Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase

Yasuhito Shomura, Ki Suk Yoon, Hirofumi Nishihara, Yoshiki Higuchi

Research output: Contribution to journalArticle

189 Citations (Scopus)

Abstract

Membrane-bound respiratory [NiFe]-hydrogenase (MBH), a H 2-uptake enzyme found in the periplasmic space of bacteria, catalyses the oxidation of dihydrogen: H 2 →2H + + 2e - (ref. 1). In contrast to the well-studied O 2-sensitive [NiFe]-hydrogenases (referred to as the standard enzymes), MBH has an O 2-tolerant H 2 oxidation activity; however, the mechanism of O 2 tolerance is unclear. Here we report the crystal structures of Hydrogenovibrio marinus MBH in three different redox conditions at resolutions between 1.18 and 1.32Å We find that the proximal iron-sulphur (Fe-S) cluster of MBH has a [4Fe-3S] structure coordinated by six cysteine residues-in contrast to the [4Fe-4S] cubane structure coordinated by four cysteine residues found in the proximal Fe-S cluster of the standard enzymes-and that an amide nitrogen of the polypeptide backbone is deprotonated and additionally coordinates the cluster when chemically oxidized, thus stabilizing the superoxidized state of the cluster. The structure of MBH is very similar to that of the O 2-sensitive standard enzymes except for the proximal Fe-S cluster. Our results give a reasonable explanation why the O 2 tolerance of MBH is attributable to the unique proximal Fe-S cluster; we propose that the cluster is not only a component of the electron transfer for the catalytic cycle, but that it also donates two electrons and one proton crucial for the appropriate reduction of O 2 in preventing the formation of an unready, inactive state of the enzyme.

Original languageEnglish
Pages (from-to)253-256
Number of pages4
JournalNature
Volume479
Issue number7372
DOIs
Publication statusPublished - Nov 10 2011

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Oxygen
Membranes
Enzymes
Cysteine
Electrons
Periplasm
Sulfur
Amides
Oxidation-Reduction
Protons
Nitrogen
Iron
nickel-iron hydrogenase
Bacteria
Peptides

All Science Journal Classification (ASJC) codes

  • General

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Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase. / Shomura, Yasuhito; Yoon, Ki Suk; Nishihara, Hirofumi; Higuchi, Yoshiki.

In: Nature, Vol. 479, No. 7372, 10.11.2011, p. 253-256.

Research output: Contribution to journalArticle

Shomura, Yasuhito ; Yoon, Ki Suk ; Nishihara, Hirofumi ; Higuchi, Yoshiki. / Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase. In: Nature. 2011 ; Vol. 479, No. 7372. pp. 253-256.
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abstract = "Membrane-bound respiratory [NiFe]-hydrogenase (MBH), a H 2-uptake enzyme found in the periplasmic space of bacteria, catalyses the oxidation of dihydrogen: H 2 →2H + + 2e - (ref. 1). In contrast to the well-studied O 2-sensitive [NiFe]-hydrogenases (referred to as the standard enzymes), MBH has an O 2-tolerant H 2 oxidation activity; however, the mechanism of O 2 tolerance is unclear. Here we report the crystal structures of Hydrogenovibrio marinus MBH in three different redox conditions at resolutions between 1.18 and 1.32{\AA} We find that the proximal iron-sulphur (Fe-S) cluster of MBH has a [4Fe-3S] structure coordinated by six cysteine residues-in contrast to the [4Fe-4S] cubane structure coordinated by four cysteine residues found in the proximal Fe-S cluster of the standard enzymes-and that an amide nitrogen of the polypeptide backbone is deprotonated and additionally coordinates the cluster when chemically oxidized, thus stabilizing the superoxidized state of the cluster. The structure of MBH is very similar to that of the O 2-sensitive standard enzymes except for the proximal Fe-S cluster. Our results give a reasonable explanation why the O 2 tolerance of MBH is attributable to the unique proximal Fe-S cluster; we propose that the cluster is not only a component of the electron transfer for the catalytic cycle, but that it also donates two electrons and one proton crucial for the appropriate reduction of O 2 in preventing the formation of an unready, inactive state of the enzyme.",
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