hydroxylase from Methylococcus capsulatus (Bath) in both its oxidized diiron(III), H_ox, and dithionite-treated, reduced diiron(II), H_red, oxidation states were determined at -160 °C. The structure of the diiron center in H_ox differs from that previously reported at 2.2 Å resolution and 4 °C. Although the hydroxide bridge is retained, the bidentate, bridging ligand assigned as acetate is replaced by a weakly coordinating monoatomic water bridge. In the resulting four-membered Fe(OH)Fe(OH₂) ring, the Fe...Fe distance is shortened from 3.4 Å to 3.1 Å. In protomer A of H_red, the hydroxide bridge is displaced by an oxygen atom of Glu243, which undergoes a carboxylate shift from its terminal monodentate binding mode in H_ox to a mode in which the carboxylate is both monoatomic bridging and bidentate chelating. We therefore conclude that the center has been reduced to the diiron(II) oxidation state. Both iron atoms are coordinated to five ligands and weakly to a sixth water molecule in the resulting structure. The diiron center in protomer B of H_red has the same composition as those in H_ox. In both the oxidized and reduced structures, the diiron core is connected through hydrogen bonds involving exogenous species to Thr213 in the active site cavity. Conclusions: The diiron center in H_ox can change its exogenous ligand coordination and geometry, a property that could be important in the catalytic cycle of sMMO. In H_red, a carboxylate shift occurs, extruding hydroxide ion and opening coordination sites for reaction with O₂ to form the diiron(III) peroxo intermediate, H_peroxo. Residue Thr213 may function in catalysis.

Original language	English (US)
Pages (from-to)	409-418
Number of pages	10
Journal	Chemistry and Biology
Volume	2
Issue number	6
DOIs	https://doi.org/10.1016/1074-5521(95)90222-8
State	Published - Jun 1995

Funding

AcknowledgementxThis work was supported by grants from the National Institute of General Medical Sciences (GM32134 to S.J.L. and GM48388 to C.A.E and S.J.L.) and from the Claudia Adams Barr Foundation (C.A.F.). A.C.R. is the recipient of NIGMS postdoctoral fellowship GM15914. We thank B.E. Earp and D.A. Whittington for assistance with data collection, the staffs at SSRL and the Photon Factory for support, and PA. Karplus for helpful discussions.

Keywords

Methylococcus capsulatus (Bath)
X-ray crystallography
carboxylate shift
dinuclear iron center
methane oxidation

ASJC Scopus subject areas

Biochemistry
Molecular Medicine
Molecular Biology
Pharmacology
Drug Discovery
Clinical Biochemistry

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10.1016/1074-5521(95)90222-8

Cite this

@article{2b59e97aa20940659349dd9923d99e5a,

title = "Geometry of the soluble methane monooxygenase catalytic diiron center in two oxidation states",

abstract = "Background: The hydroxylase component of soluble methane monooxygenase (sMMO) contains a dinuclear iron center responsible for the oxidation of methane to methanol. As isolated, the center is in the oxidized, diiron(III) state. The 2.2 {\AA} resolution X-ray structure of the oxidized hydroxylase, Hox, from Methylococcus capsulatus (Bath) was previously determined at 4 °C. In this structure the two iron atoms are bridged by a glutamate, a hydroxide ion, and an acetate ion, and additionally coordinated to two His residues, three. Glu residues, and a water molecule. Results: The 1.7 {\AA} resolution crystal structures of the sMMO hydroxylase from Methylococcus capsulatus (Bath) in both its oxidized diiron(III), Hox, and dithionite-treated, reduced diiron(II), Hred, oxidation states were determined at -160 °C. The structure of the diiron center in Hox differs from that previously reported at 2.2 {\AA} resolution and 4 °C. Although the hydroxide bridge is retained, the bidentate, bridging ligand assigned as acetate is replaced by a weakly coordinating monoatomic water bridge. In the resulting four-membered Fe(OH)Fe(OH2) ring, the Fe...Fe distance is shortened from 3.4 {\AA} to 3.1 {\AA}. In protomer A of Hred, the hydroxide bridge is displaced by an oxygen atom of Glu243, which undergoes a carboxylate shift from its terminal monodentate binding mode in Hox to a mode in which the carboxylate is both monoatomic bridging and bidentate chelating. We therefore conclude that the center has been reduced to the diiron(II) oxidation state. Both iron atoms are coordinated to five ligands and weakly to a sixth water molecule in the resulting structure. The diiron center in protomer B of Hred has the same composition as those in Hox. In both the oxidized and reduced structures, the diiron core is connected through hydrogen bonds involving exogenous species to Thr213 in the active site cavity. Conclusions: The diiron center in Hox can change its exogenous ligand coordination and geometry, a property that could be important in the catalytic cycle of sMMO. In Hred, a carboxylate shift occurs, extruding hydroxide ion and opening coordination sites for reaction with O2 to form the diiron(III) peroxo intermediate, Hperoxo. Residue Thr213 may function in catalysis.",

keywords = "Methylococcus capsulatus (Bath), X-ray crystallography, carboxylate shift, dinuclear iron center, methane oxidation",

author = "Rosenzweig, {Amy C.} and P{\"a}r Nordlund and Takahara, {Patricia M.} and Frederick, {Christin A.} and Lippard, {Stephen J.}",

note = "Funding Information: AcknowledgementxThis work was supported by grants from the National Institute of General Medical Sciences (GM32134 to S.J.L. and GM48388 to C.A.E and S.J.L.) and from the Claudia Adams Barr Foundation (C.A.F.). A.C.R. is the recipient of NIGMS postdoctoral fellowship GM15914. We thank B.E. Earp and D.A. Whittington for assistance with data collection, the staffs at SSRL and the Photon Factory for support, and PA. Karplus for helpful discussions.",

year = "1995",

month = jun,

doi = "10.1016/1074-5521(95)90222-8",

language = "English (US)",

volume = "2",

pages = "409--418",

journal = "Chemistry and Biology",

issn = "1074-5521",

publisher = "Elsevier Inc.",

number = "6",

}

TY - JOUR

T1 - Geometry of the soluble methane monooxygenase catalytic diiron center in two oxidation states

AU - Rosenzweig, Amy C.

AU - Nordlund, Pär

AU - Takahara, Patricia M.

AU - Frederick, Christin A.

AU - Lippard, Stephen J.

N1 - Funding Information: AcknowledgementxThis work was supported by grants from the National Institute of General Medical Sciences (GM32134 to S.J.L. and GM48388 to C.A.E and S.J.L.) and from the Claudia Adams Barr Foundation (C.A.F.). A.C.R. is the recipient of NIGMS postdoctoral fellowship GM15914. We thank B.E. Earp and D.A. Whittington for assistance with data collection, the staffs at SSRL and the Photon Factory for support, and PA. Karplus for helpful discussions.

PY - 1995/6

Y1 - 1995/6

N2 - Background: The hydroxylase component of soluble methane monooxygenase (sMMO) contains a dinuclear iron center responsible for the oxidation of methane to methanol. As isolated, the center is in the oxidized, diiron(III) state. The 2.2 Å resolution X-ray structure of the oxidized hydroxylase, Hox, from Methylococcus capsulatus (Bath) was previously determined at 4 °C. In this structure the two iron atoms are bridged by a glutamate, a hydroxide ion, and an acetate ion, and additionally coordinated to two His residues, three. Glu residues, and a water molecule. Results: The 1.7 Å resolution crystal structures of the sMMO hydroxylase from Methylococcus capsulatus (Bath) in both its oxidized diiron(III), Hox, and dithionite-treated, reduced diiron(II), Hred, oxidation states were determined at -160 °C. The structure of the diiron center in Hox differs from that previously reported at 2.2 Å resolution and 4 °C. Although the hydroxide bridge is retained, the bidentate, bridging ligand assigned as acetate is replaced by a weakly coordinating monoatomic water bridge. In the resulting four-membered Fe(OH)Fe(OH2) ring, the Fe...Fe distance is shortened from 3.4 Å to 3.1 Å. In protomer A of Hred, the hydroxide bridge is displaced by an oxygen atom of Glu243, which undergoes a carboxylate shift from its terminal monodentate binding mode in Hox to a mode in which the carboxylate is both monoatomic bridging and bidentate chelating. We therefore conclude that the center has been reduced to the diiron(II) oxidation state. Both iron atoms are coordinated to five ligands and weakly to a sixth water molecule in the resulting structure. The diiron center in protomer B of Hred has the same composition as those in Hox. In both the oxidized and reduced structures, the diiron core is connected through hydrogen bonds involving exogenous species to Thr213 in the active site cavity. Conclusions: The diiron center in Hox can change its exogenous ligand coordination and geometry, a property that could be important in the catalytic cycle of sMMO. In Hred, a carboxylate shift occurs, extruding hydroxide ion and opening coordination sites for reaction with O2 to form the diiron(III) peroxo intermediate, Hperoxo. Residue Thr213 may function in catalysis.

AB - Background: The hydroxylase component of soluble methane monooxygenase (sMMO) contains a dinuclear iron center responsible for the oxidation of methane to methanol. As isolated, the center is in the oxidized, diiron(III) state. The 2.2 Å resolution X-ray structure of the oxidized hydroxylase, Hox, from Methylococcus capsulatus (Bath) was previously determined at 4 °C. In this structure the two iron atoms are bridged by a glutamate, a hydroxide ion, and an acetate ion, and additionally coordinated to two His residues, three. Glu residues, and a water molecule. Results: The 1.7 Å resolution crystal structures of the sMMO hydroxylase from Methylococcus capsulatus (Bath) in both its oxidized diiron(III), Hox, and dithionite-treated, reduced diiron(II), Hred, oxidation states were determined at -160 °C. The structure of the diiron center in Hox differs from that previously reported at 2.2 Å resolution and 4 °C. Although the hydroxide bridge is retained, the bidentate, bridging ligand assigned as acetate is replaced by a weakly coordinating monoatomic water bridge. In the resulting four-membered Fe(OH)Fe(OH2) ring, the Fe...Fe distance is shortened from 3.4 Å to 3.1 Å. In protomer A of Hred, the hydroxide bridge is displaced by an oxygen atom of Glu243, which undergoes a carboxylate shift from its terminal monodentate binding mode in Hox to a mode in which the carboxylate is both monoatomic bridging and bidentate chelating. We therefore conclude that the center has been reduced to the diiron(II) oxidation state. Both iron atoms are coordinated to five ligands and weakly to a sixth water molecule in the resulting structure. The diiron center in protomer B of Hred has the same composition as those in Hox. In both the oxidized and reduced structures, the diiron core is connected through hydrogen bonds involving exogenous species to Thr213 in the active site cavity. Conclusions: The diiron center in Hox can change its exogenous ligand coordination and geometry, a property that could be important in the catalytic cycle of sMMO. In Hred, a carboxylate shift occurs, extruding hydroxide ion and opening coordination sites for reaction with O2 to form the diiron(III) peroxo intermediate, Hperoxo. Residue Thr213 may function in catalysis.

KW - Methylococcus capsulatus (Bath)

KW - X-ray crystallography

KW - carboxylate shift

KW - dinuclear iron center

KW - methane oxidation

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U2 - 10.1016/1074-5521(95)90222-8

DO - 10.1016/1074-5521(95)90222-8

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C2 - 9383443

AN - SCOPUS:58149367966

SN - 1074-5521

VL - 2

SP - 409

EP - 418

JO - Chemistry and Biology

JF - Chemistry and Biology

IS - 6

ER -

Geometry of the soluble methane monooxygenase catalytic diiron center in two oxidation states

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