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 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 (US)
    Pages (from-to)14008-14016
    Number of pages9
    JournalJournal of Physical Chemistry B
    Volume116
    Issue number48
    DOIs
    StatePublished - 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; 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, K & 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 ; 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{508756c47d5e415bba3e7fd9641c42cd,
    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 Kevin Redding and {Van Der Est}, Art",
    year = "2012",
    month = "12",
    day = "6",
    doi = "10.1021/jp309410w",
    language = "English (US)",
    volume = "116",
    pages = "14008--14016",
    journal = "Journal of Physical Chemistry B Materials",
    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

    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 Materials

    JF - Journal of Physical Chemistry B Materials

    SN - 1520-6106

    IS - 48

    ER -