Trinuclear copper biocatalytic center forms an active site of thiocyanate dehydrogenase

Tamara V. Tikhonova; Dimitry Y. Sorokin; Wilfred R. Hagen; Maria G. Khrenova; Gerard Muyzer; Tatiana V. Rakitina; Ivan G. Shabalin; Anton A. Trofimov; Stanislav I. Tsallagov; Vladimir O. Popov

doi:10.1073/pnas.1922133117

Trinuclear copper biocatalytic center forms an active site of thiocyanate dehydrogenase

Tamara V. Tikhonova, Dimitry Y. Sorokin, Wilfred R. Hagen, Maria G. Khrenova, Gerard Muyzer, Tatiana V. Rakitina, Ivan G. Shabalin, Anton A. Trofimov, Stanislav I. Tsallagov, Vladimir O. Popov^*

^*Corresponding author for this work

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Abstract

Biocatalytic copper centers are generally involved in the activation and reduction of dioxygen, with only few exceptions known. Here we report the discovery and characterization of a previously undescribed copper center that forms the active site of a copper-containing enzyme thiocyanate dehydrogenase (suggested EC 1.8.2.7) that was purified from the haloalkaliphilic sulfur-oxidizing bacterium of the genus Thioalkalivibrio ubiquitous in saline alkaline soda lakes. The copper cluster is formed by three copper ions located at the corners of a near-isosceles triangle and facilitates a direct thiocyanate conversion into cyanate, elemental sulfur, and two reducing equivalents without involvement of molecular oxygen. A molecular mechanism of catalysis is suggested based on high-resolution three-dimensional structures, electron paramagnetic resonance (EPR) spectroscopy, quantum mechanics/molecular mechanics (QM/MM) simulations, kinetic studies, and the results of site-directed mutagenesis.

Original language	English
Pages (from-to)	5280-5290
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	117
Issue number	10
DOIs	https://doi.org/10.1073/pnas.1922133117
Publication status	Published - 2020

Bibliographical note

Green Open Access added to TU Delft Institutional Repository ‘You share, we take care!’ – Taverne project https://www.openaccess.nl/en/you-share-we-take-care
Otherwise as indicated in the copyright section: the publisher is the copyright holder of this work and the author uses the Dutch legislation to make this work public.

Keywords

Copper centers
Crystal structure
EPR
Molecular mechanism
Thiocyanate dehydrogenase

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Tikhonova, T. V., Sorokin, D. Y., Hagen, W. R., Khrenova, M. G., Muyzer, G., Rakitina, T. V., Shabalin, I. G., Trofimov, A. A., Tsallagov, S. I., & Popov, V. O. (2020). Trinuclear copper biocatalytic center forms an active site of thiocyanate dehydrogenase. Proceedings of the National Academy of Sciences of the United States of America, 117(10), 5280-5290. https://doi.org/10.1073/pnas.1922133117

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title = "Trinuclear copper biocatalytic center forms an active site of thiocyanate dehydrogenase",

abstract = "Biocatalytic copper centers are generally involved in the activation and reduction of dioxygen, with only few exceptions known. Here we report the discovery and characterization of a previously undescribed copper center that forms the active site of a copper-containing enzyme thiocyanate dehydrogenase (suggested EC 1.8.2.7) that was purified from the haloalkaliphilic sulfur-oxidizing bacterium of the genus Thioalkalivibrio ubiquitous in saline alkaline soda lakes. The copper cluster is formed by three copper ions located at the corners of a near-isosceles triangle and facilitates a direct thiocyanate conversion into cyanate, elemental sulfur, and two reducing equivalents without involvement of molecular oxygen. A molecular mechanism of catalysis is suggested based on high-resolution three-dimensional structures, electron paramagnetic resonance (EPR) spectroscopy, quantum mechanics/molecular mechanics (QM/MM) simulations, kinetic studies, and the results of site-directed mutagenesis.",

keywords = "Copper centers, Crystal structure, EPR, Molecular mechanism, Thiocyanate dehydrogenase",

author = "Tikhonova, {Tamara V.} and Sorokin, {Dimitry Y.} and Hagen, {Wilfred R.} and Khrenova, {Maria G.} and Gerard Muyzer and Rakitina, {Tatiana V.} and Shabalin, {Ivan G.} and Trofimov, {Anton A.} and Tsallagov, {Stanislav I.} and Popov, {Vladimir O.}",

note = "Green Open Access added to TU Delft Institutional Repository {\textquoteleft}You share, we take care!{\textquoteright} – Taverne project https://www.openaccess.nl/en/you-share-we-take-care Otherwise as indicated in the copyright section: the publisher is the copyright holder of this work and the author uses the Dutch legislation to make this work public. ",

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doi = "10.1073/pnas.1922133117",

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Tikhonova, TV, Sorokin, DY , Hagen, WR, Khrenova, MG, Muyzer, G, Rakitina, TV, Shabalin, IG, Trofimov, AA, Tsallagov, SI & Popov, VO 2020, 'Trinuclear copper biocatalytic center forms an active site of thiocyanate dehydrogenase', Proceedings of the National Academy of Sciences of the United States of America, vol. 117, no. 10, pp. 5280-5290. https://doi.org/10.1073/pnas.1922133117

TY - JOUR

T1 - Trinuclear copper biocatalytic center forms an active site of thiocyanate dehydrogenase

AU - Tikhonova, Tamara V.

AU - Sorokin, Dimitry Y.

AU - Hagen, Wilfred R.

AU - Khrenova, Maria G.

AU - Muyzer, Gerard

AU - Rakitina, Tatiana V.

AU - Shabalin, Ivan G.

AU - Trofimov, Anton A.

AU - Tsallagov, Stanislav I.

AU - Popov, Vladimir O.

N1 - Green Open Access added to TU Delft Institutional Repository ‘You share, we take care!’ – Taverne project https://www.openaccess.nl/en/you-share-we-take-care Otherwise as indicated in the copyright section: the publisher is the copyright holder of this work and the author uses the Dutch legislation to make this work public.

PY - 2020

Y1 - 2020

N2 - Biocatalytic copper centers are generally involved in the activation and reduction of dioxygen, with only few exceptions known. Here we report the discovery and characterization of a previously undescribed copper center that forms the active site of a copper-containing enzyme thiocyanate dehydrogenase (suggested EC 1.8.2.7) that was purified from the haloalkaliphilic sulfur-oxidizing bacterium of the genus Thioalkalivibrio ubiquitous in saline alkaline soda lakes. The copper cluster is formed by three copper ions located at the corners of a near-isosceles triangle and facilitates a direct thiocyanate conversion into cyanate, elemental sulfur, and two reducing equivalents without involvement of molecular oxygen. A molecular mechanism of catalysis is suggested based on high-resolution three-dimensional structures, electron paramagnetic resonance (EPR) spectroscopy, quantum mechanics/molecular mechanics (QM/MM) simulations, kinetic studies, and the results of site-directed mutagenesis.

AB - Biocatalytic copper centers are generally involved in the activation and reduction of dioxygen, with only few exceptions known. Here we report the discovery and characterization of a previously undescribed copper center that forms the active site of a copper-containing enzyme thiocyanate dehydrogenase (suggested EC 1.8.2.7) that was purified from the haloalkaliphilic sulfur-oxidizing bacterium of the genus Thioalkalivibrio ubiquitous in saline alkaline soda lakes. The copper cluster is formed by three copper ions located at the corners of a near-isosceles triangle and facilitates a direct thiocyanate conversion into cyanate, elemental sulfur, and two reducing equivalents without involvement of molecular oxygen. A molecular mechanism of catalysis is suggested based on high-resolution three-dimensional structures, electron paramagnetic resonance (EPR) spectroscopy, quantum mechanics/molecular mechanics (QM/MM) simulations, kinetic studies, and the results of site-directed mutagenesis.

KW - Copper centers

KW - Crystal structure

KW - EPR

KW - Molecular mechanism

KW - Thiocyanate dehydrogenase

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U2 - 10.1073/pnas.1922133117

DO - 10.1073/pnas.1922133117

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AN - SCOPUS:85081681106

SN - 0027-8424

VL - 117

SP - 5280

EP - 5290

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 10

ER -

Trinuclear copper biocatalytic center forms an active site of thiocyanate dehydrogenase

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Keywords

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