Introduction of a hydrogen bond between phylloquinone PhQA and a threonine side-chain OH group in photosystem i

Sam Mula, Michael D. McConnell, Amy Ching, Nan Zhao, Heather L. Gordon, Gary Hastings, Kevin Edward Redding, Art Van Der Est

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

The phylloquinone acceptor PhQA in photosystem I binds to the protein through a single H-bond to the backbone nitrogen of PsaA-L722. Here, we investigate the effect of this H-bond on the electron transfer (ET) kinetics by substituting threonine for PsaA-L722. Room temperature spin-polarized transient EPR measurements show that in the PsaA-L722T mutant, the rate of PhQ A - to FX ET increases and the hyperfine coupling to the 2-methyl group of PhQA is much larger than in the wild type. Molecular dynamics simulations and ONIOM type electronic structure calculations indicate that it is possible for the OH group of the Thr side chain to form an H-bond to the carbonyl oxygen atom, O4 of the phylloquinone, and that this results in an increase in the 2-methyl hyperfine couplings as observed in the transient EPR data. The Arrhenius plot of the PhQA - to FX ET in the PsaA-L722T mutant suggests that the increased rate is probably the result of a slight change in the electronic coupling between PhQA - and FX. The strong deviation from Arrhenius behavior observed at ∼200 K can be reproduced using a semiclassical model, which takes the zero-point energy of the mode coupled to the ET into account. However, since the change in slope of the Arrhenius plot occurs at the protein glass transition temperature, it is argued that it could be the result of a change in the protein relaxation dynamics at this temperature rather than quantum mechanical effects.

Original languageEnglish
Pages (from-to)14008-14016
Number of pages9
JournalJournal of Physical Chemistry B
Volume116
Issue number48
DOIs
Publication statusPublished - Dec 6 2012

Fingerprint

phylloquinone
Vitamin K 1
Threonine
Hydrogen bonds
electron transfer
hydrogen bonds
Arrhenius plots
Electrons
proteins
Proteins
Paramagnetic resonance
plots
Photosystem I Protein Complex
zero point energy
glass transition temperature
coupled modes
Electronic structure
Molecular dynamics
oxygen atoms
Nitrogen

ASJC Scopus subject areas

  • Physical and Theoretical Chemistry
  • Materials Chemistry
  • Surfaces, Coatings and Films

Cite this

Mula, S., McConnell, M. D., Ching, A., Zhao, N., Gordon, H. L., Hastings, G., ... Van Der Est, A. (2012). Introduction of a hydrogen bond between phylloquinone PhQA and a threonine side-chain OH group in photosystem i. Journal of Physical Chemistry B, 116(48), 14008-14016. https://doi.org/10.1021/jp309410w

Introduction of a hydrogen bond between phylloquinone PhQA and a threonine side-chain OH group in photosystem i. / Mula, Sam; McConnell, Michael D.; Ching, Amy; Zhao, Nan; Gordon, Heather L.; Hastings, Gary; Redding, Kevin Edward; Van Der Est, Art.

In: Journal of Physical Chemistry B, Vol. 116, No. 48, 06.12.2012, p. 14008-14016.

Research output: Contribution to journalArticle

Mula, S, McConnell, MD, Ching, A, Zhao, N, Gordon, HL, Hastings, G, Redding, KE & Van Der Est, A 2012, 'Introduction of a hydrogen bond between phylloquinone PhQA and a threonine side-chain OH group in photosystem i', Journal of Physical Chemistry B, vol. 116, no. 48, pp. 14008-14016. https://doi.org/10.1021/jp309410w
Mula, Sam ; McConnell, Michael D. ; Ching, Amy ; Zhao, Nan ; Gordon, Heather L. ; Hastings, Gary ; Redding, Kevin Edward ; Van Der Est, Art. / Introduction of a hydrogen bond between phylloquinone PhQA and a threonine side-chain OH group in photosystem i. In: Journal of Physical Chemistry B. 2012 ; Vol. 116, No. 48. pp. 14008-14016.
@article{0005cd44c06e4968905ff086a077d107,
title = "Introduction of a hydrogen bond between phylloquinone PhQA and a threonine side-chain OH group in photosystem i",
abstract = "The phylloquinone acceptor PhQA in photosystem I binds to the protein through a single H-bond to the backbone nitrogen of PsaA-L722. Here, we investigate the effect of this H-bond on the electron transfer (ET) kinetics by substituting threonine for PsaA-L722. Room temperature spin-polarized transient EPR measurements show that in the PsaA-L722T mutant, the rate of PhQ A - to FX ET increases and the hyperfine coupling to the 2-methyl group of PhQA is much larger than in the wild type. Molecular dynamics simulations and ONIOM type electronic structure calculations indicate that it is possible for the OH group of the Thr side chain to form an H-bond to the carbonyl oxygen atom, O4 of the phylloquinone, and that this results in an increase in the 2-methyl hyperfine couplings as observed in the transient EPR data. The Arrhenius plot of the PhQA - to FX ET in the PsaA-L722T mutant suggests that the increased rate is probably the result of a slight change in the electronic coupling between PhQA - and FX. The strong deviation from Arrhenius behavior observed at ∼200 K can be reproduced using a semiclassical model, which takes the zero-point energy of the mode coupled to the ET into account. However, since the change in slope of the Arrhenius plot occurs at the protein glass transition temperature, it is argued that it could be the result of a change in the protein relaxation dynamics at this temperature rather than quantum mechanical effects.",
author = "Sam Mula and McConnell, {Michael D.} and Amy Ching and Nan Zhao and Gordon, {Heather L.} and Gary Hastings and Redding, {Kevin Edward} and {Van Der Est}, Art",
year = "2012",
month = "12",
day = "6",
doi = "10.1021/jp309410w",
language = "English",
volume = "116",
pages = "14008--14016",
journal = "Journal of Physical Chemistry B",
issn = "1520-6106",
publisher = "American Chemical Society",
number = "48",

}

TY - JOUR

T1 - Introduction of a hydrogen bond between phylloquinone PhQA and a threonine side-chain OH group in photosystem i

AU - Mula, Sam

AU - McConnell, Michael D.

AU - Ching, Amy

AU - Zhao, Nan

AU - Gordon, Heather L.

AU - Hastings, Gary

AU - Redding, Kevin Edward

AU - Van Der Est, Art

PY - 2012/12/6

Y1 - 2012/12/6

N2 - The phylloquinone acceptor PhQA in photosystem I binds to the protein through a single H-bond to the backbone nitrogen of PsaA-L722. Here, we investigate the effect of this H-bond on the electron transfer (ET) kinetics by substituting threonine for PsaA-L722. Room temperature spin-polarized transient EPR measurements show that in the PsaA-L722T mutant, the rate of PhQ A - to FX ET increases and the hyperfine coupling to the 2-methyl group of PhQA is much larger than in the wild type. Molecular dynamics simulations and ONIOM type electronic structure calculations indicate that it is possible for the OH group of the Thr side chain to form an H-bond to the carbonyl oxygen atom, O4 of the phylloquinone, and that this results in an increase in the 2-methyl hyperfine couplings as observed in the transient EPR data. The Arrhenius plot of the PhQA - to FX ET in the PsaA-L722T mutant suggests that the increased rate is probably the result of a slight change in the electronic coupling between PhQA - and FX. The strong deviation from Arrhenius behavior observed at ∼200 K can be reproduced using a semiclassical model, which takes the zero-point energy of the mode coupled to the ET into account. However, since the change in slope of the Arrhenius plot occurs at the protein glass transition temperature, it is argued that it could be the result of a change in the protein relaxation dynamics at this temperature rather than quantum mechanical effects.

AB - The phylloquinone acceptor PhQA in photosystem I binds to the protein through a single H-bond to the backbone nitrogen of PsaA-L722. Here, we investigate the effect of this H-bond on the electron transfer (ET) kinetics by substituting threonine for PsaA-L722. Room temperature spin-polarized transient EPR measurements show that in the PsaA-L722T mutant, the rate of PhQ A - to FX ET increases and the hyperfine coupling to the 2-methyl group of PhQA is much larger than in the wild type. Molecular dynamics simulations and ONIOM type electronic structure calculations indicate that it is possible for the OH group of the Thr side chain to form an H-bond to the carbonyl oxygen atom, O4 of the phylloquinone, and that this results in an increase in the 2-methyl hyperfine couplings as observed in the transient EPR data. The Arrhenius plot of the PhQA - to FX ET in the PsaA-L722T mutant suggests that the increased rate is probably the result of a slight change in the electronic coupling between PhQA - and FX. The strong deviation from Arrhenius behavior observed at ∼200 K can be reproduced using a semiclassical model, which takes the zero-point energy of the mode coupled to the ET into account. However, since the change in slope of the Arrhenius plot occurs at the protein glass transition temperature, it is argued that it could be the result of a change in the protein relaxation dynamics at this temperature rather than quantum mechanical effects.

UR - http://www.scopus.com/inward/record.url?scp=84870817675&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84870817675&partnerID=8YFLogxK

U2 - 10.1021/jp309410w

DO - 10.1021/jp309410w

M3 - Article

VL - 116

SP - 14008

EP - 14016

JO - Journal of Physical Chemistry B

JF - Journal of Physical Chemistry B

SN - 1520-6106

IS - 48

ER -