Biological Electron Transfer and Catalysis
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1 Biological Electron Transfer and Catalysis The mission of the BETCy EFRC is to define BETCy EFRC uses advanced physical the molecular mechanisms controlling techniques to delineate the molecular electron flow in coupling electrochemical and atomic determinants of factors that potential energy to chemical bond formation. support highly efficient electron transfer reactions. The studies provide a framework of design principles to advance the development of next generation catalysts. Research Team 12 PIs & 34 research personnel John Peters Montana State University & Washington State University (Director) Structure/ Biochemistry Mike Adams University of Georgia (Assoc. Director) - Biochemistry Pin-Ching Maness (Assoc. Director) Biochemistry / Physiology Paul King National Renewable Energy Laboratory - Spectroscopy Carrie Harwood University of Washington Biochemistry / Genetics Lance Seefeldt Utah State University Nitrogenase Biochemistry Anne Jones Arizona State University Direct Electrochemistry David Beratan Duke University Electron Transfer Theory Anne-Frances Miller University of Kentucky Optical Spectroscopy / Mechanism Brian Bothner - Montana State University Mass Spectrometry Eric Boyd Montana State University Informatics Ross Carlson Montana State University Modeling
2 BETCy Scientific Organization Research Thrusts Elucidating catalytic mechanisms for efficient interconversion of electrochemical potential and chemical bond energy Thrust 1 Electron Bifurcation Mechanism of coupling exergonic and endergonic electron transfer reactions by electron. Spontaneous electron transfer reaction coupled to thermodynamically unfavorable (non-spontaneous) electron transfer reaction Thrust Leaders Adams King Light Organics Thrust 2 Chemical Bond Driven Redox Chemistry Coupling chemical bond energy and electrochemical potential to achieve very low potential reductions. Harwood Seefeldt Thrust 3 Catalytic Bias Atomic level determinants of enzymatic redox properties and their relationship to catalytic bias. Preference for the forward or reverse catalytic reaction. Jones Beratan 2
3 Bifurcating Nfn NADH Dependent Ferredoxin NADP Oxidoreductase More Reduced Nfn reactions Overall reaction: -500 E (mv) e - Ferredoxin mv 2NADPH + 2Fd ox + NAD + + 2NADP + + 2Fd red + NADH NfnS NfnA e - More Oxidized NADP + /NADPH mv e - NAD + /NADH mv FAD [2Fe-2S] NfnL NfnB FAD [4Fe-4S] -200 [4Fe-4S] Bifurcating Enzymes Couple Spontaneous and Non-Spontaneous Reactions
4 Mechanism of flavin based bifurcation The site where 2-electron pairs from NADPH are bifurcated to form electrons of widely different potentials (~1 V) was identified. A short-lived (picoseconds), high energy, flavin anionic semiquinone intermediate is key to driving the endergonic reduction of ferredoxin. 1 st Ox Standard Potentials 2 nd Ox Crossed Potentials 1 st Ox 2 nd Ox 2 e - Reducing Oxidizing King Peters Jones Miller Bothner Adams Mechanistic insights into energy conservation by flavin-based electron bifurcation. Lubner et al., Nat. Chem. Biol. 13:655. DOI: /nchembio
5 A role for Marcus inversion in gating electron flow -E 2 nd electron L-FAD 7.5 Å ASQ [4Fe-4S] 9.6 Å NAD + S-FAD 8.6 Å [2Fe-2S] 14.1Å 1 st electron L-FAD HQ [4Fe-4S] Fd Beratan
6 Building Synergy - Exploiting Technical Capabilities (ETC) Innovation Award BETCy established the ETC Innovation Award to catalyze high risk/high reward research collaborations within BETCy, which in combination with monthly face-to-face videoconference meetings and technical workshops act to drive research forward. ETC award has stimulated team building and interaction and encourages proposal and idea generation from grad students and postdocs. Established in Spring 2015 by internal BETCy Progress Review Panel, Awards of supplementary travel assistance/year, open to all grad students and post docs Applicants write a 1 page proposal, awardees give a 10 minute summary talk of their work during the BETCy all hands meeting Exploiting Technical Capabilities a b John Hoben (UK/Miller) and Cara Lubner (NREL/King) investigated electron donor/acceptor pairs of flavin sites in bifurcating enzymes using transient absorption spectroscopy Data obtained to probe the mechanism of electron transfer at flavin sites of bifurcating enzymes The short-lived transient species at 365 nm (assigned to anionic semiquinone) may be a signature of bifurcating flavin sites (a). Global analysis has been initiated to aid spectral assignments using NR as a non-bifurcating model (b). Equilibrium and ultrafast kinetic studies manipulating electron transfer: a short-lived flavin semiquinone is not sufficient for electron bifurcation. Hoben, et al. J. Biol. Chem., DOI: /jbc.M
7 Light driven nitrogenase:cds hybrid turnover (min -1 ) mol MoFe protein Electrochemical potential required for N 2 activation is provided by Fe protein mediated hydrolysis of ~16 ATP ( 488 kj mol -1 or 5 ev, or ~0.62 ev/e ). CdS Nanorod e - MoFe Protein β Under illumination photoexcited CdS nanorods (orange) provide activated electrons to MoFe protein for the catalytic synthesis of NH 3. D D ox h + [8Fe-7S] 1e - N 2+ nh + FeMo-co 2NH 3 + H 2 ½ MoFe protein α mol NH 3 15x King Seefeldt illumination time (min) 0 10% 10% H2 10% 100% N 2 C 2 H 2 CO H 2 Ar 100% 90% N 2 Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid. Brown, et al. Science 352:448 DOI: /science.aaf2091
8 Building Technical Capabilities Laser Integrated EPR Enables light triggered transient spectroscopic measurements For BETCy, this unique capability provides new ways through photochemical reactions to capture reaction intermediates and measure in real time how redox active centers function in electron-transfer and energy catalysis. Enables in-situ controlled and timed optical excitation of EPR samples EPR with integrated OpoTek Radiant 355 LD pulsed laser Nanosecond pulses up to 30mJ/pulse Wavelengths from 400 to 2100 nm Synchronization of light and microwave pulses up to 10 Hz repetition rates NREL and BETCy scientists Dave Bobela and David Mulder talk about EPR and light-triggered processes at an open house showcasing the new capabilities. Photo: Dennis Schroeder, NREL
9 BETCy Talks Speaker(s) Title ID Day Time Carolyn E. Lubner NREL Electron Bifurcation Mechanistic First Principles C-I-4 Mon 4:00-4:20 pm Lubner Nguyen Yuly Diep Nguyen UGA Jonathan Yuly Duke Mechanistic insights into energy conservation by flavin-based electron bifurcation Team Science Competition A-III-1 Tue 10:40-11:00 am Jones King Anne K. Jones ASU Paul W. King NREL Oxidative Inactivation of [FeFe]-Hydrogenase as a Model for Redox Tuning of Enzyme Active Site Reactivity A-III-3 Tue 11:20-11:40 am Lance C. Seefeldt USU Caroline S. Harwood UW Light Driven N-H and C-H Bond Formation by Nitrogenase C-IV-2 Tue 1:50-2:10 pm Seefeldt Harwood 9
10 BETCy Posters Presenters Title ID Day Time Lubner Nguyen Beratan Carolyn E. Lubner, Diep M.N. Nguyen, David Beratan Physical and Thermodynamic Determinants of Flavin-Based Electron Bifurcation PI-A-4 Mon 5:00-6:30 pm Tokmina- Lukaszewska Peters Monika Tokmina- Lukaszewska, John W. Peters Nitrogenase Fe Protein Cycle PI-C-2 Mon 5:00-6:30 pm Yanning Zheng, Rhesa N. Ledbetter Fe-Nitrogenase: C-H and N-H Bond Formation PI-C-10 Mon 5:00-6:30 pm Zheng Ledbetter Artz Yuly Adams Jacob H. Artz, Jonathan L. Yuly, Michael W.W. Adams Physical and Thermodynamic Determinants of Non-Flavin Based Electron Bifurcation PII-A-2 Tue 3:30-5:00 pm S. Garrett Williams, Paul W. King Energetics of [FeS] Cluster Assemblies and Influence on Catalysis PII-C-6 Tue 3:30-5:00 pm Williams King 10
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