Evidence That the Pi Release Event Is the Rate-Limiting Step in the Nitrogenase Catalytic Cycle

Yang, Zhi-Yong; Ledbetter, Rhesa; Shaw, Sudipta; Pence, Natasha; Tokmina-Lukaszewska, Monika; Eilers, Brian; Guo, Qingjuan; Pokhrel, Nilisha; Cash, Valerie L.; Dean, Dennis R.; Antony, Edwin; Bothner, Brian; Peters, John W.; Seefeldt, Lance C.

doi:10.1021/acs.biochem.6b00421

Evidence That the P_i Release Event Is the Rate-Limiting Step in the Nitrogenase Catalytic Cycle

Journal Article · Wed Jun 22 00:00:00 EDT 2016 · Biochemistry

DOI:https://doi.org/10.1021/acs.biochem.6b00421· OSTI ID:1387866

Yang, Zhi-Yong ^[1]; Ledbetter, Rhesa ^[1]; Shaw, Sudipta ^[1]; Pence, Natasha ^[2]; Tokmina-Lukaszewska, Monika ^[2]; Eilers, Brian ^[2]; Guo, Qingjuan ^[1]; Pokhrel, Nilisha ^[3]; Cash, Valerie L. ^[4]; Dean, Dennis R. ^[4]; Antony, Edwin ^[3]; Bothner, Brian ^[2]; Peters, John W. ^[2]; Seefeldt, Lance C. ^[1]

Utah State Univ., Logan, UT (United States). Dept. of Chemistry and Biochemistry
Montana State Univ., Bozeman, MT (United States). Dept. of Chemistry and Biochemistry
Marquette Univ., Milwaukee, WI (United States). Dept. of Biological Sciences
Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States). Dept. of Biochemistry

Nitrogenase reduction of dinitrogen (N₂) to ammonia (NH₃) involves a sequence of events that occur upon the transient association of the reduced Fe protein containing two ATP molecules with the MoFe protein that includes electron transfer, ATP hydrolysis, Pi release, and dissociation of the oxidized, ADP-containing Fe protein from the reduced MoFe protein. Numerous kinetic studies using the nonphysiological electron donor dithionite have suggested that the rate-limiting step in this reaction cycle is the dissociation of the Fe protein from the MoFe protein. Here, we have established the rate constants for each of the key steps in the catalytic cycle using the physiological reductant flavodoxin protein in its hydroquinone state. The findings indicate that with this reductant, the rate-limiting step in the reaction cycle is not protein–protein dissociation or reduction of the oxidized Fe protein, but rather events associated with the Pi release step. Further, it is demonstrated that (i) Fe protein transfers only one electron to MoFe protein in each Fe protein cycle coupled with hydrolysis of two ATP molecules, (ii) the oxidized Fe protein is not reduced when bound to MoFe protein, and (iii) the Fe protein interacts with flavodoxin using the same binding interface that is used with the MoFe protein. These findings allow a revision of the rate-limiting step in the nitrogenase Fe protein cycle.

View Accepted Manuscript (DOE)

Research Organization:: Energy Frontier Research Centers (EFRC) (United States). Center for Biological Electron Transfer and Catalysis (BETCy)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: SC0012518

OSTI ID:: 1387866

Journal Information:: Biochemistry, Journal Name: Biochemistry Journal Issue: 26 Vol. 55; ISSN 0006-2960

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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