Bicarbonate-induced redox tuning in Photosystem II for regulation and protection

Abstract

The midpoint potential ( E _m ) of ${\mathrm{Q}}_{\mathrm{A}}/{\mathrm{Q}}_{\mathrm{A}}^{-\mathrm{•}}$ , the one-electron acceptor quinone of Photosystem II (PSII), provides the thermodynamic reference for calibrating PSII bioenergetics. Uncertainty exists in the literature, with two values differing by ∼80 mV. Here, we have resolved this discrepancy by using spectroelectrochemistry on plant PSII-enriched membranes. Removal of bicarbonate (HCO ₃ ⁻) shifts the E _m from ∼−145 mV to −70 mV. The higher values reported earlier are attributed to the loss of HCO ₃ ⁻ during the titrations (pH 6.5, stirred under argon gassing). These findings mean that HCO ₃ ⁻ binds less strongly when Q _A ^−• is present. Light-induced Q _A ^−• formation triggered HCO ₃ ⁻ loss as manifest by the slowed electron transfer and the upshift in the E _m of Q _A. HCO ₃ ⁻-depleted PSII also showed diminished light-induced ¹O ₂ formation. This finding is consistent with a model in which the increase in the E _m of ${\mathrm{Q}}_{\mathrm{A}}/{\mathrm{Q}}_{\mathrm{A}}^{-\mathrm{•}}$ promotes safe, direct ${\mathrm{P}}^{+\mathrm{•}}{\mathrm{Q}}_{\mathrm{A}}^{-\mathrm{•}}$ charge recombination at the expense of the damaging back-reaction route that involves chlorophyll triplet-mediated ¹O ₂ formation [Johnson GN, et al. (1995) Biochim Biophys Acta 1229:202–207]. These findings provide a redox tuning mechanism, in which the interdependence of the redox state of Q _A and the binding by HCO ₃ ⁻ regulates and protects PSII. The potential for a sink (CO ₂) to source (PSII) feedback mechanism is discussed.