The strontium inorganic mutant of the water oxidizing center (CaMn4O5) of PSII improves WOC efficiency but slows electron flux through the terminal acceptors

Abstract

Herein we extend prior studies of biosynthetic strontium replacement of calcium in PSII-WOC core particles to characterize whole cells. Previous studies of Thermosynechococcus elongatus found a lower rate of light-saturated O2 from isolated PSII-WOC(Sr) cores and 5-8× slower rate of oxygen release. We find similar properties in whole cells, and show it is due to a 20% larger Arrhenius activation barrier for O2 evolution. Cellular adaptation to the sluggish PSII-WOC(Sr) cycle occurs in which flux through the QAQB acceptor gate becomes limiting for turnover rate in vivo. Benzoquinone derivatives that bind to QB site remove this kinetic chokepoint yielding 31% greater O2 quantum yield (QY) of PSII-WOC(Sr) vs. PSII-WOC(Ca). QY and efficiency of the WOC(Sr) catalytic cycle are greatly improved at low light flux, due to fewer misses and backward transitions and 3-fold longer lifetime of the unstable S3 state, attributed to greater thermodynamic stabilization of the WOC(Sr) relative to the photoactive tyrosine YZ. More linear and less cyclic electron flow through PSII occurs per PSII-WOC(Sr). The organismal response to the more active PSII centers in Sr-grown cells at 45°C is to lower the number of active PSII-WOC per Chl, producing comparable oxygen and energy per cell. We conclude that redox and protonic energy fluxes created by PSII are primary determinants for optimal growth rate of T. elongatus. We further conclude that the (Sr-favored) intermediate-spin S=5/2 form of the S2 state is the active form in the catalytic cycle relative to the low-spin S=1/2 form.

Missing Pieces in the Puzzle of Biological Water Oxidation

“…For example, Boussac et al observed that in both Ca and Sr PSII, the high-spin form of the S 2 state is capable of advancing to S 3 at low temperature (198 K), and they suggested this to be an experimental demonstration that the low-spin S 2 state advances to S 3 via the high-spin S 2 state without detectable intermediates. Gates et al similarly concluded that the S = 5 / 2 form of the S 2 state, the form stabilized by strontium substitution, is the active form in the catalytic cycle relative to the low-spin S = 1 / 2 form.…”

Energetics and Kinetics of S-State Transitions Monitored by Delayed Chlorophyll Fluorescence

“…These 8 parameters are the same for all temperatures, assuming linear Arrhenius plots in the temperature range from 0 to 30°C. The linear Arrhenius plot is predicted by standard electron-transfer as well as transition-state theory and largely has been experimentally confirmed for the reactions in the oxygen-evolving complex of PSII (Klauss et al, 2012; Bao and Burnap, 2015; Klauss et al, 2015; Gates et al, 2016). Using this rationale, instead of 7 × 9 = 63 adjustable parameter for the set of 7 DF decays measured at different temperatures, the overall number of parameters was reduced to 8 + 5 × 7 = 43 free parameters (Zaharieva et al, 2013).…”

‘Birth defects’ of photosystem II make it highly susceptible to photodamage during chloroplast biogenesis

“…As no change in miss parameters was found in the latter sample types, we attribute this phenomenon (of increased O 2 signals) to a sedimentation of the samples onto the membrane surface that covers Pt‐electrode during relatively long FIOPs measurements. Precisely, the same settling phenomenon is seen with whole cells of algae (Gates et al ).…”

“…S1). Because DMBQ, in contrast to PPBQ/FeCy, does not provide significant artifacts in FIOPs experiments (Ananyev et al , Gates et al ), DMBQ was employed throughout this study.…”