Alteration of the H-Bond to the A1A phylloquinone in photosystem I: Influence on the kinetics and energetics of electron transfer

Nithya Srinivasan, Stefano Santabarbara, Fabrice Rappaport, Donatella Carbonera, Kevin Redding, Art Van Der Est, John H. Golbeck

    Research output: Contribution to journalArticle

    16 Citations (Scopus)

    Abstract

    In Photosystem I, the backbone nitrogen of Leu722PsaA forms a hydro-gen bond with the C4 carbonyl oxygen of phylloquinone in the A1A site. A previous low-temperature EPR study indicated that substitution of Leu722PsaA with a bulky Trp residue results in a weakened H-bond. Here, we employ room temperature, time-resolved optical spectroscopy and variable temperature, transient EPR spectroscopy to probe the effect of the altered H-bond on the energetics and kinetics of electron transfer. Relative to the wild type, we find that the rate of electron transfer from A1A - to FX in the L722WPsaA variant is faster by a factor of 3. This change is attributed to a lowered midpoint potential of A1A/A1A -, resulting in a larger Gibbs free energy change between A1A/A1A - and FX/FX -. An activation energy of 180 ± 10 meV is determined for the A1A --to- FX forward electron transfer step in the L722WPsaA variant compared with 220 ± 10 meV in the wild type. The Arrhenius plot shows a break at ∼200 K, below which the rate becomes nearly independent of temperature. This behavior is described using a quantum mechanical treatment that takes the zero-point energy into account as well as an alternative model that invokes a dynamical transition in the protein at ∼200 K.

    Original languageEnglish (US)
    Pages (from-to)1751-1759
    Number of pages9
    JournalJournal of Physical Chemistry B
    Volume115
    Issue number8
    DOIs
    StatePublished - Mar 3 2011

    Fingerprint

    phylloquinone
    Vitamin K 1
    Photosystem I Protein Complex
    electron transfer
    Kinetics
    Electrons
    kinetics
    Paramagnetic resonance
    zero point energy
    Gibbs free energy
    Arrhenius plots
    Temperature
    spectroscopy
    plots
    substitutes
    activation energy
    proteins
    nitrogen
    Substitution reactions
    Nitrogen

    ASJC Scopus subject areas

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

    Cite this

    Alteration of the H-Bond to the A1A phylloquinone in photosystem I : Influence on the kinetics and energetics of electron transfer. / Srinivasan, Nithya; Santabarbara, Stefano; Rappaport, Fabrice; Carbonera, Donatella; Redding, Kevin; Van Der Est, Art; Golbeck, John H.

    In: Journal of Physical Chemistry B, Vol. 115, No. 8, 03.03.2011, p. 1751-1759.

    Research output: Contribution to journalArticle

    Srinivasan, Nithya ; Santabarbara, Stefano ; Rappaport, Fabrice ; Carbonera, Donatella ; Redding, Kevin ; Van Der Est, Art ; Golbeck, John H. / Alteration of the H-Bond to the A1A phylloquinone in photosystem I : Influence on the kinetics and energetics of electron transfer. In: Journal of Physical Chemistry B. 2011 ; Vol. 115, No. 8. pp. 1751-1759.
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    abstract = "In Photosystem I, the backbone nitrogen of Leu722PsaA forms a hydro-gen bond with the C4 carbonyl oxygen of phylloquinone in the A1A site. A previous low-temperature EPR study indicated that substitution of Leu722PsaA with a bulky Trp residue results in a weakened H-bond. Here, we employ room temperature, time-resolved optical spectroscopy and variable temperature, transient EPR spectroscopy to probe the effect of the altered H-bond on the energetics and kinetics of electron transfer. Relative to the wild type, we find that the rate of electron transfer from A1A - to FX in the L722WPsaA variant is faster by a factor of 3. This change is attributed to a lowered midpoint potential of A1A/A1A -, resulting in a larger Gibbs free energy change between A1A/A1A - and FX/FX -. An activation energy of 180 ± 10 meV is determined for the A1A --to- FX forward electron transfer step in the L722WPsaA variant compared with 220 ± 10 meV in the wild type. The Arrhenius plot shows a break at ∼200 K, below which the rate becomes nearly independent of temperature. This behavior is described using a quantum mechanical treatment that takes the zero-point energy into account as well as an alternative model that invokes a dynamical transition in the protein at ∼200 K.",
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