Negative cooperativity in the nitrogenase Fe protein electron delivery cycle

Karamatullah Danyal, Sudipta Shaw, Taylor R. Page, Simon Duval, Masaki Horitani, Amy R. Marts, Dmitriy Lukoyanov, Dennis R. Dean, Simone Raugei, Brian M. Hoffman, Lance C. Seefeldt, Edwin Antony

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Nitrogenase catalyzes the ATP-dependent reduction of dinitrogen (N2) to two ammonia (NH3) molecules through the participation of its two protein components, the MoFe and Fe proteins. Electron transfer (ET) from the Fe protein to the catalytic MoFe protein involves a series of synchronized events requiring the transient association of one Fe protein with each αβ half of the α2β2 MoFe protein. This process is referred to as the Fe protein cycle and includes binding of two ATP to an Fe protein, association of an Fe protein with the MoFe protein, ET from the Fe protein to the MoFe protein, hydrolysis of the two ATP to two ADP and two Pi for each ET, Pi release, and dissociation of oxidized Fe protein-(ADP)2 from the MoFe protein. Because the MoFe protein tetramer has two separate αβ active units, it participates in two distinct Fe protein cycles. Quantitative kinetic measurements of ET, ATP hydrolysis, and Pi release during the presteady-state phase of electron delivery demonstrate that the two halves of the ternary complex between the MoFe protein and two reduced Fe protein-(ATP)2 do not undergo the Fe protein cycle independently. Instead, the data are globally fit with a two-branch negative-cooperativity kinetic model in which ET in one-half of the complex partially suppresses this process in the other. A possible mechanism for communication between the two halves of the nitrogenase complex is suggested by normal-mode calculations showing correlated and anticorrelated motions between the two halves.

Original languageEnglish
Pages (from-to)E5783-E5791
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number40
DOIs
Publication statusPublished - Oct 4 2016

Fingerprint

Molybdoferredoxin
Electrons
Proteins
Adenosine Triphosphate
Nitrogenase
Adenosine Diphosphate
Hydrolysis
nitrogenase reductase
Ammonia

Keywords

  • Allosteric control
  • ATP hydrolysis
  • Conformational control
  • Half-sites reactivity

ASJC Scopus subject areas

  • General

Cite this

Negative cooperativity in the nitrogenase Fe protein electron delivery cycle. / Danyal, Karamatullah; Shaw, Sudipta; Page, Taylor R.; Duval, Simon; Horitani, Masaki; Marts, Amy R.; Lukoyanov, Dmitriy; Dean, Dennis R.; Raugei, Simone; Hoffman, Brian M.; Seefeldt, Lance C.; Antony, Edwin.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, No. 40, 04.10.2016, p. E5783-E5791.

Research output: Contribution to journalArticle

Danyal, K, Shaw, S, Page, TR, Duval, S, Horitani, M, Marts, AR, Lukoyanov, D, Dean, DR, Raugei, S, Hoffman, BM, Seefeldt, LC & Antony, E 2016, 'Negative cooperativity in the nitrogenase Fe protein electron delivery cycle', Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 40, pp. E5783-E5791. https://doi.org/10.1073/pnas.1613089113
Danyal, Karamatullah ; Shaw, Sudipta ; Page, Taylor R. ; Duval, Simon ; Horitani, Masaki ; Marts, Amy R. ; Lukoyanov, Dmitriy ; Dean, Dennis R. ; Raugei, Simone ; Hoffman, Brian M. ; Seefeldt, Lance C. ; Antony, Edwin. / Negative cooperativity in the nitrogenase Fe protein electron delivery cycle. In: Proceedings of the National Academy of Sciences of the United States of America. 2016 ; Vol. 113, No. 40. pp. E5783-E5791.
@article{e90414d29d7b42eca0e34cbc067d72eb,
title = "Negative cooperativity in the nitrogenase Fe protein electron delivery cycle",
abstract = "Nitrogenase catalyzes the ATP-dependent reduction of dinitrogen (N2) to two ammonia (NH3) molecules through the participation of its two protein components, the MoFe and Fe proteins. Electron transfer (ET) from the Fe protein to the catalytic MoFe protein involves a series of synchronized events requiring the transient association of one Fe protein with each αβ half of the α2β2 MoFe protein. This process is referred to as the Fe protein cycle and includes binding of two ATP to an Fe protein, association of an Fe protein with the MoFe protein, ET from the Fe protein to the MoFe protein, hydrolysis of the two ATP to two ADP and two Pi for each ET, Pi release, and dissociation of oxidized Fe protein-(ADP)2 from the MoFe protein. Because the MoFe protein tetramer has two separate αβ active units, it participates in two distinct Fe protein cycles. Quantitative kinetic measurements of ET, ATP hydrolysis, and Pi release during the presteady-state phase of electron delivery demonstrate that the two halves of the ternary complex between the MoFe protein and two reduced Fe protein-(ATP)2 do not undergo the Fe protein cycle independently. Instead, the data are globally fit with a two-branch negative-cooperativity kinetic model in which ET in one-half of the complex partially suppresses this process in the other. A possible mechanism for communication between the two halves of the nitrogenase complex is suggested by normal-mode calculations showing correlated and anticorrelated motions between the two halves.",
keywords = "Allosteric control, ATP hydrolysis, Conformational control, Half-sites reactivity",
author = "Karamatullah Danyal and Sudipta Shaw and Page, {Taylor R.} and Simon Duval and Masaki Horitani and Marts, {Amy R.} and Dmitriy Lukoyanov and Dean, {Dennis R.} and Simone Raugei and Hoffman, {Brian M.} and Seefeldt, {Lance C.} and Edwin Antony",
year = "2016",
month = "10",
day = "4",
doi = "10.1073/pnas.1613089113",
language = "English",
volume = "113",
pages = "E5783--E5791",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "40",

}

TY - JOUR

T1 - Negative cooperativity in the nitrogenase Fe protein electron delivery cycle

AU - Danyal, Karamatullah

AU - Shaw, Sudipta

AU - Page, Taylor R.

AU - Duval, Simon

AU - Horitani, Masaki

AU - Marts, Amy R.

AU - Lukoyanov, Dmitriy

AU - Dean, Dennis R.

AU - Raugei, Simone

AU - Hoffman, Brian M.

AU - Seefeldt, Lance C.

AU - Antony, Edwin

PY - 2016/10/4

Y1 - 2016/10/4

N2 - Nitrogenase catalyzes the ATP-dependent reduction of dinitrogen (N2) to two ammonia (NH3) molecules through the participation of its two protein components, the MoFe and Fe proteins. Electron transfer (ET) from the Fe protein to the catalytic MoFe protein involves a series of synchronized events requiring the transient association of one Fe protein with each αβ half of the α2β2 MoFe protein. This process is referred to as the Fe protein cycle and includes binding of two ATP to an Fe protein, association of an Fe protein with the MoFe protein, ET from the Fe protein to the MoFe protein, hydrolysis of the two ATP to two ADP and two Pi for each ET, Pi release, and dissociation of oxidized Fe protein-(ADP)2 from the MoFe protein. Because the MoFe protein tetramer has two separate αβ active units, it participates in two distinct Fe protein cycles. Quantitative kinetic measurements of ET, ATP hydrolysis, and Pi release during the presteady-state phase of electron delivery demonstrate that the two halves of the ternary complex between the MoFe protein and two reduced Fe protein-(ATP)2 do not undergo the Fe protein cycle independently. Instead, the data are globally fit with a two-branch negative-cooperativity kinetic model in which ET in one-half of the complex partially suppresses this process in the other. A possible mechanism for communication between the two halves of the nitrogenase complex is suggested by normal-mode calculations showing correlated and anticorrelated motions between the two halves.

AB - Nitrogenase catalyzes the ATP-dependent reduction of dinitrogen (N2) to two ammonia (NH3) molecules through the participation of its two protein components, the MoFe and Fe proteins. Electron transfer (ET) from the Fe protein to the catalytic MoFe protein involves a series of synchronized events requiring the transient association of one Fe protein with each αβ half of the α2β2 MoFe protein. This process is referred to as the Fe protein cycle and includes binding of two ATP to an Fe protein, association of an Fe protein with the MoFe protein, ET from the Fe protein to the MoFe protein, hydrolysis of the two ATP to two ADP and two Pi for each ET, Pi release, and dissociation of oxidized Fe protein-(ADP)2 from the MoFe protein. Because the MoFe protein tetramer has two separate αβ active units, it participates in two distinct Fe protein cycles. Quantitative kinetic measurements of ET, ATP hydrolysis, and Pi release during the presteady-state phase of electron delivery demonstrate that the two halves of the ternary complex between the MoFe protein and two reduced Fe protein-(ATP)2 do not undergo the Fe protein cycle independently. Instead, the data are globally fit with a two-branch negative-cooperativity kinetic model in which ET in one-half of the complex partially suppresses this process in the other. A possible mechanism for communication between the two halves of the nitrogenase complex is suggested by normal-mode calculations showing correlated and anticorrelated motions between the two halves.

KW - Allosteric control

KW - ATP hydrolysis

KW - Conformational control

KW - Half-sites reactivity

UR - http://www.scopus.com/inward/record.url?scp=84989819113&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84989819113&partnerID=8YFLogxK

U2 - 10.1073/pnas.1613089113

DO - 10.1073/pnas.1613089113

M3 - Article

C2 - 27698129

AN - SCOPUS:84989819113

VL - 113

SP - E5783-E5791

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 40

ER -