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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. LU ; Leidel, Nils ; Sanganas, Oliver ; Chernev, Petko ; Lenz, Oliver ; Yoon, Ki Seok ; Nishihara, Hirofumi ; Parkin, Alison ; Armstrong, Fraser A. and Dementin, Sébastien , et al. (2015) In Biochimica et Biophysica Acta - Bioenergetics 1847(2). p.162-170
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... (More)

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.

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publishing date
type
Contribution to journal
publication status
published
keywords
FeS cluster, O-tolerance, X-ray absorption spectroscopy, [NiFe] active site, [NiFe]-hydrogenase
in
Biochimica et Biophysica Acta - Bioenergetics
volume
1847
issue
2
pages
9 pages
publisher
Elsevier
external identifiers
  • scopus:84911869446
  • pmid:25316302
ISSN
0005-2728
DOI
10.1016/j.bbabio.2014.06.011
language
English
LU publication?
no
id
5d893726-3e5b-4761-a521-9b8b00809a1f
date added to LUP
2020-01-15 10:12:27
date last changed
2021-02-17 07:08:59
@article{5d893726-3e5b-4761-a521-9b8b00809a1f,
  abstract     = {<p>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 O<sub>2</sub> tolerance.</p>},
  author       = {Sigfridsson, Kajsa G.V. and Leidel, Nils and Sanganas, Oliver and Chernev, Petko and Lenz, Oliver and Yoon, Ki Seok and Nishihara, Hirofumi and Parkin, Alison and Armstrong, Fraser A. and Dementin, Sébastien and Rousset, Marc and De Lacey, Antonio L. and Haumann, Michael},
  issn         = {0005-2728},
  language     = {eng},
  month        = {01},
  number       = {2},
  pages        = {162--170},
  publisher    = {Elsevier},
  series       = {Biochimica et Biophysica Acta - Bioenergetics},
  title        = {Structural differences of oxidized iron-sulfur and nickel-iron cofactors in O<sub>2</sub>-tolerant and O<sub>2</sub>-sensitive hydrogenases studied by X-ray absorption spectroscopy},
  url          = {http://dx.doi.org/10.1016/j.bbabio.2014.06.011},
  doi          = {10.1016/j.bbabio.2014.06.011},
  volume       = {1847},
  year         = {2015},
}