The catalytic mechanism of electron-bifurcating electron transfer flavoproteins (ETFs) involves an intermediary complex with NAD+
Abstract
Electron bifurcation plays a key role in anaerobic energy metabolism but it is a relatively new discovery and only limited mechanistic information is available on the diverse enzymes that employ it. Herein, we focused on the bifurcating electron transfer flavoprotein (ETF) from the hyperthermophilic archaeon Pyrobaculum aerophilum. The EtfABCX enzyme complex couples NADH oxidation to the endergonic reduction of ferredoxin and exergonic reduction of menaquinone. We developed a model for the enzyme structure by using non-denaturing MS, cross-linking and homology modeling in which EtfA, B, and C each contained FAD, whereas EtfX contained two [4Fe-4S] clusters. On the basis of analyses using transient absorption, EPR and optical titrations with NADH or inorganic reductants with and without NAD+, we propose a catalytic cycle involving formation of an intermediary NAD+-bound complex. A charge transfer signal revealed an intriguing interplay of flavin semiquinones and a protein conformational change that gated electron transfer between the low- and high-potential pathways. We found that despite a common bifurcating flavin site, the proposed EtfABCX catalytic cycle is distinct from that of the genetically-unrelated bifurcating NADH-dependent ferredoxin NADP+ oxidoreductase (NfnI). The two enzymes particularly differed in the role of NAD+, the resting and bifurcating-ready states of the enzymes,more »
- Publication Date:
- Research Org.:
- Energy Frontier Research Centers (EFRC) (United States). Center for Biological Electron Transfer and Catalysis (BETCy); National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1769438
- Alternate Identifier(s):
- OSTI ID: 1490994
- Report Number(s):
- NREL/JA-2700-72604
Journal ID: ISSN 0021-9258; S0021925820392589; PII: S0021925820392589
- Grant/Contract Number:
- AC36-08GO28308
- Resource Type:
- Published Article
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Name: Journal of Biological Chemistry Journal Volume: 294 Journal Issue: 9; Journal ID: ISSN 0021-9258
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; bifurcation; electron paramagnetic resonance (EPR); electron transport; flavoprotein archaea; extreme thermophile; bioenergetics; flavin; radical
Citation Formats
Schut, Gerrit J., Mohamed-Raseek, Nishya, Tokmina-Lukaszewska, Monika, Mulder, David W., Nguyen, Diep M. N., Lipscomb, Gina L., Hoben, John P., Patterson, Angela, Lubner, Carolyn E., King, Paul W., Peters, John W., Bothner, Brian, Miller, Anne-Frances, and Adams, Michael W. W. The catalytic mechanism of electron-bifurcating electron transfer flavoproteins (ETFs) involves an intermediary complex with NAD+. United States: N. p., 2019.
Web. doi:10.1074/jbc.RA118.005653.
Schut, Gerrit J., Mohamed-Raseek, Nishya, Tokmina-Lukaszewska, Monika, Mulder, David W., Nguyen, Diep M. N., Lipscomb, Gina L., Hoben, John P., Patterson, Angela, Lubner, Carolyn E., King, Paul W., Peters, John W., Bothner, Brian, Miller, Anne-Frances, & Adams, Michael W. W. The catalytic mechanism of electron-bifurcating electron transfer flavoproteins (ETFs) involves an intermediary complex with NAD+. United States. https://doi.org/10.1074/jbc.RA118.005653
Schut, Gerrit J., Mohamed-Raseek, Nishya, Tokmina-Lukaszewska, Monika, Mulder, David W., Nguyen, Diep M. N., Lipscomb, Gina L., Hoben, John P., Patterson, Angela, Lubner, Carolyn E., King, Paul W., Peters, John W., Bothner, Brian, Miller, Anne-Frances, and Adams, Michael W. W. Fri .
"The catalytic mechanism of electron-bifurcating electron transfer flavoproteins (ETFs) involves an intermediary complex with NAD+". United States. https://doi.org/10.1074/jbc.RA118.005653.
@article{osti_1769438,
title = {The catalytic mechanism of electron-bifurcating electron transfer flavoproteins (ETFs) involves an intermediary complex with NAD+},
author = {Schut, Gerrit J. and Mohamed-Raseek, Nishya and Tokmina-Lukaszewska, Monika and Mulder, David W. and Nguyen, Diep M. N. and Lipscomb, Gina L. and Hoben, John P. and Patterson, Angela and Lubner, Carolyn E. and King, Paul W. and Peters, John W. and Bothner, Brian and Miller, Anne-Frances and Adams, Michael W. W.},
abstractNote = {Electron bifurcation plays a key role in anaerobic energy metabolism but it is a relatively new discovery and only limited mechanistic information is available on the diverse enzymes that employ it. Herein, we focused on the bifurcating electron transfer flavoprotein (ETF) from the hyperthermophilic archaeon Pyrobaculum aerophilum. The EtfABCX enzyme complex couples NADH oxidation to the endergonic reduction of ferredoxin and exergonic reduction of menaquinone. We developed a model for the enzyme structure by using non-denaturing MS, cross-linking and homology modeling in which EtfA, B, and C each contained FAD, whereas EtfX contained two [4Fe-4S] clusters. On the basis of analyses using transient absorption, EPR and optical titrations with NADH or inorganic reductants with and without NAD+, we propose a catalytic cycle involving formation of an intermediary NAD+-bound complex. A charge transfer signal revealed an intriguing interplay of flavin semiquinones and a protein conformational change that gated electron transfer between the low- and high-potential pathways. We found that despite a common bifurcating flavin site, the proposed EtfABCX catalytic cycle is distinct from that of the genetically-unrelated bifurcating NADH-dependent ferredoxin NADP+ oxidoreductase (NfnI). The two enzymes particularly differed in the role of NAD+, the resting and bifurcating-ready states of the enzymes, how electron flow is gated, and in the two two-electron cycles constituting the overall four-electron reaction. Here, we conclude that P. aerophilum EtfABCX provides a model catalytic mechanism that builds on and extends previous studies of related bifurcating ETF's and can be applied to the large bifurcating ETF family.},
doi = {10.1074/jbc.RA118.005653},
journal = {Journal of Biological Chemistry},
number = 9,
volume = 294,
place = {United States},
year = {Fri Mar 01 00:00:00 EST 2019},
month = {Fri Mar 01 00:00:00 EST 2019}
}
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https://doi.org/10.1074/jbc.RA118.005653
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