Structural differences of oxidized iron-sulfur and nickel-iron cofactors in O2-tolerant and O2-sensitive hydrogenases studied by X-ray absorption spectroscopy

Kajsa G.V. Sigfridsson, Nils Leidel, Oliver Sanganas, Petko Chernev, Oliver Lenz, Ki Suk Yoon, Hirofumi Nishihara, Alison Parkin, Fraser A. Armstrong, Sébastien Dementin, Marc Rousset, Antonio L. De Lacey, Michael Haumann

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

The class of [NiFe]-hydrogenases comprises oxygen-sensitive periplasmic (PH) and oxygen-tolerant membrane-bound (MBH) enzymes. For three PHs and four MBHs from six bacterial species, structural features of the nickel-iron active site of hydrogen turnover and of the iron-sulfur clusters functioning in electron transfer were determined using X-ray absorption spectroscopy (XAS). Fe-XAS indicated surplus oxidized iron and a lower number of ∼ 2.7 Å Fe-Fe distances plus additional shorter and longer distances in the oxidized MBHs compared to the oxidized PHs. This supported a double-oxidized and modified proximal FeS cluster in all MBHs with an apparent trimer-plus-monomer arrangement of its four iron atoms, in agreement with crystal data showing a [4Fe3S] cluster instead of a [4Fe4S] cubane as in the PHs. Ni-XAS indicated coordination of the nickel by the thiol group sulfurs of four conserved cysteines and at least one iron-oxygen bond in both MBH and PH proteins. Structural differences of the oxidized inactive [NiFe] cofactor of MBHs in the Ni-B state compared to PHs in the Ni-A state included a ∼ 0.05 Å longer Ni-O bond, a two times larger spread of the Ni-S bond lengths, and a ∼ 0.1 Å shorter Ni-Fe distance. The modified proximal [4Fe3S] cluster, weaker binding of the Ni-Fe bridging oxygen species, and an altered localization of reduced oxygen species at the active site may each contribute to O2 tolerance.

Original languageEnglish
Pages (from-to)162-170
Number of pages9
JournalBiochimica et Biophysica Acta - Bioenergetics
Volume1847
Issue number2
DOIs
Publication statusPublished - Jan 1 2015

Fingerprint

X-Ray Absorption Spectroscopy
Hydrogenase
X ray absorption spectroscopy
Nickel
Sulfur
Iron
Oxygen
Catalytic Domain
Bond length
Sulfhydryl Compounds
Cysteine
Hydrogen
Monomers
Electrons
Membranes
Atoms
Crystals
Enzymes
Proteins

All Science Journal Classification (ASJC) codes

  • Biophysics
  • Biochemistry
  • Cell Biology

Cite this

Structural differences of oxidized iron-sulfur and nickel-iron cofactors in O2-tolerant and O2-sensitive hydrogenases studied by X-ray absorption spectroscopy. / Sigfridsson, Kajsa G.V.; Leidel, Nils; Sanganas, Oliver; Chernev, Petko; Lenz, Oliver; Yoon, Ki Suk; Nishihara, Hirofumi; Parkin, Alison; Armstrong, Fraser A.; Dementin, Sébastien; Rousset, Marc; De Lacey, Antonio L.; Haumann, Michael.

In: Biochimica et Biophysica Acta - Bioenergetics, Vol. 1847, No. 2, 01.01.2015, p. 162-170.

Research output: Contribution to journalArticle

Sigfridsson, KGV, Leidel, N, Sanganas, O, Chernev, P, Lenz, O, Yoon, KS, Nishihara, H, Parkin, A, Armstrong, FA, Dementin, S, Rousset, M, De Lacey, AL & Haumann, M 2015, 'Structural differences of oxidized iron-sulfur and nickel-iron cofactors in O2-tolerant and O2-sensitive hydrogenases studied by X-ray absorption spectroscopy', Biochimica et Biophysica Acta - Bioenergetics, vol. 1847, no. 2, pp. 162-170. https://doi.org/10.1016/j.bbabio.2014.06.011
Sigfridsson, Kajsa G.V. ; Leidel, Nils ; Sanganas, Oliver ; Chernev, Petko ; Lenz, Oliver ; Yoon, Ki Suk ; Nishihara, Hirofumi ; Parkin, Alison ; Armstrong, Fraser A. ; Dementin, Sébastien ; Rousset, Marc ; De Lacey, Antonio L. ; Haumann, Michael. / Structural differences of oxidized iron-sulfur and nickel-iron cofactors in O2-tolerant and O2-sensitive hydrogenases studied by X-ray absorption spectroscopy. In: Biochimica et Biophysica Acta - Bioenergetics. 2015 ; Vol. 1847, No. 2. pp. 162-170.
@article{de21bf0084d343a9b5d5e3e3085b9935,
title = "Structural differences of oxidized iron-sulfur and nickel-iron cofactors in O2-tolerant and O2-sensitive hydrogenases studied by X-ray absorption spectroscopy",
abstract = "The class of [NiFe]-hydrogenases comprises oxygen-sensitive periplasmic (PH) and oxygen-tolerant membrane-bound (MBH) enzymes. For three PHs and four MBHs from six bacterial species, structural features of the nickel-iron active site of hydrogen turnover and of the iron-sulfur clusters functioning in electron transfer were determined using X-ray absorption spectroscopy (XAS). Fe-XAS indicated surplus oxidized iron and a lower number of ∼ 2.7 {\AA} Fe-Fe distances plus additional shorter and longer distances in the oxidized MBHs compared to the oxidized PHs. This supported a double-oxidized and modified proximal FeS cluster in all MBHs with an apparent trimer-plus-monomer arrangement of its four iron atoms, in agreement with crystal data showing a [4Fe3S] cluster instead of a [4Fe4S] cubane as in the PHs. Ni-XAS indicated coordination of the nickel by the thiol group sulfurs of four conserved cysteines and at least one iron-oxygen bond in both MBH and PH proteins. Structural differences of the oxidized inactive [NiFe] cofactor of MBHs in the Ni-B state compared to PHs in the Ni-A state included a ∼ 0.05 {\AA} longer Ni-O bond, a two times larger spread of the Ni-S bond lengths, and a ∼ 0.1 {\AA} shorter Ni-Fe distance. The modified proximal [4Fe3S] cluster, weaker binding of the Ni-Fe bridging oxygen species, and an altered localization of reduced oxygen species at the active site may each contribute to O2 tolerance.",
author = "Sigfridsson, {Kajsa G.V.} and Nils Leidel and Oliver Sanganas and Petko Chernev and Oliver Lenz and Yoon, {Ki Suk} and Hirofumi Nishihara and Alison Parkin and Armstrong, {Fraser A.} and S{\'e}bastien Dementin and Marc Rousset and {De Lacey}, {Antonio L.} and Michael Haumann",
year = "2015",
month = "1",
day = "1",
doi = "10.1016/j.bbabio.2014.06.011",
language = "English",
volume = "1847",
pages = "162--170",
journal = "Biochimica et Biophysica Acta - Bioenergetics",
issn = "0005-2728",
publisher = "Elsevier",
number = "2",

}

TY - JOUR

T1 - Structural differences of oxidized iron-sulfur and nickel-iron cofactors in O2-tolerant and O2-sensitive hydrogenases studied by X-ray absorption spectroscopy

AU - Sigfridsson, Kajsa G.V.

AU - Leidel, Nils

AU - Sanganas, Oliver

AU - Chernev, Petko

AU - Lenz, Oliver

AU - Yoon, Ki Suk

AU - Nishihara, Hirofumi

AU - Parkin, Alison

AU - Armstrong, Fraser A.

AU - Dementin, Sébastien

AU - Rousset, Marc

AU - De Lacey, Antonio L.

AU - Haumann, Michael

PY - 2015/1/1

Y1 - 2015/1/1

N2 - The class of [NiFe]-hydrogenases comprises oxygen-sensitive periplasmic (PH) and oxygen-tolerant membrane-bound (MBH) enzymes. For three PHs and four MBHs from six bacterial species, structural features of the nickel-iron active site of hydrogen turnover and of the iron-sulfur clusters functioning in electron transfer were determined using X-ray absorption spectroscopy (XAS). Fe-XAS indicated surplus oxidized iron and a lower number of ∼ 2.7 Å Fe-Fe distances plus additional shorter and longer distances in the oxidized MBHs compared to the oxidized PHs. This supported a double-oxidized and modified proximal FeS cluster in all MBHs with an apparent trimer-plus-monomer arrangement of its four iron atoms, in agreement with crystal data showing a [4Fe3S] cluster instead of a [4Fe4S] cubane as in the PHs. Ni-XAS indicated coordination of the nickel by the thiol group sulfurs of four conserved cysteines and at least one iron-oxygen bond in both MBH and PH proteins. Structural differences of the oxidized inactive [NiFe] cofactor of MBHs in the Ni-B state compared to PHs in the Ni-A state included a ∼ 0.05 Å longer Ni-O bond, a two times larger spread of the Ni-S bond lengths, and a ∼ 0.1 Å shorter Ni-Fe distance. The modified proximal [4Fe3S] cluster, weaker binding of the Ni-Fe bridging oxygen species, and an altered localization of reduced oxygen species at the active site may each contribute to O2 tolerance.

AB - The class of [NiFe]-hydrogenases comprises oxygen-sensitive periplasmic (PH) and oxygen-tolerant membrane-bound (MBH) enzymes. For three PHs and four MBHs from six bacterial species, structural features of the nickel-iron active site of hydrogen turnover and of the iron-sulfur clusters functioning in electron transfer were determined using X-ray absorption spectroscopy (XAS). Fe-XAS indicated surplus oxidized iron and a lower number of ∼ 2.7 Å Fe-Fe distances plus additional shorter and longer distances in the oxidized MBHs compared to the oxidized PHs. This supported a double-oxidized and modified proximal FeS cluster in all MBHs with an apparent trimer-plus-monomer arrangement of its four iron atoms, in agreement with crystal data showing a [4Fe3S] cluster instead of a [4Fe4S] cubane as in the PHs. Ni-XAS indicated coordination of the nickel by the thiol group sulfurs of four conserved cysteines and at least one iron-oxygen bond in both MBH and PH proteins. Structural differences of the oxidized inactive [NiFe] cofactor of MBHs in the Ni-B state compared to PHs in the Ni-A state included a ∼ 0.05 Å longer Ni-O bond, a two times larger spread of the Ni-S bond lengths, and a ∼ 0.1 Å shorter Ni-Fe distance. The modified proximal [4Fe3S] cluster, weaker binding of the Ni-Fe bridging oxygen species, and an altered localization of reduced oxygen species at the active site may each contribute to O2 tolerance.

UR - http://www.scopus.com/inward/record.url?scp=84911869446&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84911869446&partnerID=8YFLogxK

U2 - 10.1016/j.bbabio.2014.06.011

DO - 10.1016/j.bbabio.2014.06.011

M3 - Article

VL - 1847

SP - 162

EP - 170

JO - Biochimica et Biophysica Acta - Bioenergetics

JF - Biochimica et Biophysica Acta - Bioenergetics

SN - 0005-2728

IS - 2

ER -