Interquinone electron transfer in photosystem i as evidenced by altering the hydrogen bond strength to the phylloquinone(s)

Stefano Santabarbara, Kiera Reifschneider, Audrius Jasaitis, Feifei Gu, Giancarlo Agostini, Donatella Carbonera, Fabrice Rappaport, Kevin Redding

    Research output: Contribution to journalArticle

    23 Citations (Scopus)

    Abstract

    The kinetics of electron transfer from phyllosemiquinone (PhQ ̇-) to the iron sulfur cluster FX in Photosystem I (PS I) are described by lifetimes of ∼20 and ∼250 ns. These two rates are attributed to reactions involving the quinones bound primarily by the PsaB (PhQB) and PsaA (PhQA) subunits, respectively. The factors leading to a ∼10-fold difference between the observed lifetimes are not yet clear. The peptide nitrogen of conserved residues PsaA-Leu722 and PsaB-Leu706 is involved in asymmetric hydrogen-bonding to PhQA and PhQ B, respectively. Upon mutation of these residues in PS I of the green alga, Chlamydomonas reinhardtii, we observe an acceleration of the oxidation kinetics of the PhQ̇- interacting with the targeted residue: from ∼255 to ∼180 ns in PsaA-L722Y/T and from ∼24 to ∼10 ns in PsaB-L706Y. The acceleration of the kinetics in the mutants is consistent with a perturbation of the H-bond, destabilizing the PhQ̇- state, and increasing the driving force of its oxidation. Surprisingly, the relative amplitudes of the phases reflecting PhQA ̇- and PhQB ̇- oxidation were also affected by these mutations: the apparent PhQA ̇-/PhQB ̇- ratio is shifted from 0.65:0.35 in wild-type reaction centers to 0.5:0.5 in PsaA-L722Y/T and to 0.8:0.2 in PsaB-L706Y. The most consistent account for all these observations involves considering reversibility of oxidation of PhQA ̇- and PhQB ̇- by FX, and asymmetry in the driving forces for these electron transfer reactions, which in turn leads to Fx-mediated interquinone electron transfer.

    Original languageEnglish (US)
    Pages (from-to)9300-9312
    Number of pages13
    JournalJournal of Physical Chemistry B
    Volume114
    Issue number28
    DOIs
    StatePublished - Jul 22 2010

    Fingerprint

    phylloquinone
    Vitamin K 1
    Hydrogen bonds
    electron transfer
    hydrogen bonds
    Photosystem I Protein Complex
    Oxidation
    oxidation
    Electrons
    mutations
    Kinetics
    kinetics
    life (durability)
    Quinones
    quinones
    algae
    Algae
    Sulfur
    Peptides
    peptides

    ASJC Scopus subject areas

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

    Cite this

    Interquinone electron transfer in photosystem i as evidenced by altering the hydrogen bond strength to the phylloquinone(s). / Santabarbara, Stefano; Reifschneider, Kiera; Jasaitis, Audrius; Gu, Feifei; Agostini, Giancarlo; Carbonera, Donatella; Rappaport, Fabrice; Redding, Kevin.

    In: Journal of Physical Chemistry B, Vol. 114, No. 28, 22.07.2010, p. 9300-9312.

    Research output: Contribution to journalArticle

    Santabarbara, S, Reifschneider, K, Jasaitis, A, Gu, F, Agostini, G, Carbonera, D, Rappaport, F & Redding, K 2010, 'Interquinone electron transfer in photosystem i as evidenced by altering the hydrogen bond strength to the phylloquinone(s)' Journal of Physical Chemistry B, vol. 114, no. 28, pp. 9300-9312. https://doi.org/10.1021/jp1038656
    Santabarbara, Stefano ; Reifschneider, Kiera ; Jasaitis, Audrius ; Gu, Feifei ; Agostini, Giancarlo ; Carbonera, Donatella ; Rappaport, Fabrice ; Redding, Kevin. / Interquinone electron transfer in photosystem i as evidenced by altering the hydrogen bond strength to the phylloquinone(s). In: Journal of Physical Chemistry B. 2010 ; Vol. 114, No. 28. pp. 9300-9312.
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    abstract = "The kinetics of electron transfer from phyllosemiquinone (PhQ ̇-) to the iron sulfur cluster FX in Photosystem I (PS I) are described by lifetimes of ∼20 and ∼250 ns. These two rates are attributed to reactions involving the quinones bound primarily by the PsaB (PhQB) and PsaA (PhQA) subunits, respectively. The factors leading to a ∼10-fold difference between the observed lifetimes are not yet clear. The peptide nitrogen of conserved residues PsaA-Leu722 and PsaB-Leu706 is involved in asymmetric hydrogen-bonding to PhQA and PhQ B, respectively. Upon mutation of these residues in PS I of the green alga, Chlamydomonas reinhardtii, we observe an acceleration of the oxidation kinetics of the PhQ̇- interacting with the targeted residue: from ∼255 to ∼180 ns in PsaA-L722Y/T and from ∼24 to ∼10 ns in PsaB-L706Y. The acceleration of the kinetics in the mutants is consistent with a perturbation of the H-bond, destabilizing the PhQ̇- state, and increasing the driving force of its oxidation. Surprisingly, the relative amplitudes of the phases reflecting PhQA ̇- and PhQB ̇- oxidation were also affected by these mutations: the apparent PhQA ̇-/PhQB ̇- ratio is shifted from 0.65:0.35 in wild-type reaction centers to 0.5:0.5 in PsaA-L722Y/T and to 0.8:0.2 in PsaB-L706Y. The most consistent account for all these observations involves considering reversibility of oxidation of PhQA ̇- and PhQB ̇- by FX, and asymmetry in the driving forces for these electron transfer reactions, which in turn leads to Fx-mediated interquinone electron transfer.",
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    AU - Santabarbara, Stefano

    AU - Reifschneider, Kiera

    AU - Jasaitis, Audrius

    AU - Gu, Feifei

    AU - Agostini, Giancarlo

    AU - Carbonera, Donatella

    AU - Rappaport, Fabrice

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