Tuning Catalytic Bias of Hydrogen Gas Producing Hydrogenases

Jacob H. Artz; Oleg A. Zadvornyy; David W. Mulder; Stephen M. Keable; Aina E. Cohen; Michael W. Ratzloff; S. Garrett Williams; Bojana Ginovska; Neeraj Kumar; Jinhu Song; Scott E. McPhillips; Catherine M. Davidson; Artem Y. Lyubimov; Natasha Pence; Gerrit J. Schut; Anne K. Jones; S. Michael Soltis; Michael W.W. Adams; Simone Raugei; Paul W. King; John W. Peters

doi:10.1021/jacs.9b08756

Tuning Catalytic Bias of Hydrogen Gas Producing Hydrogenases

Jacob H. Artz, Oleg A. Zadvornyy, David W. Mulder, Stephen M. Keable, Aina E. Cohen, Michael W. Ratzloff, S. Garrett Williams, Bojana Ginovska, Neeraj Kumar, Jinhu Song, Scott E. McPhillips, Catherine M. Davidson, Artem Y. Lyubimov, Natasha Pence, Gerrit J. Schut, Anne K. Jones, S. Michael Soltis, Michael W.W. Adams, Simone Raugei, Paul W. KingJohn W. Peters

Molecular Sciences, School of (SMS)

Research output: Contribution to journal › Article › peer-review

50 Scopus citations

Abstract

Hydrogenases display a wide range of catalytic rates and biases in reversible hydrogen gas oxidation catalysis. The interactions of the iron-sulfur-containing catalytic site with the local protein environment are thought to contribute to differences in catalytic reactivity, but this has not been demonstrated. The microbe Clostridium pasteurianum produces three [FeFe]-hydrogenases that differ in "catalytic bias" by exerting a disproportionate rate acceleration in one direction or the other that spans a remarkable 6 orders of magnitude. The combination of high-resolution structural work, biochemical analyses, and computational modeling indicates that protein secondary interactions directly influence the relative stabilization/destabilization of different oxidation states of the active site metal cluster. This selective stabilization or destabilization of oxidation states can preferentially promote hydrogen oxidation or proton reduction and represents a simple yet elegant model by which a protein catalytic site can confer catalytic bias.

Original language	English (US)
Pages (from-to)	1227-1235
Number of pages	9
Journal	Journal of the American Chemical Society
Volume	142
Issue number	3
DOIs	https://doi.org/10.1021/jacs.9b08756
State	Published - Jan 22 2020

ASJC Scopus subject areas

Catalysis
General Chemistry
Biochemistry
Colloid and Surface Chemistry

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10.1021/jacs.9b08756

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Artz, J. H., Zadvornyy, O. A., Mulder, D. W., Keable, S. M., Cohen, A. E., Ratzloff, M. W., Williams, S. G., Ginovska, B., Kumar, N., Song, J., McPhillips, S. E., Davidson, C. M., Lyubimov, A. Y., Pence, N., Schut, G. J., Jones, A. K., Soltis, S. M., Adams, M. W. W., Raugei, S., ... Peters, J. W. (2020). Tuning Catalytic Bias of Hydrogen Gas Producing Hydrogenases. Journal of the American Chemical Society, 142(3), 1227-1235. https://doi.org/10.1021/jacs.9b08756

Artz, JH, Zadvornyy, OA, Mulder, DW, Keable, SM, Cohen, AE, Ratzloff, MW, Williams, SG, Ginovska, B, Kumar, N, Song, J, McPhillips, SE, Davidson, CM, Lyubimov, AY, Pence, N, Schut, GJ, Jones, AK, Soltis, SM, Adams, MWW, Raugei, S, King, PW & Peters, JW 2020, 'Tuning Catalytic Bias of Hydrogen Gas Producing Hydrogenases', Journal of the American Chemical Society, vol. 142, no. 3, pp. 1227-1235. https://doi.org/10.1021/jacs.9b08756

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abstract = "Hydrogenases display a wide range of catalytic rates and biases in reversible hydrogen gas oxidation catalysis. The interactions of the iron-sulfur-containing catalytic site with the local protein environment are thought to contribute to differences in catalytic reactivity, but this has not been demonstrated. The microbe Clostridium pasteurianum produces three [FeFe]-hydrogenases that differ in {"}catalytic bias{"} by exerting a disproportionate rate acceleration in one direction or the other that spans a remarkable 6 orders of magnitude. The combination of high-resolution structural work, biochemical analyses, and computational modeling indicates that protein secondary interactions directly influence the relative stabilization/destabilization of different oxidation states of the active site metal cluster. This selective stabilization or destabilization of oxidation states can preferentially promote hydrogen oxidation or proton reduction and represents a simple yet elegant model by which a protein catalytic site can confer catalytic bias.",

author = "Artz, {Jacob H.} and Zadvornyy, {Oleg A.} and Mulder, {David W.} and Keable, {Stephen M.} and Cohen, {Aina E.} and Ratzloff, {Michael W.} and Williams, {S. Garrett} and Bojana Ginovska and Neeraj Kumar and Jinhu Song and McPhillips, {Scott E.} and Davidson, {Catherine M.} and Lyubimov, {Artem Y.} and Natasha Pence and Schut, {Gerrit J.} and Jones, {Anne K.} and Soltis, {S. Michael} and Adams, {Michael W.W.} and Simone Raugei and King, {Paul W.} and Peters, {John W.}",

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AU - Pence, Natasha

AU - Schut, Gerrit J.

AU - Jones, Anne K.

AU - Soltis, S. Michael

AU - Adams, Michael W.W.

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AU - King, Paul W.

AU - Peters, John W.

PY - 2020/1/22

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AB - Hydrogenases display a wide range of catalytic rates and biases in reversible hydrogen gas oxidation catalysis. The interactions of the iron-sulfur-containing catalytic site with the local protein environment are thought to contribute to differences in catalytic reactivity, but this has not been demonstrated. The microbe Clostridium pasteurianum produces three [FeFe]-hydrogenases that differ in "catalytic bias" by exerting a disproportionate rate acceleration in one direction or the other that spans a remarkable 6 orders of magnitude. The combination of high-resolution structural work, biochemical analyses, and computational modeling indicates that protein secondary interactions directly influence the relative stabilization/destabilization of different oxidation states of the active site metal cluster. This selective stabilization or destabilization of oxidation states can preferentially promote hydrogen oxidation or proton reduction and represents a simple yet elegant model by which a protein catalytic site can confer catalytic bias.

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Tuning Catalytic Bias of Hydrogen Gas Producing Hydrogenases

Abstract

ASJC Scopus subject areas

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Crystal structure of [FeFe]-hydrogenase I (CpI) solved with single pulse free electron laser data

1.0 Angstrom crystal structure of [FeFe]-hydrogenase

Crystal structure of [FeFe]-hydrogenase in the presence of 7 mM Sodium dithionite

Cite this

Tuning Catalytic Bias of Hydrogen Gas Producing Hydrogenases

Abstract

ASJC Scopus subject areas

Access to Document

Other files and links

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Datasets

Crystal structure of [FeFe]-hydrogenase I (CpI) solved with single pulse free electron laser data

1.0 Angstrom crystal structure of [FeFe]-hydrogenase

Crystal structure of [FeFe]-hydrogenase in the presence of 7 mM Sodium dithionite

Cite this