Identification and structure of a novel archaeal HypB for [NiFe] hydrogenase maturation

Daisuke Sasaki, Satoshi Watanabe, Rie Matsumi, Toshihisa Shoji, Ayako Yasukochi, Kenta Tagashira, Wakao Fukuda, Tamotsu Kanai, Haruyuki Atomi, Tadayuki Imanaka, Kunio Miki

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14 Citations (Scopus)

Abstract

HypB (metal-binding GTPase) and HypA (nickel metallochaperone) are required for nickel insertion into [NiFe] hydrogenase. However, the HypB homolog proteins are not found in some archaeal species including Thermococcales. In this article, we identify a novel archaeal Mrp/MinD family ATPase-type HypB from Thermococcus kodakarensis (Tk-mmHypB) and determine its crystal structure. The mmhypB gene is conserved among species lacking the hypB gene and is located adjacent to the hypA gene on their genome. Deletion of the mmhypB gene leads to a significant reduction in hydrogen-dependent growth of T. kodakarensis, which is restored by nickel supplementation. The monomer structure of Tk-mmHypB is similar to those of the Mrp/MinD family ATPases. The ADP molecules are tightly bound to the protein. Isothermal titration calorimetry shows that Tk-mmHypB binds ATP with a Kd value of 84 nM. ADP binds more tightly than does ATP, with a Kd value of 15 nM. The closed Tk-mmHypB dimer in the crystallographic asymmetric unit is consistent with the ATP-hydrolysis-deficient dimer of the Mrp/MinD family Soj/MinD proteins. Structural comparisons with these proteins suggest the ATP-binding dependent conformational change and rearrangement of the Tk-mmHypB dimer. These observations imply that the nickel insertion process during the [NiFe] hydrogenase maturation is performed by HypA, mmHypB, and a nucleotide exchange factor in these archaea.

Original languageEnglish
Pages (from-to)1627-1640
Number of pages14
JournalJournal of Molecular Biology
Volume425
Issue number10
DOIs
Publication statusPublished - May 27 2013

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Nickel
Adenosine Triphosphate
Adenosine Diphosphate
Thermococcales
Adenosine Triphosphatases
Metallochaperones
Proteins
Thermococcus
Genes
Calorimetry
GTP Phosphohydrolases
Archaea
Gene Deletion
Hydrogen
Hydrolysis
Nucleotides
Metals
Genome
nickel-iron hydrogenase
Growth

All Science Journal Classification (ASJC) codes

  • Structural Biology
  • Molecular Biology

Cite this

Sasaki, D., Watanabe, S., Matsumi, R., Shoji, T., Yasukochi, A., Tagashira, K., ... Miki, K. (2013). Identification and structure of a novel archaeal HypB for [NiFe] hydrogenase maturation. Journal of Molecular Biology, 425(10), 1627-1640. https://doi.org/10.1016/j.jmb.2013.02.004

Identification and structure of a novel archaeal HypB for [NiFe] hydrogenase maturation. / Sasaki, Daisuke; Watanabe, Satoshi; Matsumi, Rie; Shoji, Toshihisa; Yasukochi, Ayako; Tagashira, Kenta; Fukuda, Wakao; Kanai, Tamotsu; Atomi, Haruyuki; Imanaka, Tadayuki; Miki, Kunio.

In: Journal of Molecular Biology, Vol. 425, No. 10, 27.05.2013, p. 1627-1640.

Research output: Contribution to journalArticle

Sasaki, D, Watanabe, S, Matsumi, R, Shoji, T, Yasukochi, A, Tagashira, K, Fukuda, W, Kanai, T, Atomi, H, Imanaka, T & Miki, K 2013, 'Identification and structure of a novel archaeal HypB for [NiFe] hydrogenase maturation', Journal of Molecular Biology, vol. 425, no. 10, pp. 1627-1640. https://doi.org/10.1016/j.jmb.2013.02.004
Sasaki D, Watanabe S, Matsumi R, Shoji T, Yasukochi A, Tagashira K et al. Identification and structure of a novel archaeal HypB for [NiFe] hydrogenase maturation. Journal of Molecular Biology. 2013 May 27;425(10):1627-1640. https://doi.org/10.1016/j.jmb.2013.02.004
Sasaki, Daisuke ; Watanabe, Satoshi ; Matsumi, Rie ; Shoji, Toshihisa ; Yasukochi, Ayako ; Tagashira, Kenta ; Fukuda, Wakao ; Kanai, Tamotsu ; Atomi, Haruyuki ; Imanaka, Tadayuki ; Miki, Kunio. / Identification and structure of a novel archaeal HypB for [NiFe] hydrogenase maturation. In: Journal of Molecular Biology. 2013 ; Vol. 425, No. 10. pp. 1627-1640.
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AU - Tagashira, Kenta

AU - Fukuda, Wakao

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