Involvement of molecular oxygen in the donor-side photoinhibition of Mn-depleted photosystem II membranes

Abstract

It has been shown by Khorobrykh et al. (Biochemistry (Moscow) 67:683-688, 2002); Yanykin et al. (Biochim Biophys Acta 1797:516-523, 2010); Khorobrykh et al. (Biochemistry 50:10658-10665, 2011) that Mn-depleted photosystem II (PSII) membrane fragments are characterized by an enhanced oxygen photoconsumption on the donor side of PSII which is accompanied with hydroperoxide formation and it was suggested that the events are related to the oxidative photoinhibition of PSII. Experimental confirmation of this suggestion is presented in this work. The degree of photoinhibition was determined by the loss of the capability of exogenous electron donors (Mn(2+) or sodium ascorbate) to the reactivation of electron transport [measured by the light-induced changes of chlorophyll fluorescence yield (∆F)] in Mn-depleted PSII membranes. The transition from anaerobic conditions to aerobic ones significantly activated photoinhibition of Mn-depleted PSII membranes both in the absence and in the presence of exogenous electron acceptor, ferricyanide. The photoinhibition of Mn-depleted PSII membranes was suppressed upon the addition of exogenous electron donors (Mn(2+), diphenylcarbazide, and ferrocyanide). The addition of superoxide dismutase did not affect the photoinhibition of Mn-depleted PSII membranes. It is concluded that the interaction of molecular oxygen (rather than superoxide anion radical formed on the acceptor side of PSII) with the oxidized components of the donor side of PSII reflects the involvement of O2 in the donor-side photoinhibition of Mn-depleted PSII membranes.

Enhancement of photoassembly of the functionally active water-oxidizing complex in Mn-depleted photosystem II membranes upon transition to anaerobic conditions

“…We assume that the decrease in the efficiency of apo-WOC-PSII photoactivation under aerobic conditions is due to the oxygen dependent photoinactivation of PSII. This conclusion is supported by data showing that rate of photoinactivation of apo-WOC-PSII is slowed under anaerobic conditions both in the absence and in the presence of an exogenous electron acceptor (ferricyanide), thus indicating the involvement of molecular oxygen in the donor side photoinhibition of PSII [30].…”

“…Most likely the increase of electron donation to the reaction center of PSII (at high concentration of Mn 2+ ) leads to a more efficient reduction of the long-lived P680 + • and TyrZ• states produced during illumination of apo-WOC-PSII preparations and, thereby, to the suppression of the donor side photoinactivation of PSII. Taking into account that the molecular oxygen is involved in photoinhibition of the donor side of PSII [30], the efficient suppression of P680 + • and TyrZ• at high concentration of Mn 2+ will lead to a decrease in the observed effect of anaerobiosis. The assumption is supported by previously obtained data [27] showing that a significant inhibition of the light-induced O 2 uptake in apo-WOC-PSII preparations occurs at high concentrations of Mn 2+ (N 15 μM, corresponding to 150 Mn per one PSII reaction centre) while the addition of Mn 2+ at low concentrations (1-2 μM, corresponding to 10-20 Mn per one RC) even activates the O 2 photoconsumption.…”

“…The light-dependent formation of ROOH in Mn-depleted PSII membranes was confirmed experimentally by using a lipophilic fluorescence probe specific to peroxides [28, see also 29]. In this case, molecular oxygen may be directly involved in the general mechanism of the donor side photoinhibition of PSII [30].…”

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It has been shown earlier (Khorobrykh and Klimov, 2015) that molecular oxygen is directly involved in the general mechanism of the donor side photoinhibition of photosystem II (PSII) membranes. In the present work the effect of oxygen on photoassembly ("photoactivation") of the functionally active inorganic core of the water-oxidizing complex (WOC) in Mn-depleted PSII preparations (apo-WOC-PSII) in the presence of exogenous Mn 2+ , Ca 2+ as well as ferricyanide was investigated.

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Formation of singlet oxygen by decomposition of protein hydroperoxide in photosystem II

“…It was evidenced that POOH is less abundant (4 molecules per PSII reaction center), while LOOH is more abundant (200 molecules per PSII reaction center). More recently, it has been evidenced that LOOH and POOH might play a crucial role in PSII damage on the PSII electron donor side [20]. …”