The 'prismane' protein resolved: X-ray structure at 1.7 Å and multiple spectroscopy of two novel 4Fe clusters

Alexander F. Arendsen; Jonathan Hadden; Graeme Card; Alan S. McAlpine; Susan Bailey; Vjacheslav Zaitsev; Elizabeth H.M. Duke; Peter F. Lindley; Monika Kröckel; Alfred X. Trautwein; Martinus C. Feiters; John M. Charnock; C. David Garner; Sophie J. Marritt; Andrew J. Thomson; Ingeborg M. Kooter; Michael K. Johnson; Willy A.M. Van Den Berg; Walter M.A.M. Van Dongen; Wilfred R. Hagen

doi:10.1007/s007750050210

The 'prismane' protein resolved: X-ray structure at 1.7 Å and multiple spectroscopy of two novel 4Fe clusters

Alexander F. Arendsen, Jonathan Hadden, Graeme Card, Alan S. McAlpine, Susan Bailey, Vjacheslav Zaitsev, Elizabeth H.M. Duke, Peter F. Lindley^*, Monika Kröckel, Alfred X. Trautwein, Martinus C. Feiters, John M. Charnock, C. David Garner, Sophie J. Marritt, Andrew J. Thomson, Ingeborg M. Kooter, Michael K. Johnson, Willy A.M. Van Den Berg, Walter M.A.M. Van Dongen, Wilfred R. Hagen

^*Korrespondierende/r Autor/-in für diese Arbeit

Institut für Physik

77 Zitate (Scopus)

Abstract

The three-dimensional structure of the native 'putative prismane' protein from Desulfovibrio vulgaris (Hildenborough) has been solved by X-ray crystallography to a resolution of 1.72 Å. The molecule does not contain a [6Fe-6S] prismane cluster, but rather two 4Fe clusters some 12 Å apart and situated close to the interfaces formed by the three domains of the protein. Cluster 1 is a conventional [4Fe-4S] cubane bound, however, near the N- terminus by an unusual, sequential arrangement of four cysteine residues (Cys 3, 6, 15, 21). Cluster 2 is a novel 4Fe structure with two μ₂-sulfido bridges, two μ₂-oxo bridges, and a partially occupied, unidentified μ₂ bridge X. The protein ligands of cluster 2 are widely scattered through the second half of the sequence and include three cysteine residues (Cys 312, 434, 459), one persulfido-cysteine (Cys 406), two glutamates (Glu 268, 494), and one histidine (His 244). With this unusual mixture of bridging and external type of ligands, cluster 2 is named the 'hybrid' cluster, and its asymmetric, open structure suggests that it could be the site of a catalytic activity. X-ray absorption spectroscopy at the Fe K-edge is readily interpretable in terms of the crystallographic model when allowance is made for volume contraction at 10K; no Fe··Fe distances beyond 3.1 Å could be identified. EPR, Mossbauer and MCD spectroscopy have been used to define the oxidation states and the magnetism of the clusters in relation to the crystallographic structure. Reduced cluster 1 is a [4Fe-4S]¹⁺ cubane with S = 3/2; it is the first biological example of a 'spin-admixed' iron-sulfur cluster. The hybrid cluster 2 has four oxidation states from (formally) all Fe(III) to three Fe(II) plus one Fe(III). The four iron ions are exchange coupled resulting in the system spins S = 0, 9/2, 0 (and 4), 1/2, respectively for the four redox states. Resonance Raman spectroscopy suggests that the bridging ligand X which could not be identified unambiguously in the crystal structure is a solvent-exchangeable oxygen.

Originalsprache	Englisch
Zeitschrift	Journal of Biological Inorganic Chemistry
Jahrgang	3
Ausgabenummer	1
Seiten (von - bis)	81-95
Seitenumfang	15
ISSN	0949-8257
DOIs	https://doi.org/10.1007/s007750050210
Publikationsstatus	Veröffentlicht - 01.02.1998

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Acknowledgements We are grateful to C. Veeger for his continuous support to this project over many years. Y.B.M. Bulsink has assisted in the protein purification. We thank J.N. Butt, A.J. Pier-ik, M. Oversluizen and J.F.W. Mosselmans for their help in the EXAFS measurements. Support is acknowledged from the following national institutions: The UK inter-research council Biology Program Joint Steering Committee (MRC, BBSRC and EPSRC) which supports the structural biology program at the SRS, Daresbury Laboratory; the Netherlands Foundation for Chemical Research (SON) with financial aid from the Netherlands Organization for Scientific Research (NWO); the German Federal Ministery of Education, Science, Research and Technology (BMBF) through grant O3R624BO; the US National Institutes of Health (GM51962) and the US National Science Foundation (MCB9419019). This work was also supported by the European Commission through the Human Capital and Mobility programme, specifically the Access to Large Installations Project, the Network programme, MASIMO, Metalloproteins Activating Small Inorganic Molecules (ERBCHRXCT920072), an Individual Post-Doc Fellowship to SJM (ERBCHBICT941322), and the Network programme Structure-function relationships of iron-sulfur proteins (ERBCHRXCT940626).

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Arendsen, A. F., Hadden, J., Card, G., McAlpine, A. S., Bailey, S., Zaitsev, V., Duke, E. H. M., Lindley, P. F., Kröckel, M., Trautwein, A. X., Feiters, M. C., Charnock, J. M., Garner, C. D., Marritt, S. J., Thomson, A. J., Kooter, I. M., Johnson, M. K., Van Den Berg, W. A. M., Van Dongen, W. M. A. M., & Hagen, W. R. (1998). The 'prismane' protein resolved: X-ray structure at 1.7 Å and multiple spectroscopy of two novel 4Fe clusters. Journal of Biological Inorganic Chemistry, 3(1), 81-95. https://doi.org/10.1007/s007750050210

@article{b4863af050d34e3a9745bd34217e3d3e,

title = "The 'prismane' protein resolved: X-ray structure at 1.7 {\AA} and multiple spectroscopy of two novel 4Fe clusters",

abstract = "The three-dimensional structure of the native 'putative prismane' protein from Desulfovibrio vulgaris (Hildenborough) has been solved by X-ray crystallography to a resolution of 1.72 {\AA}. The molecule does not contain a [6Fe-6S] prismane cluster, but rather two 4Fe clusters some 12 {\AA} apart and situated close to the interfaces formed by the three domains of the protein. Cluster 1 is a conventional [4Fe-4S] cubane bound, however, near the N- terminus by an unusual, sequential arrangement of four cysteine residues (Cys 3, 6, 15, 21). Cluster 2 is a novel 4Fe structure with two μ2-sulfido bridges, two μ2-oxo bridges, and a partially occupied, unidentified μ2 bridge X. The protein ligands of cluster 2 are widely scattered through the second half of the sequence and include three cysteine residues (Cys 312, 434, 459), one persulfido-cysteine (Cys 406), two glutamates (Glu 268, 494), and one histidine (His 244). With this unusual mixture of bridging and external type of ligands, cluster 2 is named the 'hybrid' cluster, and its asymmetric, open structure suggests that it could be the site of a catalytic activity. X-ray absorption spectroscopy at the Fe K-edge is readily interpretable in terms of the crystallographic model when allowance is made for volume contraction at 10K; no Fe··Fe distances beyond 3.1 {\AA} could be identified. EPR, Mossbauer and MCD spectroscopy have been used to define the oxidation states and the magnetism of the clusters in relation to the crystallographic structure. Reduced cluster 1 is a [4Fe-4S]1+ cubane with S = 3/2; it is the first biological example of a 'spin-admixed' iron-sulfur cluster. The hybrid cluster 2 has four oxidation states from (formally) all Fe(III) to three Fe(II) plus one Fe(III). The four iron ions are exchange coupled resulting in the system spins S = 0, 9/2, 0 (and 4), 1/2, respectively for the four redox states. Resonance Raman spectroscopy suggests that the bridging ligand X which could not be identified unambiguously in the crystal structure is a solvent-exchangeable oxygen.",

author = "Arendsen, \{Alexander F.\} and Jonathan Hadden and Graeme Card and McAlpine, \{Alan S.\} and Susan Bailey and Vjacheslav Zaitsev and Duke, \{Elizabeth H.M.\} and Lindley, \{Peter F.\} and Monika Kr{\"o}ckel and Trautwein, \{Alfred X.\} and Feiters, \{Martinus C.\} and Charnock, \{John M.\} and Garner, \{C. David\} and Marritt, \{Sophie J.\} and Thomson, \{Andrew J.\} and Kooter, \{Ingeborg M.\} and Johnson, \{Michael K.\} and \{Van Den Berg\}, \{Willy A.M.\} and \{Van Dongen\}, \{Walter M.A.M.\} and Hagen, \{Wilfred R.\}",

year = "1998",

month = feb,

day = "1",

doi = "10.1007/s007750050210",

language = "English",

volume = "3",

pages = "81--95",

journal = "Journal of Biological Inorganic Chemistry",

issn = "0949-8257",

publisher = "Springer Science and Business Media Deutschland GmbH",

number = "1",

}

Arendsen, AF, Hadden, J, Card, G, McAlpine, AS, Bailey, S, Zaitsev, V, Duke, EHM, Lindley, PF, Kröckel, M, Trautwein, AX, Feiters, MC, Charnock, JM, Garner, CD, Marritt, SJ, Thomson, AJ, Kooter, IM, Johnson, MK, Van Den Berg, WAM, Van Dongen, WMAM & Hagen, WR 1998, 'The 'prismane' protein resolved: X-ray structure at 1.7 Å and multiple spectroscopy of two novel 4Fe clusters', Journal of Biological Inorganic Chemistry, Jg. 3, Nr. 1, S. 81-95. https://doi.org/10.1007/s007750050210

TY - JOUR

T1 - The 'prismane' protein resolved: X-ray structure at 1.7 Å and multiple spectroscopy of two novel 4Fe clusters

AU - Arendsen, Alexander F.

AU - Hadden, Jonathan

AU - Card, Graeme

AU - McAlpine, Alan S.

AU - Bailey, Susan

AU - Zaitsev, Vjacheslav

AU - Duke, Elizabeth H.M.

AU - Lindley, Peter F.

AU - Kröckel, Monika

AU - Trautwein, Alfred X.

AU - Feiters, Martinus C.

AU - Charnock, John M.

AU - Garner, C. David

AU - Marritt, Sophie J.

AU - Thomson, Andrew J.

AU - Kooter, Ingeborg M.

AU - Johnson, Michael K.

AU - Van Den Berg, Willy A.M.

AU - Van Dongen, Walter M.A.M.

AU - Hagen, Wilfred R.

PY - 1998/2/1

Y1 - 1998/2/1

N2 - The three-dimensional structure of the native 'putative prismane' protein from Desulfovibrio vulgaris (Hildenborough) has been solved by X-ray crystallography to a resolution of 1.72 Å. The molecule does not contain a [6Fe-6S] prismane cluster, but rather two 4Fe clusters some 12 Å apart and situated close to the interfaces formed by the three domains of the protein. Cluster 1 is a conventional [4Fe-4S] cubane bound, however, near the N- terminus by an unusual, sequential arrangement of four cysteine residues (Cys 3, 6, 15, 21). Cluster 2 is a novel 4Fe structure with two μ2-sulfido bridges, two μ2-oxo bridges, and a partially occupied, unidentified μ2 bridge X. The protein ligands of cluster 2 are widely scattered through the second half of the sequence and include three cysteine residues (Cys 312, 434, 459), one persulfido-cysteine (Cys 406), two glutamates (Glu 268, 494), and one histidine (His 244). With this unusual mixture of bridging and external type of ligands, cluster 2 is named the 'hybrid' cluster, and its asymmetric, open structure suggests that it could be the site of a catalytic activity. X-ray absorption spectroscopy at the Fe K-edge is readily interpretable in terms of the crystallographic model when allowance is made for volume contraction at 10K; no Fe··Fe distances beyond 3.1 Å could be identified. EPR, Mossbauer and MCD spectroscopy have been used to define the oxidation states and the magnetism of the clusters in relation to the crystallographic structure. Reduced cluster 1 is a [4Fe-4S]1+ cubane with S = 3/2; it is the first biological example of a 'spin-admixed' iron-sulfur cluster. The hybrid cluster 2 has four oxidation states from (formally) all Fe(III) to three Fe(II) plus one Fe(III). The four iron ions are exchange coupled resulting in the system spins S = 0, 9/2, 0 (and 4), 1/2, respectively for the four redox states. Resonance Raman spectroscopy suggests that the bridging ligand X which could not be identified unambiguously in the crystal structure is a solvent-exchangeable oxygen.

AB - The three-dimensional structure of the native 'putative prismane' protein from Desulfovibrio vulgaris (Hildenborough) has been solved by X-ray crystallography to a resolution of 1.72 Å. The molecule does not contain a [6Fe-6S] prismane cluster, but rather two 4Fe clusters some 12 Å apart and situated close to the interfaces formed by the three domains of the protein. Cluster 1 is a conventional [4Fe-4S] cubane bound, however, near the N- terminus by an unusual, sequential arrangement of four cysteine residues (Cys 3, 6, 15, 21). Cluster 2 is a novel 4Fe structure with two μ2-sulfido bridges, two μ2-oxo bridges, and a partially occupied, unidentified μ2 bridge X. The protein ligands of cluster 2 are widely scattered through the second half of the sequence and include three cysteine residues (Cys 312, 434, 459), one persulfido-cysteine (Cys 406), two glutamates (Glu 268, 494), and one histidine (His 244). With this unusual mixture of bridging and external type of ligands, cluster 2 is named the 'hybrid' cluster, and its asymmetric, open structure suggests that it could be the site of a catalytic activity. X-ray absorption spectroscopy at the Fe K-edge is readily interpretable in terms of the crystallographic model when allowance is made for volume contraction at 10K; no Fe··Fe distances beyond 3.1 Å could be identified. EPR, Mossbauer and MCD spectroscopy have been used to define the oxidation states and the magnetism of the clusters in relation to the crystallographic structure. Reduced cluster 1 is a [4Fe-4S]1+ cubane with S = 3/2; it is the first biological example of a 'spin-admixed' iron-sulfur cluster. The hybrid cluster 2 has four oxidation states from (formally) all Fe(III) to three Fe(II) plus one Fe(III). The four iron ions are exchange coupled resulting in the system spins S = 0, 9/2, 0 (and 4), 1/2, respectively for the four redox states. Resonance Raman spectroscopy suggests that the bridging ligand X which could not be identified unambiguously in the crystal structure is a solvent-exchangeable oxygen.

UR - https://www.scopus.com/pages/publications/12144286845

U2 - 10.1007/s007750050210

DO - 10.1007/s007750050210

M3 - Journal articles

AN - SCOPUS:12144286845

SN - 0949-8257

VL - 3

SP - 81

EP - 95

JO - Journal of Biological Inorganic Chemistry

JF - Journal of Biological Inorganic Chemistry

IS - 1

ER -

The 'prismane' protein resolved: X-ray structure at 1.7 Å and multiple spectroscopy of two novel 4Fe clusters

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