Photosystem II-cyclic electron flow powers exceptional photoprotection and record growth in the microalga Chlorella ohadii

Abstract

The desert microalga Chlorella ohadii was reported to grow at extreme light intensities with minimal photoinhibition, tolerate frequent de/re-hydrations, yet minimally employs antenna-based non-photochemical quenching for photoprotection. Here we investigate the molecular mechanisms by measuring Photosystem II charge separation yield (chlorophyll variable fluorescence, Fv/Fm) and flash-induced O yield to measure the contributions from both linear (PSII-LEF) and cyclic (PSII-CEF) electron flow within PSII. Cells grow increasingly faster at higher light intensities (μE/m/s) from low (20) to high (200) to extreme (2000) by escalating photoprotection via shifting from PSII-LEF to PSII-CEF. This shifts PSII charge separation from plastoquinone reduction (PSII-LEF) to plastoquinol oxidation (PSII-CEF), here postulated to enable proton gradient and ATP generation that powers photoprotection. Low light-grown cells have unusually small antennae (332 Chl/PSII), use mainly PSII-LEF (95%) and convert 40% of PSII charge separations into O (a high O quantum yield of 0.06mol/mol PSII/flash). High light-grown cells have smaller antenna and lower PSII-LEF (63%). Extreme light-grown cells have only 42 Chl/PSII (no LHCII antenna), minimal PSII-LEF (10%), and grow faster than any known phototroph (doubling time 1.3h). Adding a synthetic quinone in excess to supplement the PQ pool fully uncouples PSII-CEF from its natural regulation and produces maximum PSII-LEF. Upon dark adaptation PSII-LEF rapidly reverts to PSII-CEF, a transient protection mechanism to conserve water and minimize the cost of antenna biosynthesis. The capacity of the electron acceptor pool (plastoquinone pool), and the characteristic times for exchange of (PQH) with PQ and reoxidation of (PQH) were determined.

Unresolved quenching mechanisms of chlorophyll fluorescence may invalidate MT saturating pulse analyses of photosynthetic electron transfer in microalgae

“…An interesting case of almost total uncoupling of fluorescence‐based estimates of PSII activity and oxygen evolution in microalgae is Chlorella ohadii , a green alga isolated from desert crust of Israel (Treves et al ). The uncoupling of the two parameters in C. ohadii was assigned to the proposed cyclic electron flow pathway within PSII (Treves et al , Ananyev et al ), a pathway suggested to participate in photoprotection in excess light also in the diatom P. tricornutum (Feikema et al ).…”

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

“…Polarographic measurements of flash‐induced O 2 evolution patterns (FIOPs) in plastids were performed in the presence of DMBQ as an electron acceptor using in‐house Clark‐type Pt/Ir electrode with a thin‐layer microchamber configuration described recently (Ananyev et al , Ananyev et al ). The electrode was equipped with a thin (∼0.5 μm) polyethylene membrane which prevented the interference of DMBQ with a current of the cathode–anode system.…”

“…With exception of a few known unique photoinhibition-tolerant species (Fukuda et al 2008, Ananyev et al 2017, all photosynthetic organisms, under environmental stress and excessive light energy, are prone to photoinhibition, which strongly affects their photosynthetic activity, growth and productivity. To cope with photodamage, mature plants have developed diverse photoprotection mechanisms and are capable of reassembly and replacement of the damaged PSII centers via a PSII repair cycle (Nixon et al 2010, Takahashi and Badger 2011, Järvi et al 2015, Pinnola and Bassi 2018.…”

Nutrient gradients simulate different adjustments of coral-algal symbiosis

“…For instance, Turpin and Bruce [40] discovered that ammonia assimilation could induce state transitions of photosynthesis, and nonphotochemical quenching of PSII was associated with uorescence yield of PSI increase during ammonia assimilation due to high energy requirement. PSII is surrounded by cyclic electron ow which can also generate ATP for potential nutrient assimilation [43]. 2) The high expression of PSII under nutrient stress is due to its self-repairment and re-assembly to guarantee its function [44,45].…”