New Insights into [FeFe] Hydrogenase Activation and Maturase Function
Abstract
[FeFe] hydrogenases catalyze H2 production using the H-cluster, an iron-sulfur cofactor that contains carbon monoxide (CO), cyanide (CN–), and a dithiolate bridging ligand. The HydE, HydF, and HydG maturases assist in assembling the H-cluster and maturing hydrogenases into their catalytically active form. Characterization of these maturases and in vitro hydrogenase activation methods have helped elucidate steps in the H-cluster biosynthetic pathway such as the HydG-catalyzed generation of the CO and CN– ligands from free tyrosine. We have refined our cell-free approach for H-cluster synthesis and hydrogenase maturation by using separately expressed and purified HydE, HydF, and HydG. In this report, we illustrate how substrates and protein constituents influence hydrogenase activation, and for the first time, we show that each maturase can function catalytically during the maturation process. With precise control over the biomolecular components, we also provide evidence for H-cluster synthesis in the absence of either HydE or HydF, and we further show that hydrogenase activation can occur without exogenous tyrosine. Given these findings, we suggest a new reaction sequence for the [FeFe] hydrogenase maturation pathway. In our model, HydG independently synthesizes an iron-based compound with CO and CN– ligands that is a precursor to the H-cluster [2Fe]H subunit, andmore »
- Authors:
-
- Stanford Univ., CA (United States); Univ. of California, Davis, CA (United States)
- Univ. of California, Davis, CA (United States)
- Stanford Univ., CA (United States)
- Publication Date:
- Research Org.:
- Stanford Univ., CA (United States); Univ. of California, Davis, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Materials Sciences & Engineering Division (MSE)
- OSTI Identifier:
- 1904544
- Grant/Contract Number:
- SC0002010; SC0004334; FG02-09ER46632
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 7; Journal Issue: 9; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; tyrosine; electron spin resonance spectroscopy; chemical synthesis; biochemical cofactors; cysteine; small molecules; chemical radicals; enzymes
Citation Formats
Kuchenreuther, Jon M., Britt, R. David, and Swartz, James R. New Insights into [FeFe] Hydrogenase Activation and Maturase Function. United States: N. p., 2012.
Web. doi:10.1371/journal.pone.0045850.
Kuchenreuther, Jon M., Britt, R. David, & Swartz, James R. New Insights into [FeFe] Hydrogenase Activation and Maturase Function. United States. https://doi.org/10.1371/journal.pone.0045850
Kuchenreuther, Jon M., Britt, R. David, and Swartz, James R. Tue .
"New Insights into [FeFe] Hydrogenase Activation and Maturase Function". United States. https://doi.org/10.1371/journal.pone.0045850. https://www.osti.gov/servlets/purl/1904544.
@article{osti_1904544,
title = {New Insights into [FeFe] Hydrogenase Activation and Maturase Function},
author = {Kuchenreuther, Jon M. and Britt, R. David and Swartz, James R.},
abstractNote = {[FeFe] hydrogenases catalyze H2 production using the H-cluster, an iron-sulfur cofactor that contains carbon monoxide (CO), cyanide (CN–), and a dithiolate bridging ligand. The HydE, HydF, and HydG maturases assist in assembling the H-cluster and maturing hydrogenases into their catalytically active form. Characterization of these maturases and in vitro hydrogenase activation methods have helped elucidate steps in the H-cluster biosynthetic pathway such as the HydG-catalyzed generation of the CO and CN– ligands from free tyrosine. We have refined our cell-free approach for H-cluster synthesis and hydrogenase maturation by using separately expressed and purified HydE, HydF, and HydG. In this report, we illustrate how substrates and protein constituents influence hydrogenase activation, and for the first time, we show that each maturase can function catalytically during the maturation process. With precise control over the biomolecular components, we also provide evidence for H-cluster synthesis in the absence of either HydE or HydF, and we further show that hydrogenase activation can occur without exogenous tyrosine. Given these findings, we suggest a new reaction sequence for the [FeFe] hydrogenase maturation pathway. In our model, HydG independently synthesizes an iron-based compound with CO and CN– ligands that is a precursor to the H-cluster [2Fe]H subunit, and which we have termed HydG-co. We further propose that HydF is a transferase that stabilizes HydG-co and also shuttles the complete [2Fe]H subcluster to the hydrogenase, a translocation process that may be catalyzed by HydE. In summary, this report describes the first example of reconstructing the [FeFe] hydrogenase maturation pathway using purified maturases and subsequently utilizing this in vitro system to better understand the roles of HydE, HydF, and HydG.},
doi = {10.1371/journal.pone.0045850},
journal = {PLoS ONE},
number = 9,
volume = 7,
place = {United States},
year = {Tue Sep 25 00:00:00 EDT 2012},
month = {Tue Sep 25 00:00:00 EDT 2012}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
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:
[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
Further Characterization of the [FeFe]-Hydrogenase Maturase HydG
journal, February 2011
- Tron, Cécile; Cherrier, Mickaël V.; Amara, Patricia
- European Journal of Inorganic Chemistry, Vol. 2011, Issue 7
Biochemical characterization of the HydE and HydG iron-only hydrogenase maturation enzymes from Thermatoga maritima
journal, August 2005
- Rubach, Jon K.; Brazzolotto, Xavier; Gaillard, Jacques
- FEBS Letters, Vol. 579, Issue 22
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
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
The [FeFe]-hydrogenase maturase HydF from Clostridium acetobutylicum contains a CO and CN − ligated iron cofactor
journal, December 2009
- Czech, Ilka; Silakov, Alexey; Lubitz, Wolfgang
- FEBS Letters, Vol. 584, Issue 3
A glycyl free radical as the precursor in the synthesis of carbon monoxide and cyanide by the [FeFe]-hydrogenase maturase HydG
journal, September 2010
- Nicolet, Yvain; Martin, Lydie; Tron, Cécile
- FEBS Letters, Vol. 584, Issue 19
Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center
journal, January 1999
- Nicolet, Yvain; Piras, Claudine; Legrand, Pierre
- Structure, Vol. 7, Issue 1, p. 13-23
Identification of Lysine 346 as a Functionally Important Residue for Pyridoxal 5‘-Phosphate Binding and Catalysis in Lysine 2,3-Aminomutase from Bacillus subtilis †
journal, January 2001
- Chen, Dawei; Frey, Perry A.
- Biochemistry, Vol. 40, Issue 2
Mechanism of Cysteine Desulfurase Slr0387 from Synechocystis sp. PCC 6803: Kinetic Analysis of Cleavage of the Persulfide Intermediate by Chemical Reductants
journal, September 2004
- Behshad, Elham; Parkin, Sara E.; Bollinger, J. Martin
- Biochemistry, Vol. 43, Issue 38
HscA and HscB Stimulate [2Fe-2S] Cluster Transfer from IscU to Apoferredoxin in an ATP-Dependent Reaction †
journal, September 2006
- Chandramouli, Kala; Johnson, Michael K.
- Biochemistry, Vol. 45, Issue 37
Formation and Properties of [4Fe-4S] Clusters on the IscU Scaffold Protein †
journal, June 2007
- Chandramouli, Kala; Unciuleac, Mihaela-Carmen; Naik, Sunil
- Biochemistry, Vol. 46, Issue 23
Pyrroloquinoline Quinone Biogenesis: Demonstration That PqqE from Klebsiella pneumoniae Is a Radical S -Adenosyl- l -methionine Enzyme
journal, October 2009
- Wecksler, Stephen R.; Stoll, Stefan; Tran, Ha
- Biochemistry, Vol. 48, Issue 42
[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
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
Quantum Refinement of [FeFe] Hydrogenase Indicates a Dithiomethylamine Ligand
journal, April 2010
- Ryde, Ulf; Greco, Claudio; De Gioia, Luca
- Journal of the American Chemical Society, Vol. 132, Issue 13
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
NifB-dependent in vitro synthesis of the iron-molybdenum cofactor of nitrogenase
journal, March 2006
- Curatti, L.; Ludden, P. W.; Rubio, L. M.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 14
In vitro synthesis of the iron molybdenum cofactor of nitrogenase from iron, sulfur, molybdenum, and homocitrate using purified proteins
journal, October 2007
- Curatti, L.; Hernandez, J. A.; Igarashi, R. Y.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 45
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
Spectroscopic studies of ferricyanide oxidation of Azotobacter vinelandii ferredoxin I.
journal, April 1984
- Morgan, T. V.; Stephens, P. J.; Devlin, F.
- Proceedings of the National Academy of Sciences, Vol. 81, Issue 7
The Requirement of Reductant for in Vitro Biosynthesis of the Iron-Molybdenum Cofactor of Nitrogenase
journal, February 1996
- Allen, Ronda M.; Chatterjee, Ranjini; Ludden, Paul W.
- Journal of Biological Chemistry, Vol. 271, Issue 8
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
The [Fe-Fe]-Hydrogenase Maturation Protein HydF from Thermotoga maritima Is a GTPase with an Iron-Sulfur Cluster
journal, November 2005
- Brazzolotto, Xavier; Rubach, Jon K.; Gaillard, Jacques
- Journal of Biological Chemistry, Vol. 281, Issue 2
Interplay of IscA and IscU in Biogenesis of Iron-Sulfur Clusters
journal, September 2006
- Yang, Juanjuan; Bitoun, Jacob P.; Ding, Huangen
- Journal of Biological Chemistry, Vol. 281, Issue 38
Lysine 2,3‐aminomutase: is adenosylmethionine a poor man's adenosylcobalamin?
journal, May 1993
- Frey, Perry A.
- The FASEB Journal, Vol. 7, Issue 8
Similarities in the Architecture of the Active Sites of Ni-Hydrogenases and Fe-Hydrogenases Detected by Means of Infrared Spectroscopy
journal, May 1996
- Spek, Trienke M.; Arendsen, Alexander F.; Happe, Randolph P.
- European Journal of Biochemistry, Vol. 237, Issue 3
Pyridoxal Phosphate Enzymes: Mechanistic, Structural, and Evolutionary Considerations
journal, June 2004
- Eliot, Andrew C.; Kirsch, Jack F.
- Annual Review of Biochemistry, Vol. 73, Issue 1
Tyrosine, Cysteine, and S-Adenosyl Methionine Stimulate In Vitro [FeFe] Hydrogenase Activation
journal, October 2009
- Kuchenreuther, Jon M.; Stapleton, James A.; Swartz, James R.
- PLoS ONE, Vol. 4, Issue 10
High-Yield Expression of Heterologous [FeFe] Hydrogenases in Escherichia coli
journal, November 2010
- Kuchenreuther, Jon M.; Grady-Smith, Celestine S.; Bingham, Alyssa S.
- PLoS ONE, Vol. 5, Issue 11
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
Works referencing / citing this record:
[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
Electron Spin Relaxation and Biochemical Characterization of the Hydrogenase Maturase HydF: Insights into [2Fe-2S] and [4Fe-4S] Cluster Communication and Hydrogenase Activation
journal, May 2017
- Shepard, Eric M.; Byer, Amanda S.; Aggarwal, Priyanka
- Biochemistry, Vol. 56, Issue 25
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
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