The binuclear cluster of [FeFe] hydrogenase is formed with sulfur donated by cysteine of an [Fe(Cys)(CO) 2 (CN)] organometallic precursor
Abstract
Significance [FeFe]-hydrogenases catalyze H 2 evolution at extraordinary rates at low overpotential using base metal (not platinum). In the field of renewable energy, the biosynthesis of these enzymes’ active sites, the H-cluster, is of intense interest. Among its many cofactors, the azadithiolate is unique, and its biosynthesis remains enigmatic. Three Fe–S proteins, HydE, HydF, and HydG, are essential for the H-cluster bioassembly. This paper describes an in vitro assembly approach where a synthetic [Fe(cysteine)(CO) 2 (CN)] complex, “syn-B,” allows HydG-free biosynthesis of the active enzyme. Using isotopic and S/Se labeling, syn-B is shown to contribute Fe(CO) 2 (CN)S to the biosynthesis. This work sets the stage for further investigation of the H-cluster bioassembly.
- Authors:
-
[1];
[3];
[1];
[2]
- Department of Chemistry, University of California, Davis, CA 95616,
- School of Chemical Sciences, University of Illinois at Urbana–Champaign, Urbana, IL 61801,
- Department of Chemical Physiology and Biochemistry, Oregon Health and Science University, Portland, OR 97239
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1567868
- Grant/Contract Number:
- AC02-76SF00515
- Resource Type:
- Published Article
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 42; Journal ID: ISSN 0027-8424
- Publisher:
- Proceedings of the National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
Citation Formats
Rao, Guodong, Pattenaude, Scott A., Alwan, Katherine, Blackburn, Ninian J., Britt, R. David, and Rauchfuss, Thomas B. The binuclear cluster of [FeFe] hydrogenase is formed with sulfur donated by cysteine of an [Fe(Cys)(CO) 2 (CN)] organometallic precursor. United States: N. p., 2019.
Web. doi:10.1073/pnas.1913324116.
Rao, Guodong, Pattenaude, Scott A., Alwan, Katherine, Blackburn, Ninian J., Britt, R. David, & Rauchfuss, Thomas B. The binuclear cluster of [FeFe] hydrogenase is formed with sulfur donated by cysteine of an [Fe(Cys)(CO) 2 (CN)] organometallic precursor. United States. https://doi.org/10.1073/pnas.1913324116
Rao, Guodong, Pattenaude, Scott A., Alwan, Katherine, Blackburn, Ninian J., Britt, R. David, and Rauchfuss, Thomas B. Mon .
"The binuclear cluster of [FeFe] hydrogenase is formed with sulfur donated by cysteine of an [Fe(Cys)(CO) 2 (CN)] organometallic precursor". United States. https://doi.org/10.1073/pnas.1913324116.
@article{osti_1567868,
title = {The binuclear cluster of [FeFe] hydrogenase is formed with sulfur donated by cysteine of an [Fe(Cys)(CO) 2 (CN)] organometallic precursor},
author = {Rao, Guodong and Pattenaude, Scott A. and Alwan, Katherine and Blackburn, Ninian J. and Britt, R. David and Rauchfuss, Thomas B.},
abstractNote = {Significance [FeFe]-hydrogenases catalyze H 2 evolution at extraordinary rates at low overpotential using base metal (not platinum). In the field of renewable energy, the biosynthesis of these enzymes’ active sites, the H-cluster, is of intense interest. Among its many cofactors, the azadithiolate is unique, and its biosynthesis remains enigmatic. Three Fe–S proteins, HydE, HydF, and HydG, are essential for the H-cluster bioassembly. This paper describes an in vitro assembly approach where a synthetic [Fe(cysteine)(CO) 2 (CN)] complex, “syn-B,” allows HydG-free biosynthesis of the active enzyme. Using isotopic and S/Se labeling, syn-B is shown to contribute Fe(CO) 2 (CN)S to the biosynthesis. This work sets the stage for further investigation of the H-cluster bioassembly.},
doi = {10.1073/pnas.1913324116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 42,
volume = 116,
place = {United States},
year = {Mon Sep 30 00:00:00 EDT 2019},
month = {Mon Sep 30 00:00:00 EDT 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.1913324116
https://doi.org/10.1073/pnas.1913324116
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 23 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
The role of the maturase HydG in [FeFe]‐hydrogenase active site synthesis and assembly
journal, January 2009
- Pilet, Eric; Nicolet, Yvain; Mathevon, Carole
- FEBS Letters, Vol. 583, Issue 3
Structural and functional characterization of the hydrogenase-maturation HydF protein
journal, May 2017
- Caserta, Giorgio; Pecqueur, Ludovic; Adamska-Venkatesh, Agnieszka
- Nature Chemical Biology, Vol. 13, Issue 7
The Cyanide Ligands of [FeFe] Hydrogenase: Pulse EPR Studies of 13 C and 15 N-Labeled H-Cluster
journal, August 2014
- Myers, William K.; Stich, Troy A.; Suess, Daniel L. M.
- Journal of the American Chemical Society, Vol. 136, Issue 35
[FeFe]-Hydrogenase Maturation: HydG-Catalyzed Synthesis of Carbon Monoxide
journal, July 2010
- Shepard, Eric M.; Duffus, Benjamin R.; George, Simon J.
- Journal of the American Chemical Society, Vol. 132, Issue 27
Biochemical and Kinetic Characterization of Radical S -Adenosyl- l -methionine Enzyme HydG
journal, November 2013
- Driesener, Rebecca C.; Duffus, Benjamin R.; Shepard, Eric M.
- Biochemistry, Vol. 52, Issue 48
Biomimetic assembly and activation of [FeFe]-hydrogenases
journal, June 2013
- Berggren, G.; Adamska, A.; Lambertz, C.
- Nature, Vol. 499, Issue 7456
Precursors to [FeFe]-Hydrogenase Models: Syntheses of Fe 2 (SR) 2 (CO) 6 from CO-Free Iron Sources
journal, August 2008
- Volkers, Phillip I.; Boyke, Christine A.; Chen, Jinzhu
- Inorganic Chemistry, Vol. 47, Issue 15
Frequency and potential dependence of reversible electrocatalytic hydrogen interconversion by [FeFe]-hydrogenases
journal, March 2017
- Pandey, Kavita; Islam, Shams T. A.; Happe, Thomas
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 15
Carbon–sulfur bond-forming reaction catalysed by the radical SAM enzyme HydE
journal, April 2016
- Rohac, Roman; Amara, Patricia; Benjdia, Alhosna
- Nature Chemistry, Vol. 8, Issue 5
The Radical SAM Enzyme HydG Requires Cysteine and a Dangler Iron for Generating an Organometallic Precursor to the [FeFe]-Hydrogenase H-Cluster
journal, January 2016
- Suess, Daniel L. M.; Pham, Cindy C.; Bürstel, Ingmar
- Journal of the American Chemical Society, Vol. 138, Issue 4
Electronic Structure of Two Catalytic States of the [FeFe] Hydrogenase H-Cluster As Probed by Pulse Electron Paramagnetic Resonance Spectroscopy
journal, August 2018
- Rao, Guodong; Britt, R. David
- Inorganic Chemistry, Vol. 57, Issue 17
Cysteine as a ligand platform in the biosynthesis of the FeFe hydrogenase H cluster
journal, August 2015
- Suess, Daniel L. M.; Bürstel, Ingmar; De La Paz, Liliana
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 37
[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation
journal, June 2015
- Peters, John W.; Schut, Gerrit J.; Boyd, Eric S.
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 6
Proton Coupled Electronic Rearrangement within the H-Cluster as an Essential Step in the Catalytic Cycle of [FeFe] Hydrogenases
journal, January 2017
- Sommer, Constanze; Adamska-Venkatesh, Agnieszka; Pawlak, Krzysztof
- Journal of the American Chemical Society, Vol. 139, Issue 4
[FeFe]-Hydrogenase Maturation
journal, June 2014
- Shepard, Eric M.; Mus, Florence; Betz, Jeremiah N.
- Biochemistry, Vol. 53, Issue 25
The HydG Enzyme Generates an Fe(CO)2(CN) Synthon in Assembly of the FeFe Hydrogenase H-Cluster
journal, January 2014
- Kuchenreuther, J. M.; Myers, W. K.; Suess, D. L. M.
- Science, Vol. 343, Issue 6169
Dinuclear Iron(II)−Cyanocarbonyl Complexes Linked by Two/Three Bridging Ethylthiolates: Relevance to the Active Site of [Fe] Hydrogenases
journal, April 2003
- Liaw, Wen-Feng; Tsai, Wen-Ting; Gau, Hung-Bin
- Inorganic Chemistry, Vol. 42, Issue 8
HydF as a scaffold protein in [FeFe] hydrogenase H-cluster biosynthesis
journal, May 2008
- McGlynn, Shawn E.; Shepard, Eric M.; Winslow, Mark A.
- FEBS Letters, Vol. 582, Issue 15
Function and biogenesis of iron–sulphur proteins
journal, August 2009
- Lill, Roland
- Nature, Vol. 460, Issue 7257
Identification of a Catalytic Iron-Hydride at the H-Cluster of [FeFe]-Hydrogenase
journal, December 2016
- Mulder, David W.; Guo, Yisong; Ratzloff, Michael W.
- Journal of the American Chemical Society, Vol. 139, Issue 1
Direct Observation of an Iron-Bound Terminal Hydride in [FeFe]-Hydrogenase by Nuclear Resonance Vibrational Spectroscopy
journal, March 2017
- Reijerse, Edward J.; Pham, Cindy C.; Pelmenschikov, Vladimir
- Journal of the American Chemical Society, Vol. 139, Issue 12
[FeFe]-Hydrogenase Maturation: Insights into the Role HydE Plays in Dithiomethylamine Biosynthesis
journal, March 2015
- Betz, Jeremiah N.; Boswell, Nicholas W.; Fugate, Corey J.
- Biochemistry, Vol. 54, Issue 9
X-ray crystallographic and EPR spectroscopic analysis of HydG, a maturase in [FeFe]-hydrogenase H-cluster assembly
journal, January 2015
- Dinis, Pedro; Suess, Daniel L. M.; Fox, Stephen J.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 5
The [4Fe–4S]-cluster coordination of [FeFe]-hydrogenase maturation protein HydF as revealed by EPR and HYSCORE spectroscopies
journal, December 2012
- Berto, Paola; Di Valentin, Marilena; Cendron, Laura
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 12
Spectroscopic Characterization of the Bridging Amine in the Active Site of [FeFe] Hydrogenase Using Isotopologues of the H-Cluster
journal, September 2015
- Adamska-Venkatesh, Agnieszka; Roy, Souvik; Siebel, Judith F.
- Journal of the American Chemical Society, Vol. 137, Issue 40
A Selenocysteine Variant of the Human Copper Chaperone for Superoxide Dismutase. A Se-XAS Probe of Cluster Composition at the Domain 3−Domain 3 Dimer Interface †
journal, April 2008
- Barry, Amanda N.; Blackburn, Ninian J.
- Biochemistry, Vol. 47, Issue 17
Chalcogenide substitution in the [2Fe] cluster of [FeFe]-hydrogenases conserves high enzymatic activity
journal, January 2017
- Kertess, L.; Wittkamp, F.; Sommer, C.
- Dalton Transactions, Vol. 46, Issue 48
Biosynthesis of the [FeFe] Hydrogenase H Cluster: A Central Role for the Radical SAM Enzyme HydG
journal, November 2015
- Suess, Daniel L. M.; Kuchenreuther, Jon M.; De La Paz, Liliana
- Inorganic Chemistry, Vol. 55, Issue 2
H-Cluster assembly during maturation of the [FeFe]-hydrogenase
journal, June 2014
- Broderick, Joan B.; Byer, Amanda S.; Duschene, Kaitlin S.
- JBIC Journal of Biological Inorganic Chemistry, Vol. 19, Issue 6
Reaction Coordinate Leading to H 2 Production in [FeFe]-Hydrogenase Identified by Nuclear Resonance Vibrational Spectroscopy and Density Functional Theory
journal, November 2017
- Pelmenschikov, Vladimir; Birrell, James A.; Pham, Cindy C.
- Journal of the American Chemical Society, Vol. 139, Issue 46
Responses of the Fe(CN) 2 (CO) Unit to Electronic Changes as Related to Its Role in [NiFe]Hydrogenase
journal, October 1998
- Lai, Chia-Huei; Lee, Way-Zen; Miller, Matthew L.
- Journal of the American Chemical Society, Vol. 120, Issue 39
N-Substituted Derivatives of the Azadithiolate Cofactor from the [FeFe] Hydrogenases: Stability and Complexation
journal, May 2015
- Angamuthu, Raja; Chen, Chi-Shian; Cochrane, Tyler R.
- Inorganic Chemistry, Vol. 54, Issue 12
A Radical Intermediate in Tyrosine Scission to the CO and CN- Ligands of FeFe Hydrogenase
journal, October 2013
- Kuchenreuther, J. M.; Myers, W. K.; Stich, T. A.
- Science, Vol. 342, Issue 6157
CO and CN − syntheses by [FeFe]-hydrogenase maturase HydG are catalytically differentiated events
journal, December 2015
- Pagnier, Adrien; Martin, Lydie; Zeppieri, Laura
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 1
A Structural Model for [Fe]-Only Hydrogenases
journal, July 1998
- Kaasjager, Vincent E.; Henderson, Richard K.; Bouwman, Elisabeth
- Angewandte Chemie International Edition, Vol. 37, Issue 12
EPR-Derived Structure of a Paramagnetic Intermediate Generated by Biotin Synthase BioB
journal, September 2018
- Tao, Lizhi; Stich, Troy A.; Fugate, Corey J.
- Journal of the American Chemical Society, Vol. 140, Issue 40
Insights into [FeFe]-Hydrogenase Structure, Mechanism, and Maturation
journal, August 2011
- Mulder, David W.; Shepard, Eric M.; Meuser, Jonathan E.
- Structure, Vol. 19, Issue 8
Advances in synthesis of biotin and assembly of lipoic acid
journal, December 2018
- Cronan, John E.
- Current Opinion in Chemical Biology, Vol. 47
The value of enzymes in solar fuels research – efficient electrocatalysts through evolution
journal, January 2019
- Evans, Rhiannon M.; Siritanaratkul, Bhavin; Megarity, Clare F.
- Chemical Society Reviews, Vol. 48, Issue 7
Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydAΔEFG
journal, April 2010
- Mulder, David W.; Boyd, Eric S.; Sarma, Ranjana
- Nature, Vol. 465, Issue 7295
A [4Fe–4S]-Fe(CO)(CN)-l-cysteine intermediate is the first organometallic precursor in [FeFe] hydrogenase H-cluster bioassembly
journal, April 2018
- Rao, Guodong; Tao, Lizhi; Suess, Daniel L. M.
- Nature Chemistry, Vol. 10, Issue 5
Synthesis of the 2Fe subcluster of the [FeFe]-hydrogenase H cluster on the HydF scaffold
journal, May 2010
- Shepard, E. M.; McGlynn, S. E.; Bueling, A. L.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 23
Synthesis of fac-[FeII(CN)(CO)3I2]− and chemistry of the fac-[FeII(CN)x(CO)3I(3−x)]− series (x=1–3)
journal, April 2012
- Stock, Aryeh; Azran, Ofir; Garden, Benjamin
- Inorganic Chemistry Communications, Vol. 18
Preparative and structural studies on iron( ii )–thiolate cyanocarbonyls: relevance to the [NiFe]/[Fe]-hydrogenases
journal, January 2004
- Chen, Chien-Hong; Chang, Yung-Su; Yang, Chien-Yeh
- Dalton Trans., Issue 1
Hydrogenases
journal, March 2014
- Lubitz, Wolfgang; Ogata, Hideaki; Rüdiger, Olaf
- Chemical Reviews, Vol. 114, Issue 8
Cell-free H-cluster Synthesis and [FeFe] Hydrogenase Activation: All Five CO and CN− Ligands Derive from Tyrosine
journal, May 2011
- Kuchenreuther, Jon M.; George, Simon J.; Grady-Smith, Celestine S.
- PLoS ONE, Vol. 6, Issue 5