Trehalose stimulation of photoinduced electron transfer and oxygen photoconsumption in Mn-depleted photosystem 2 membrane fragments

• Trehalose induces a two-fold increase of oxygen photoconsumption in Mn-depleted PS2.
• Trehalose increases electron donation from Mn2 + to Mn-depleted PS2 reaction center.
• Trehalose accelerates reoxidation of QA− by QB in Mn-depleted PS2.
• Trehalose opens the so-called “closed reaction centers” in Mn-depleted PS2.

It is known that the removal of manganese from the water-oxidizing complex (WOC) of photosystem 2 (PS2) leads to activation of oxygen photoconsumption (OPC) [Khorobrykh et al., 2002; Yanykin et al., 2010] that is accompanied by the formation of organic hydroperoxides on the electron-donor side of PS2 [Khorobrykh et al., 2011]. In the present work the effect of trehalose on the OPC in Mn-depleted PS2 preparations (apo-WOC-PS2) was investigated. A more than two-fold increase of the OPC is revealed upon the addition of 1 M trehalose. Drastic (30%–70%) inhibition of the OPC upon the addition of either electron acceptor or electron donor indicates that the trehalose-induced activation of the OPC occurs on both donor and acceptor sides of PS2. A two-fold increase in the rate of superoxide-anion radical photoproduction on the electron-acceptor side of PS2 was also shown. Applying the “variable” chlorophyll fluorescence (ΔF) it was shown that the addition of trehalose induces: (i) a significant increase in the ability of exogenous Mn2 + to donate electrons to the reaction center of PS2, (ii) slowing down the photoaccumulation of the primary quinone electron acceptor of PS2 (QA−) under aerobic conditions, (iii) acceleration of the reoxidation of QA− by QB (and by QB−) as well as the replacement of QB2 − by a fully oxidized plastoquinone, and (iv) restoration of the electron transfer between the quinone electron carriers in the so-called “closed reaction centers of PS2” (their content in the apo-WOC-PS2 is 41%). It is suggested that the trehalose-induced increase in efficiency of the O2 interaction with the electron-donor and electron-acceptor sides of apo-WOC-PS2 is due to structural changes leading to both a decrease in the proportion of the “closed PS2 reaction centers” and an increase in the electron transfer rate in PS2.