Integrated thermodynamic analysis of electron bifurcating [FeFe]-hydrogenase to inform anaerobic metabolism and H2 production

Jay, Zackary J.; Hunt, Kristopher A.; Chou, Katherine J.; Schut, Gerrit J.; Maness, Pin-Ching; Adams, Michael W. W.; Carlson, Ross P.

doi:10.1016/j.bbabio.2019.148087

Title: Integrated thermodynamic analysis of electron bifurcating [FeFe]-hydrogenase to inform anaerobic metabolism and H2 production

Journal Article · 31 December 2019 · Biochimica et Biophysica Acta - Bioenergetics

DOI: https://doi.org/10.1016/j.bbabio.2019.148087 · OSTI ID:1755281

Jay, Zackary J.; Hunt, Kristopher A.; Chou, Katherine J.; Schut, Gerrit J.; Maness, Pin-Ching; Adams, Michael W. W.; Carlson, Ross P.

Not Available

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0012518

OSTI ID:: 1755281

Journal Information:: Biochimica et Biophysica Acta - Bioenergetics, Journal Name: Biochimica et Biophysica Acta - Bioenergetics Journal Issue: 1 Vol. 1861; ISSN 0005-2728

Publisher:: ElsevierCopyright Statement

Country of Publication:: Netherlands

Language:: English

References (63)

Redox bifurcations: Mechanisms and importance to life now, and at its origin: A widespread means of energy conversion in biology unfolds… Nitschke, Wolfgang; Russell, Michael J. BioEssays, Vol. 34, Issue 2 https://doi.org/10.1002/bies.201100134	journal	November 2011
Thermodynamics of Reactions of Nicotinamide Adenine Dinucleotide and Nicotinamide Adenine Dinucleotide Phosphate Alberty, R. A. Archives of Biochemistry and Biophysics, Vol. 307, Issue 1 https://doi.org/10.1006/abbi.1993.1552	journal	November 1993
Standard Apparent Reduction Potentials for Biochemical Half Reactions as a Function of pH and Ionic Strength Alberty, Robert A. Archives of Biochemistry and Biophysics, Vol. 389, Issue 1 https://doi.org/10.1006/abbi.2001.2318	journal	May 2001
EPR and Redox Characterization of Ferredoxins I and II from Desulfovibrio vulgaris Miyazaki Asso, M.; Mbarki, O.; Guigliarelli, B. Biochemical and Biophysical Research Communications, Vol. 211, Issue 1 https://doi.org/10.1006/bbrc.1995.1796	journal	June 1995
Influence of temperature on energetics of hydrogen metabolism in homoacetogenic, methanogenic, and other anaerobic bacteria Conrad, Ralf; Wetter, Bettina Archives of Microbiology, Vol. 155, Issue 1 https://doi.org/10.1007/BF00291281	journal	December 1990
Contributing factors in the improvement of cellulosic H2 production in Clostridium thermocellum/Thermoanaerobacterium co-cultures Wang, Mingyu; Zhao, Qi; Li, Ling Applied Microbiology and Biotechnology, Vol. 100, Issue 19 https://doi.org/10.1007/s00253-016-7776-1	journal	August 2016
Redox thermodynamics of low-potential iron-sulfur proteins Battistuzzi, Gianantonio; D'Onofrio, Mariapina; Borsari, Marco JBIC Journal of Biological Inorganic Chemistry, Vol. 5, Issue 6 https://doi.org/10.1007/s007750000164	journal	November 2000
The value of ΔG° for the hydrolysis of ATP Rosing, J.; Slater, E. C. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 267, Issue 2 https://doi.org/10.1016/0005-2728(72)90116-8	journal	May 1972
Characterization and determination of the redox properties of the 2[4Fe-4S] ferredoxin from Methanosarcina barkeri strain MS Daas, Piet J. H.; Hagen, Wilfred R.; Keltjens, Jan T. FEBS Letters, Vol. 356, Issue 2-3 https://doi.org/10.1016/0014-5793(94)01313-6	journal	December 1994
Hyperthermophilic redox chemistry: a re-evaluation Hagedoorn, Peter L.; Driessen, Martijn C. P. F.; van den Bosch, Marieke FEBS Letters, Vol. 440, Issue 3 https://doi.org/10.1016/S0014-5793(98)01466-5	journal	December 1998
Potentiometric and electron nuclear double resonance properties of the two spin forms of the [4Fe-4S]+ cluster in the novel ferredoxin from the hyperthermophilic archaebacterium Pyrococcus furiosus. Park, J. B.; Fan, C. L.; Hoffman, B. M. Journal of Biological Chemistry, Vol. 266, Issue 29 https://doi.org/10.1016/S0021-9258(18)55004-3	journal	October 1991
Classification and phylogeny of hydrogenases Vignais, P. FEMS Microbiology Reviews, Vol. 25, Issue 4 https://doi.org/10.1016/S0168-6445(01)00063-8	journal	August 2001
Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation Buckel, Wolfgang; Thauer, Rudolf K. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2 https://doi.org/10.1016/j.bbabio.2012.07.002	journal	February 2013
The role of geochemistry and energetics in the evolution of modern respiratory complexes from a proton-reducing ancestor Schut, Gerrit J.; Zadvornyy, Oleg; Wu, Chang-Hao Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 7 https://doi.org/10.1016/j.bbabio.2016.01.010	journal	July 2016
Thermodynamics of proton transport coupled ATP synthesis Turina, Paola; Petersen, Jan; Gräber, Peter Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 6 https://doi.org/10.1016/j.bbabio.2016.02.019	journal	June 2016
[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation Peters, John W.; Schut, Gerrit J.; Boyd, Eric S. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 6 https://doi.org/10.1016/j.bbamcr.2014.11.021	journal	June 2015
Electron bifurcation Peters, John W.; Miller, Anne-Frances; Jones, Anne K. Current Opinion in Chemical Biology, Vol. 31 https://doi.org/10.1016/j.cbpa.2016.03.007	journal	April 2016
Continuous hydrogen production by the hyperthermophilic archaeon, Thermococcus kodakaraensis KOD1 Kanai, Tamotsu; Imanaka, Hiroyuki; Nakajima, Akihito Journal of Biotechnology, Vol. 116, Issue 3 https://doi.org/10.1016/j.jbiotec.2004.11.002	journal	March 2005
The energetics of metabolism in hydrothermal systems: Calculation of the standard molal thermodynamic properties of magnesium-complexed adenosine nucleotides and NAD and NADP at elevated temperatures and pressures LaRowe, Douglas E.; Helgeson, Harold C. Thermochimica Acta, Vol. 448, Issue 2 https://doi.org/10.1016/j.tca.2006.06.008	journal	September 2006
The Electron Bifurcating FixABCX Protein Complex from Azotobacter vinelandii : Generation of Low-Potential Reducing Equivalents for Nitrogenase Catalysis Ledbetter, Rhesa N.; Garcia Costas, Amaya M.; Lubner, Carolyn E. Biochemistry, Vol. 56, Issue 32 https://doi.org/10.1021/acs.biochem.7b00389	journal	August 2017
Flavin-Based Electron Bifurcation, A New Mechanism of Biological Energy Coupling Buckel, Wolfgang; Thauer, Rudolf K. Chemical Reviews, Vol. 118, Issue 7 https://doi.org/10.1021/acs.chemrev.7b00707	journal	February 2018
A Variable-Temperature Direct Electrochemical Study of Metalloproteins from Hyperthermophilic Microorganisms Involved in Hydrogen Production from Pyruvate Smith, Eugene T.; Blamey, Jenny M.; Zhou, Zhi H. Biochemistry, Vol. 34, Issue 21 https://doi.org/10.1021/bi00021a030	journal	May 1995
Effect of Iron-Sulfur Cluster Environment in Modulating the Thermodynamic Properties and Biological Function of Ferredoxin from Pyrococcus furiosus ^† Brereton, Phillip S.; Verhagen, Marc F. J. M.; Zhou, Zhi H. Biochemistry, Vol. 37, Issue 20 https://doi.org/10.1021/bi972864b	journal	May 1998
Occurrence, Classification, and Biological Function of Hydrogenases: An Overview Vignais, Paulette M.; Billoud, Bernard Chemical Reviews, Vol. 107, Issue 10, p. 4206-4272 https://doi.org/10.1021/cr050196r	journal	October 2007
The Relative Effectiveness of pH Control and Heat Treatment for Enhancing Biohydrogen Gas Production Oh, Sang-Eun; Van Ginkel, Steven; Logan, Bruce E. Environmental Science & Technology, Vol. 37, Issue 22 https://doi.org/10.1021/es034291y	journal	November 2003
Thermodynamic Evaluation on H ₂ Production in Glucose Fermentation Lee, Hyung-Sool; Salerno, Michael B.; Rittmann, Bruce E. Environmental Science & Technology, Vol. 42, Issue 7 https://doi.org/10.1021/es702610v	journal	April 2008
Oxygen activation and the conservation of energy in cell respiration Babcock, Gerald T.; Wikström, Mårten Nature, Vol. 356, Issue 6367 https://doi.org/10.1038/356301a0	journal	March 1992
Mechanistic insights into energy conservation by flavin-based electron bifurcation Lubner, Carolyn E.; Jennings, David P.; Mulder, David W. Nature Chemical Biology, Vol. 13, Issue 6 https://doi.org/10.1038/nchembio.2348	journal	April 2017
HydDB: A web tool for hydrogenase classification and analysis Søndergaard, Dan; Pedersen, Christian N. S.; Greening, Chris Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep34212	journal	September 2016
The unique features of glycolytic pathways in Archaea Verhees, Corné H.; Kengen, Servé W. M.; Tuininga, Judith E. Biochemical Journal, Vol. 375, Issue 2 https://doi.org/10.1042/bj20021472	journal	October 2003
Pathway alignment: application to the comparative analysis of glycolytic enzymes Dandekar, Thomas; Schuster, Stefan; Snel, Berend Biochemical Journal, Vol. 343, Issue 1 https://doi.org/10.1042/bj3430115	journal	September 1999
Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea Kaster, A. -K.; Moll, J.; Parey, K. Proceedings of the National Academy of Sciences, Vol. 108, Issue 7 https://doi.org/10.1073/pnas.1016761108	journal	January 2011
A simple energy-conserving system: Proton reduction coupled to proton translocation Sapra, R.; Bagramyan, K.; Adams, M. W. W. Proceedings of the National Academy of Sciences, Vol. 100, Issue 13, p. 7545-7550 https://doi.org/10.1073/pnas.1331436100	journal	June 2003
Glyceraldehyde-3-phosphate Ferredoxin Oxidoreductase, a Novel Tungsten-containing Enzyme with a Potential Glycolytic Role in the Hyperthermophilic Archaeon Pyrococcus furiosus Mukund, Swarnalatha; Adams, Michael W. W. Journal of Biological Chemistry, Vol. 270, Issue 15 https://doi.org/10.1074/jbc.270.15.8389	journal	April 1995
The Ferredoxin-dependent Conversion of Glyceraldehyde-3-phosphate in the Hyperthermophilic Archaeon Pyrococcus furiosus Represents a Novel Site of Glycolytic Regulation van der Oost, John; Schut, Gerti; Kengen, ServéW. M. Journal of Biological Chemistry, Vol. 273, Issue 43 https://doi.org/10.1074/jbc.273.43.28149	journal	October 1998
A Bacterial Electron-bifurcating Hydrogenase Schuchmann, Kai; Müller, Volker Journal of Biological Chemistry, Vol. 287, Issue 37 https://doi.org/10.1074/jbc.M112.395038	journal	July 2012
The thermophilic biomass-degrading bacterium Caldicellulosiruptor bescii utilizes two enzymes to oxidize glyceraldehyde 3-phosphate during glycolysis Scott, Israel M.; Rubinstein, Gabriel M.; Poole, Farris L. Journal of Biological Chemistry, Vol. 294, Issue 25 https://doi.org/10.1074/jbc.RA118.007120	journal	May 2019
von Bertalanffy 1.0: a COBRA toolbox extension to thermodynamically constrain metabolic models Fleming, R. M. T.; Thiele, I. Bioinformatics, Vol. 27, Issue 1 https://doi.org/10.1093/bioinformatics/btq607	journal	November 2010
eQuilibrator--the biochemical thermodynamics calculator Flamholz, A.; Noor, E.; Bar-Even, A. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr874	journal	November 2011
Desulfurococcus kamchatkensis sp. nov., a novel hyperthermophilic protein-degrading archaeon isolated from a Kamchatka hot spring Kublanov, I. V.; Bidjieva, S. Kh.; Mardanov, A. V. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 7 https://doi.org/10.1099/ijs.0.006726-0	journal	June 2009
The surprising diversity of clostridial hydrogenases: a comparative genomic perspective Calusinska, M.; Happe, T.; Joris, B. Microbiology, Vol. 156, Issue 6 https://doi.org/10.1099/mic.0.032771-0	journal	April 2010
Biological energy requirements as quantitative boundary conditions for life in the subsurface Hoehler, T. M. Geobiology, Vol. 2, Issue 4 https://doi.org/10.1111/j.1472-4677.2004.00033.x	journal	October 2004
Constructing and testing the thermodynamic limits of synthetic NAD(P)H:H ₂ pathways Veit, Andrea; Akhtar, M. Kalim; Mizutani, Taeko Microbial Biotechnology, Vol. 1, Issue 5 https://doi.org/10.1111/j.1751-7915.2008.00033.x	journal	September 2008
Methanogenic heterodisulfide reductase (HdrABC-MvhAGD) uses two noncubane [4Fe-4S] clusters for reduction Wagner, Tristan; Koch, Jürgen; Ermler, Ulrich Science, Vol. 357, Issue 6352 https://doi.org/10.1126/science.aan0425	journal	August 2017
Syntrophomonas wolfei Uses an NADH-Dependent, Ferredoxin-Independent [FeFe]-Hydrogenase To Reoxidize NADH Losey, Nathaniel A.; Mus, Florence; Peters, John W. Applied and Environmental Microbiology, Vol. 83, Issue 20 https://doi.org/10.1128/AEM.01335-17	journal	August 2017
Hydrogen Partial Pressures in a Thermophilic Acetate-Oxidizing Methanogenic Coculture Lee, Monica J.; Zinder, Stephen H. Applied and Environmental Microbiology, Vol. 54, Issue 6 https://doi.org/10.1128/AEM.54.6.1457-1461.1988	journal	January 1988
Energy conservation in chemotrophic anaerobic bacteria. Thauer, R. K.; Jungermann, K.; Decker, K. Bacteriological Reviews, Vol. 41, Issue 1 https://doi.org/10.1128/BR.41.1.100-180.1977	journal	January 1977
Complete Genome Sequence of the Cellulolytic Thermophile Clostridium thermocellum DSM1313 Feinberg, L.; Foden, J.; Barrett, T. Journal of Bacteriology, Vol. 193, Issue 11, p. 2906-2907 https://doi.org/10.1128/JB.00322-11	journal	April 2011
NADP+ Reduction with Reduced Ferredoxin and NADP+ Reduction with NADH Are Coupled via an Electron-Bifurcating Enzyme Complex in Clostridium kluyveri Wang, S.; Huang, H.; Moll, J. Journal of Bacteriology, Vol. 192, Issue 19 https://doi.org/10.1128/JB.00612-10	journal	July 2010
NADP-Specific Electron-Bifurcating [FeFe]-Hydrogenase in a Functional Complex with Formate Dehydrogenase in Clostridium autoethanogenum Grown on CO Wang, S.; Huang, H.; Kahnt, J. Journal of Bacteriology, Vol. 195, Issue 19 https://doi.org/10.1128/JB.00678-13	journal	July 2013
Energy Conservation via Electron-Transferring Flavoprotein in Anaerobic Bacteria Herrmann, G.; Jayamani, E.; Mai, G. Journal of Bacteriology, Vol. 190, Issue 3 https://doi.org/10.1128/JB.01422-07	journal	November 2007
Complete Genome Sequence of the Anaerobic, Protein-Degrading Hyperthermophilic Crenarchaeon Desulfurococcus kamchatkensis Ravin, N. V.; Mardanov, A. V.; Beletsky, A. V. Journal of Bacteriology, Vol. 191, Issue 7 https://doi.org/10.1128/JB.01525-08	journal	December 2008
The Iron-Hydrogenase of Thermotoga maritima Utilizes Ferredoxin and NADH Synergistically: a New Perspective on Anaerobic Hydrogen Production Schut, G. J.; Adams, M. W. W. Journal of Bacteriology, Vol. 191, Issue 13 https://doi.org/10.1128/JB.01582-08	journal	May 2009
Hydrogen Formation and Its Regulation in Ruminococcus albus: Involvement of an Electron-Bifurcating [FeFe]-Hydrogenase, of a Non-Electron-Bifurcating [FeFe]-Hydrogenase, and of a Putative Hydrogen-Sensing [FeFe]-Hydrogenase Zheng, Y.; Kahnt, J.; Kwon, I. H. Journal of Bacteriology, Vol. 196, Issue 22 https://doi.org/10.1128/JB.02070-14	journal	August 2014
A Reversible Electron-Bifurcating Ferredoxin- and NAD-Dependent [FeFe]-Hydrogenase (HydABC) in Moorella thermoacetica Wang, S.; Huang, H.; Kahnt, J. Journal of Bacteriology, Vol. 195, Issue 6 https://doi.org/10.1128/JB.02158-12	journal	January 2013
Carbohydrate Metabolism in Archaea: Current Insights into Unusual Enzymes and Pathways and Their Regulation Brasen, C.; Esser, D.; Rauch, B. Microbiology and Molecular Biology Reviews, Vol. 78, Issue 1 https://doi.org/10.1128/MMBR.00041-13	journal	March 2014
The complete genome sequence of Staphylothermus marinus reveals differences in sulfur metabolism among heterotrophic Crenarchaeota Anderson, Iain J.; Dharmarajan, Lakshmi; Rodriguez, Jason BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-145	journal	January 2009
Assessment of metabolic flux distribution in the thermophilic hydrogen producer Caloramator celer as affected by external pH and hydrogen partial pressure Ciranna, Alessandro; Pawar, Sudhanshu S.; Santala, Ville Microbial Cell Factories, Vol. 13, Issue 1 https://doi.org/10.1186/1475-2859-13-48	journal	January 2014
Including metabolite concentrations into flux balance analysis: thermodynamic realizability as a constraint on flux distributions in metabolic networks Hoppe, Andreas; Hoffmann, Sabrina; Holzhütter, Hermann-Georg BMC Systems Biology, Vol. 1, Issue 1 https://doi.org/10.1186/1752-0509-1-23	journal	June 2007
Elimination of hydrogenase active site assembly blocks H2 production and increases ethanol yield in Clostridium thermocellum Biswas, Ranjita; Zheng, Tianyong; Olson, Daniel G. Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0204-4	journal	January 2015
Syntrophic Acetate-Oxidizing Microbes in Methanogenic Environments Hattori, Satoshi Microbes and Environments, Vol. 23, Issue 2 https://doi.org/10.1264/jsme2.23.118	journal	January 2008
How important is thermodynamics for identifying elementary flux modes? Peres, Sabine; Jolicœur, Mario; Moulin, Cécile PLOS ONE, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pone.0171440	journal	February 2017
Flavin-Based Electron Bifurcation, Ferredoxin, Flavodoxin, and Anaerobic Respiration With Protons (Ech) or NAD+ (Rnf) as Electron Acceptors: A Historical Review Buckel, Wolfgang; Thauer, Rudolf K. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00401	journal	March 2018

Similar Records

Integrated Thermodynamic Analysis of Electron Bifurcating [FeFe]-Hydrogenase to Inform Anaerobic Metabolism and H2 Production

Journal Article · 2019 · BBA Bioenergetics · OSTI ID:1580025

Jay, Zackary J.; Hunt, Kristopher A.; Chou, Katherine J; +4 more

The Beta Subunit of Non-bifurcating NADH-Dependent [FeFe]-Hydrogenases Differs From Those of Multimeric Electron-Bifurcating [FeFe]-Hydrogenases

Journal Article · 2020 · Frontiers in Microbiology · OSTI ID:1633663

Losey, Nathaniel A.; Poudel, Saroj; Boyd, Eric S.; +1 more

System analysis and improved [FeFe] hydrogenase O2 tolerance suggest feasibility for photosynthetic H2 production

Journal Article · 2018 · Metabolic Engineering · OSTI ID:1694028

Koo, Jamin; Swartz, James R.

Title: Integrated thermodynamic analysis of electron bifurcating [FeFe]-hydrogenase to inform anaerobic metabolism and H2 production

Citation Formats

References (63)

Similar Records

Related Subjects