The catalytic mechanism of electron-bifurcating electron transfer flavoproteins (ETFs) involves an intermediary complex with NAD+

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.

doi:10.1074/jbc.RA118.005653

Title: The catalytic mechanism of electron-bifurcating electron transfer flavoproteins (ETFs) involves an intermediary complex with NAD+

Journal Article · Fri Mar 01 00:00:00 EST 2019 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.RA118.005653· OSTI ID:1769438

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.;

; Peters, John W.; Bothner, Brian;

;

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.

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Research Organization:: 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 Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC36-08GO28308

OSTI ID:: 1769438

Alternate ID(s):: OSTI ID: 1490994

Report Number(s):: NREL/JA-2700-72604; S0021925820392589; PII: S0021925820392589

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Vol. 294 Journal Issue: 9; ISSN 0021-9258

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 26 works

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Title: The catalytic mechanism of electron-bifurcating electron transfer flavoproteins (ETFs) involves an intermediary complex with NAD+

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