The Effect of Bacteriochlorophyll g Oxidation on Energy and Electron Transfer in Reaction Centers from Heliobacterium modesticaldum

Bryan Ferlez, Weibing Dong, Reza Siavashi, Kevin Redding, Harvey J M Hou, John H. Golbeck, Art Van Der Est

    Research output: Contribution to journalArticle

    6 Citations (Scopus)

    Abstract

    The heliobacteria are a family of strictly anaerobic, Gram-positive, photoheterotrophs in the Firmicutes. They make use of a homodimeric type I reaction center (RC) that contains ~20 antenna bacteriochlorophyll (BChl) g molecules, a special pair of BChl g′ molecules (P800), two 81-OH-Chl aF molecules (A0), a [4Fe-4S] iron-sulfur cluster (FX), and a carotenoid (4,4′-diaponeurosporene). It is known that in the presence of light and oxygen BChl g is converted to a species with an absorption spectrum identical to that of Chl a. Here, we show that main product of the conversion is 81-OH-Chl aF. Smaller amounts of two other oxidized Chl aF species are also produced. In the presence of light and oxygen, the kinetics of the conversion are monophasic and temperature dependent, with an activation energy of 66 ± 2 kJ mol-1. In the presence of oxygen in the dark, the conversion occurs in two temperature-dependent kinetic phases: a slow phase followed by a fast phase with an activation energy of 53 ± 1 kJ mol-1. The loss of BChl g′ occurs at the same rate as the loss of Bchl g; hence, the special pair converts at the same rate as the antenna Chls. However, the loss of P800 photooxidiation and flavodoxin reduction is not linear with the loss of BChl g. In anaerobic RCs, the charge recombination between P800 + and FX - at 80 K is monophasic with a lifetime of 4.2 ms, but after exposure to oxygen, an additional phase with a lifetime of 0.3 ms is observed. Transient EPR data show that the line width of P800 + increases as BChl g is converted to Chl aF and the rate of electron transfer from A0 to FX, as estimated from the net polarization generated by singlet-triplet mixing during the lifetime of P800 +A0 -, is unchanged. The transient EPR data also show that conversion of the BChl g results in increased formation of triplet states of both BChl g and Chl aF. The nonlinear loss of P800 photooxidiation and flavodoxin reduction, the biphasic backreaction kinetics, and the increased EPR line width of P800 + are all consistent with a model in which the BChl g′/BChl g′ and BChl g′/Chl aF′ special pairs are functional but the Chl aF′/Chl aF′ special pair is not.

    Original languageEnglish (US)
    Pages (from-to)13714-13725
    Number of pages12
    JournalJournal of Physical Chemistry B
    Volume119
    Issue number43
    DOIs
    StatePublished - Oct 29 2015

    Fingerprint

    Bacteriochlorophylls
    electron transfer
    energy transfer
    Oxidation
    oxidation
    Electrons
    Paramagnetic resonance
    Oxygen
    oxygen
    Linewidth
    life (durability)
    Molecules
    Kinetics
    kinetics
    antennas
    Activation energy
    Antennas
    activation energy
    Flavodoxin
    molecules

    ASJC Scopus subject areas

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

    Cite this

    The Effect of Bacteriochlorophyll g Oxidation on Energy and Electron Transfer in Reaction Centers from Heliobacterium modesticaldum. / Ferlez, Bryan; Dong, Weibing; Siavashi, Reza; Redding, Kevin; Hou, Harvey J M; Golbeck, John H.; Van Der Est, Art.

    In: Journal of Physical Chemistry B, Vol. 119, No. 43, 29.10.2015, p. 13714-13725.

    Research output: Contribution to journalArticle

    Ferlez, Bryan ; Dong, Weibing ; Siavashi, Reza ; Redding, Kevin ; Hou, Harvey J M ; Golbeck, John H. ; Van Der Est, Art. / The Effect of Bacteriochlorophyll g Oxidation on Energy and Electron Transfer in Reaction Centers from Heliobacterium modesticaldum. In: Journal of Physical Chemistry B. 2015 ; Vol. 119, No. 43. pp. 13714-13725.
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    abstract = "The heliobacteria are a family of strictly anaerobic, Gram-positive, photoheterotrophs in the Firmicutes. They make use of a homodimeric type I reaction center (RC) that contains ~20 antenna bacteriochlorophyll (BChl) g molecules, a special pair of BChl g′ molecules (P800), two 81-OH-Chl aF molecules (A0), a [4Fe-4S] iron-sulfur cluster (FX), and a carotenoid (4,4′-diaponeurosporene). It is known that in the presence of light and oxygen BChl g is converted to a species with an absorption spectrum identical to that of Chl a. Here, we show that main product of the conversion is 81-OH-Chl aF. Smaller amounts of two other oxidized Chl aF species are also produced. In the presence of light and oxygen, the kinetics of the conversion are monophasic and temperature dependent, with an activation energy of 66 ± 2 kJ mol-1. In the presence of oxygen in the dark, the conversion occurs in two temperature-dependent kinetic phases: a slow phase followed by a fast phase with an activation energy of 53 ± 1 kJ mol-1. The loss of BChl g′ occurs at the same rate as the loss of Bchl g; hence, the special pair converts at the same rate as the antenna Chls. However, the loss of P800 photooxidiation and flavodoxin reduction is not linear with the loss of BChl g. In anaerobic RCs, the charge recombination between P800 + and FX - at 80 K is monophasic with a lifetime of 4.2 ms, but after exposure to oxygen, an additional phase with a lifetime of 0.3 ms is observed. Transient EPR data show that the line width of P800 + increases as BChl g is converted to Chl aF and the rate of electron transfer from A0 to FX, as estimated from the net polarization generated by singlet-triplet mixing during the lifetime of P800 +A0 -, is unchanged. The transient EPR data also show that conversion of the BChl g results in increased formation of triplet states of both BChl g and Chl aF. The nonlinear loss of P800 photooxidiation and flavodoxin reduction, the biphasic backreaction kinetics, and the increased EPR line width of P800 + are all consistent with a model in which the BChl g′/BChl g′ and BChl g′/Chl aF′ special pairs are functional but the Chl aF′/Chl aF′ special pair is not.",
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    AU - Hou, Harvey J M

    AU - Golbeck, John H.

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