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Title: Compositional and structural insights into the nature of the H-cluster precursor on HydF

Abstract

Spectroscopic and computational characterization of loaded HydF reveals that the 2Fe subcluster is a coordinatively saturated Fe( i )–Fe( i ) species that contains 4 CO and 2 CN ligands, and is anchored to HydF via coordination to a [4Fe–4S] cluster.

Authors:
 [1]; ORCiD logo [1];  [2];  [2];  [1]; ORCiD logo [2];  [1];  [1]; ORCiD logo [1]
  1. Montana State Univ., Bozeman, MT (United States)
  2. National Renewable Energy Lab. (NREL), Golden, CO (United States)
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1466185
Alternate Identifier(s):
OSTI ID: 1458586
Report Number(s):
NREL/JA-2700-71169
Journal ID: ISSN 1477-9226; ICHBD9
Grant/Contract Number:  
AC36-08GO28308; AC36-08-GO28308; SC0005404
Resource Type:
Accepted Manuscript
Journal Name:
Dalton Transactions
Additional Journal Information:
Journal Volume: 47; Journal Issue: 28; Journal ID: ISSN 1477-9226
Publisher:
Royal Society of Chemistry
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; [FeFe]-hydrogenases; spectroscopy

Citation Formats

Scott, Anna G., Szilagyi, Robert K., Mulder, David W., Ratzloff, Michael W., Byer, Amanda S., King, Paul W., Broderick, William E., Shepard, Eric M., and Broderick, Joan B. Compositional and structural insights into the nature of the H-cluster precursor on HydF. United States: N. p., 2018. Web. doi:10.1039/C8DT01654B.
Scott, Anna G., Szilagyi, Robert K., Mulder, David W., Ratzloff, Michael W., Byer, Amanda S., King, Paul W., Broderick, William E., Shepard, Eric M., & Broderick, Joan B. Compositional and structural insights into the nature of the H-cluster precursor on HydF. United States. doi:https://doi.org/10.1039/C8DT01654B
Scott, Anna G., Szilagyi, Robert K., Mulder, David W., Ratzloff, Michael W., Byer, Amanda S., King, Paul W., Broderick, William E., Shepard, Eric M., and Broderick, Joan B. Tue . "Compositional and structural insights into the nature of the H-cluster precursor on HydF". United States. doi:https://doi.org/10.1039/C8DT01654B. https://www.osti.gov/servlets/purl/1466185.
@article{osti_1466185,
title = {Compositional and structural insights into the nature of the H-cluster precursor on HydF},
author = {Scott, Anna G. and Szilagyi, Robert K. and Mulder, David W. and Ratzloff, Michael W. and Byer, Amanda S. and King, Paul W. and Broderick, William E. and Shepard, Eric M. and Broderick, Joan B.},
abstractNote = {Spectroscopic and computational characterization of loaded HydF reveals that the 2Fe subcluster is a coordinatively saturated Fe( i )–Fe( i ) species that contains 4 CO and 2 CN ligands, and is anchored to HydF via coordination to a [4Fe–4S] cluster.},
doi = {10.1039/C8DT01654B},
journal = {Dalton Transactions},
number = 28,
volume = 47,
place = {United States},
year = {2018},
month = {6}
}

Journal Article:
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Cited by: 2 works
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Figures / Tables:

Figure 1 Figure 1: Overview of computational models for the [2Fe]F subcluster in HydFEG considered in the given work.

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Works referenced in this record:

[FeFe]-Hydrogenase Cyanide Ligands Derived From S-Adenosylmethionine-Dependent Cleavage of Tyrosine
journal, January 2010

  • Driesener, Rebecca C.; Challand, Martin R.; McGlynn, Shawn E.
  • Angewandte Chemie International Edition, Vol. 49, Issue 9
  • DOI: 10.1002/anie.200907047

On the accuracy of density functional theory for iron—sulfur clusters
journal, January 2006

  • Szilagyi, Robert K.; Winslow, Mark A.
  • Journal of Computational Chemistry, Vol. 27, Issue 12
  • DOI: 10.1002/jcc.20449

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
  • DOI: 10.1038/nchembio.2385

Iron Carbonyl Sulfides, Formaldehyde, and Amines Condense To Give the Proposed Azadithiolate Cofactor of the Fe-Only Hydrogenases
journal, February 2002

  • Li, Hongxiang; Rauchfuss, Thomas B.
  • Journal of the American Chemical Society, Vol. 124, Issue 5
  • DOI: 10.1021/ja016964n

Biomimetic assembly and activation of [FeFe]-hydrogenases
journal, June 2013

  • Berggren, G.; Adamska, A.; Lambertz, C.
  • Nature, Vol. 499, Issue 7456
  • DOI: 10.1038/nature12239

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
  • DOI: 10.1021/jacs.5b12512

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
  • DOI: 10.1038/nchem.2490

In vitro activation of [FeFe] hydrogenase: new insights into hydrogenase maturation
journal, March 2007

  • McGlynn, Shawn E.; Ruebush, Shane S.; Naumov, Anatoli
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 12, Issue 4
  • DOI: 10.1007/s00775-007-0224-z

An EPR/HYSCORE, Mössbauer, and resonance Raman study of the hydrogenase maturation enzyme HydF: a model for N-coordination to [4Fe–4S] clusters
journal, November 2013

  • Berggren, Gustav; Garcia-Serres, Ricardo; Brazzolotto, Xavier
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 19, Issue 1
  • DOI: 10.1007/s00775-013-1062-9

Biochemical characterization of the HydE and HydG iron-only hydrogenase maturation enzymes from Thermatoga maritima
journal, August 2005


Probing the Solvent Accessibility of the [4Fe–4S] Cluster of the Hydrogenase Maturation Protein HydF from Thermotoga neapolitana by HYSCORE and 3p-ESEEM
journal, April 2015

  • Albertini, Marco; Berto, Paola; Vallese, Francesca
  • The Journal of Physical Chemistry B, Vol. 119, Issue 43
  • DOI: 10.1021/acs.jpcb.5b03110

Targeting Intermediates of [FeFe]-Hydrogenase by CO and CN Vibrational Signatures
journal, May 2011

  • Yu, Lian; Greco, Claudio; Bruschi, Maurizio
  • Inorganic Chemistry, Vol. 50, Issue 9
  • DOI: 10.1021/ic102039z

[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
  • DOI: 10.1016/j.bbamcr.2014.11.021

[FeFe]-Hydrogenase Maturation
journal, June 2014

  • Shepard, Eric M.; Mus, Florence; Betz, Jeremiah N.
  • Biochemistry, Vol. 53, Issue 25
  • DOI: 10.1021/bi500210x

Discovery of Two Novel Radical S -Adenosylmethionine Proteins Required for the Assembly of an Active [Fe] Hydrogenase
journal, April 2004

  • Posewitz, Matthew C.; King, Paul W.; Smolinski, Sharon L.
  • Journal of Biological Chemistry, Vol. 279, Issue 24
  • DOI: 10.1074/jbc.M403206200

Hydrogenase Enzymes and Their Synthetic Models: The Role of Metal Hydrides
journal, June 2016


New Insights into [FeFe] Hydrogenase Activation and Maturase Function
journal, September 2012


Metallocofactor assembly for [FeFe]-hydrogenases
journal, December 2016

  • Dinis, Pedro; Wieckowski, Beata M.; Roach, Peter L.
  • Current Opinion in Structural Biology, Vol. 41
  • DOI: 10.1016/j.sbi.2016.06.004

From Enzyme Maturation to Synthetic Chemistry: The Case of Hydrogenases
journal, July 2015


COSMO: a new approach to dielectric screening in solvents with explicit expressions for the screening energy and its gradient
journal, January 1993


First Generation Analogues of the Binuclear Site in the Fe-Only Hydrogenases:  Fe 2 (μ-SR) 2 (CO) 4 (CN) 2 2 -
journal, October 1999

  • Schmidt, Michael; Contakes, Stephen M.; Rauchfuss, Thomas B.
  • Journal of the American Chemical Society, Vol. 121, Issue 41
  • DOI: 10.1021/ja9924187

EPR and FTIR Analysis of the Mechanism of H 2 Activation by [FeFe]-Hydrogenase HydA1 from Chlamydomonas reinhardtii
journal, April 2013

  • Mulder, David W.; Ratzloff, Michael W.; Shepard, Eric M.
  • Journal of the American Chemical Society, Vol. 135, Issue 18
  • DOI: 10.1021/ja4000257

Identification and Characterization of the “Super-Reduced” State of the H-Cluster in [FeFe] Hydrogenase: A New Building Block for the Catalytic Cycle?
journal, October 2012

  • Adamska, Agnieszka; Silakov, Alexey; Lambertz, Camilla
  • Angewandte Chemie International Edition, Vol. 51, Issue 46
  • DOI: 10.1002/anie.201204800

[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
  • DOI: 10.1021/bi501205e

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
  • DOI: 10.1007/s00775-014-1168-8

Activation of HydA ΔEFG Requires a Preformed [4Fe-4S] Cluster
journal, July 2009

  • Mulder, David W.; Ortillo, Danilo O.; Gardenghi, David J.
  • Biochemistry, Vol. 48, Issue 26
  • DOI: 10.1021/bi9000563

Stepwise isotope editing of [FeFe]-hydrogenases exposes cofactor dynamics
journal, July 2016

  • Senger, Moritz; Mebs, Stefan; Duan, Jifu
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 30
  • DOI: 10.1073/pnas.1606178113

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
  • DOI: 10.1038/nature08993

Electrochemical Investigations of the Mechanism of Assembly of the Active-Site H-Cluster of [FeFe]-Hydrogenases
journal, November 2016

  • Megarity, Clare F.; Esselborn, Julian; Hexter, Suzannah V.
  • Journal of the American Chemical Society, Vol. 138, Issue 46
  • DOI: 10.1021/jacs.6b09366

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
  • DOI: 10.1073/pnas.1001937107

Cell-free H-cluster Synthesis and [FeFe] Hydrogenase Activation: All Five CO and CN− Ligands Derive from Tyrosine
journal, May 2011


Iron-sulfur cluster coordination in the [FeFe]-hydrogenase H cluster biosynthetic factor HydF
journal, October 2012


Reversible H Atom Abstraction Catalyzed by the Radical S -Adenosylmethionine Enzyme HydG
journal, September 2014

  • Duffus, Benjamin R.; Ghose, Shourjo; Peters, John W.
  • Journal of the American Chemical Society, Vol. 136, Issue 38
  • DOI: 10.1021/ja504618y

Long-range corrected hybrid density functionals with damped atom–atom dispersion corrections
journal, January 2008

  • Chai, Jeng-Da; Head-Gordon, Martin
  • Physical Chemistry Chemical Physics, Vol. 10, Issue 44
  • DOI: 10.1039/b810189b

The role of the maturase HydG in [FeFe]‐hydrogenase active site synthesis and assembly
journal, January 2009


Carbon Monoxide and Cyanide as Intrinsic Ligands to Iron in the Active Site of [NiFe]-Hydrogenases: NiFe(CN)
journal, February 1999

  • Pierik, Antonio J.; Roseboom, Winfried; Happe, Randolph P.
  • Journal of Biological Chemistry, Vol. 274, Issue 6
  • DOI: 10.1074/jbc.274.6.3331

Refining the Active Site Structure of Iron−Iron Hydrogenase Using Computational Infrared Spectroscopy
journal, April 2008

  • Tye, Jesse W.; Darensbourg, Marcetta Y.; Hall, Michael B.
  • Inorganic Chemistry, Vol. 47, Issue 7
  • DOI: 10.1021/ic7013732

The Electronic Structure of the H-Cluster in the [FeFe]-Hydrogenase from Desulfovibrio desulfuricans : A Q-band 57 Fe-ENDOR and HYSCORE Study
journal, September 2007

  • Silakov, Alexey; Reijerse, Eduard J.; Albracht, Simon P. J.
  • Journal of the American Chemical Society, Vol. 129, Issue 37
  • DOI: 10.1021/ja072592s

[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
  • DOI: 10.1021/ja1012273

Advanced Electron Paramagnetic Resonance and Density Functional Theory Study of a {2Fe3S} Cluster Mimicking the Active Site of [FeFe] Hydrogenase
journal, December 2010

  • Silakov, Alexey; Shaw, Jennifer L.; Reijerse, Eduard J.
  • Journal of the American Chemical Society, Vol. 132, Issue 49
  • DOI: 10.1021/ja107793e

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
  • DOI: 10.1021/bi401143s

Characterization of the [FeFe]-Hydrogenase Maturation Protein HydF by EPR Techniques: Insights into the Catalytic Mechanism
journal, July 2015


Radical S -Adenosyl-l-methionine Chemistry in the Synthesis of Hydrogenase and Nitrogenase Metal Cofactors
journal, December 2014

  • Byer, Amanda S.; Shepard, Eric M.; Peters, John W.
  • Journal of Biological Chemistry, Vol. 290, Issue 7
  • DOI: 10.1074/jbc.R114.578161

X-ray Structure of the [FeFe]-Hydrogenase Maturase HydE from Thermotoga maritima
journal, April 2008

  • Nicolet, Yvain; Rubach, Jon K.; Posewitz, Matthew C.
  • Journal of Biological Chemistry, Vol. 283, Issue 27
  • DOI: 10.1074/jbc.M801161200

Spontaneous activation of [FeFe]-hydrogenases by an inorganic [2Fe] active site mimic
journal, August 2013

  • Esselborn, Julian; Lambertz, Camilla; Adamska-Venkatesh, Agnieszka
  • Nature Chemical Biology, Vol. 9, Issue 10
  • DOI: 10.1038/nchembio.1311

A low-spin iron with CN and CO as intrinsic ligands forms the core of the active site in [Fe]-hydrogenases
journal, December 1998


A Redox Active [2Fe-2S] Cluster on the Hydrogenase Maturase HydF
journal, June 2016


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
  • DOI: 10.1073/pnas.1508440112

Spectroelectrochemical Characterization of the Active Site of the [FeFe] Hydrogenase HydA1 from Chlamydomonas reinhardtii
journal, August 2009

  • Silakov, Alexey; Kamp, Christina; Reijerse, Eduard
  • Biochemistry, Vol. 48, Issue 33
  • DOI: 10.1021/bi9009105

The HydG Enzyme Generates an Fe(CO)2(CN) Synthon in Assembly of the FeFe Hydrogenase H-Cluster
journal, January 2014


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
  • DOI: 10.1021/ic0261225

HydF as a scaffold protein in [FeFe] hydrogenase H-cluster biosynthesis
journal, May 2008


Dithiomethylether as a Ligand in the Hydrogenase H-Cluster
journal, April 2008

  • Pandey, Arti S.; Harris, Travis V.; Giles, Logan J.
  • Journal of the American Chemical Society, Vol. 130, Issue 13
  • DOI: 10.1021/ja711187e

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
  • DOI: 10.1073/pnas.1417252112

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
  • DOI: 10.1016/j.bbabio.2012.09.004

Iron–Sulfur Cluster States of the Hydrogenase Maturase HydF
journal, August 2017


Correlation between computed gas-phase and experimentally determined solution-phase infrared spectra: Models of the iron–iron hydrogenase enzyme active site
journal, January 2006

  • Tye, Jesse W.; Darensbourg, Marcetta Y.; Hall, Michael B.
  • Journal of Computational Chemistry, Vol. 27, Issue 12
  • DOI: 10.1002/jcc.20456

The [FeFe]-hydrogenase maturation protein HydF contains a H-cluster like [4Fe4S]-2Fe site
journal, December 2010


EasySpin, a comprehensive software package for spectral simulation and analysis in EPR
journal, January 2006


Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center
journal, January 1999


Fully optimized contracted Gaussian basis sets of triple zeta valence quality for atoms Li to Kr
journal, April 1994

  • Schäfer, Ansgar; Huber, Christian; Ahlrichs, Reinhart
  • The Journal of Chemical Physics, Vol. 100, Issue 8
  • DOI: 10.1063/1.467146

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
  • DOI: 10.1073/pnas.1515842113

On the electronic structure of the hydrogenase H-cluster
journal, January 2006

  • Schwab, David E.; Tard, Cedric; Brecht, Eric
  • Chemical Communications, Issue 35
  • DOI: 10.1039/b604994j

Functional Studies of [FeFe] Hydrogenase Maturation in an Escherichia coli Biosynthetic System
journal, March 2006


The proton iron-sulfur cluster environment of the [FeFe]-hydrogenase maturation protein HydF from Thermotoga neapolitana
journal, October 2014

  • Albertini, Marco; Vallese, Francesca; Di Valentin, Marilena
  • International Journal of Hydrogen Energy, Vol. 39, Issue 32
  • DOI: 10.1016/j.ijhydene.2013.12.164

Hydrogenases
journal, March 2014

  • Lubitz, Wolfgang; Ogata, Hideaki; Rüdiger, Olaf
  • Chemical Reviews, Vol. 114, Issue 8
  • DOI: 10.1021/cr4005814

The [FeFe]-hydrogenase maturase HydF from Clostridium acetobutylicum contains a CO and CN ligated iron cofactor
journal, December 2009


Multi-edge X-ray Absorption Spectroscopy. 1. X-ray Absorption near-Edge Structure Analysis of a Biomimetic Model of FeFe-Hydrogenase
journal, December 2012

  • Giles, Logan J.; Grigoropoulos, Alexios; Szilagyi, Robert K.
  • The Journal of Physical Chemistry A, Vol. 116, Issue 50
  • DOI: 10.1021/jp303932k

    Works referencing / citing this record:

    Monitoring H-cluster assembly using a semi-synthetic HydF protein
    journal, January 2019

    • Németh, Brigitta; Esmieu, Charlène; Redman, Holly J.
    • Dalton Transactions, Vol. 48, Issue 18
    • DOI: 10.1039/c8dt04294b

    Overview of the Maturation Machinery of the H-Cluster of [FeFe]-Hydrogenases with a Focus on HydF
    journal, October 2018

    • Bortolus, Marco; Costantini, Paola; Doni, Davide
    • International Journal of Molecular Sciences, Vol. 19, Issue 10
    • DOI: 10.3390/ijms19103118

      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.