PSI Mehler reaction is the main alternative photosynthetic electron pathway in Symbiodinium sp., symbiotic dinoflagellates of cnidarians

Abstract

SummaryPhotosynthetic organisms have developed various photoprotective mechanisms to cope with exposure to high light intensities. In photosynthetic dinoflagellates that live in symbiosis with cnidarians, the nature and relative amplitude of these regulatory mechanisms are a matter of debate. In our study, the amplitude of photosynthetic alternative electron flows (AEF) to oxygen (chlororespiration, Mehler reaction), the mitochondrial respiration and the Photosystem I (PSI) cyclic electron flow were investigated in strains belonging to three clades (A1, B1 and F1) of Symbiodinium.Cultured Symbiodinium strains were maintained under identical environmental conditions, and measurements of oxygen evolution, fluorescence emission and absorption changes at specific wavelengths were used to evaluate PSI and PSII electron transfer rates (ETR).A light-and O 2 -dependent ETR was observed in all strains. This electron transfer chain involves PSII and PSI and is insensitive to inhibitors of mitochondrial activity and carbon fixation.We demonstrate that in all strains, the Mehler reaction responsible for photoreduction of oxygen by the PSI under high light, is the main AEF at the onset and at the steady state of photosynthesis. This sustained photosynthetic AEF under high light intensities acts as a photoprotective mechanism and leads to an increase of the ATP/NADPH ratio.

Non-intrusive Assessment of Photosystem II and Photosystem I in Whole Coral Tissues

“…Figures 2, 4). The fact that the steady-state P700 + level drops even in the presence of DCMU (when linear electron flow is blocked) indicates that alternative electron transport pathways might have been initiated under heat stress, the existence of which has been shown in Symbiodinium (Reynolds et al, 2008;Roberty et al, 2014;Aihara et al, 2016). The diminished response of steady-state P700 + under heat stress, when DCMU was applied might be due to the disturbance of the redox poise of P700 by DCMU (Fan et al, 2016a).…”

“…Under these circumstances, as indicated here, there may be side effects on cyclic electron transport and the Mehler-AscorbatePeroxidase (MAP) pathway. Recent works (Reynolds et al, 2008;Roberty et al, 2014;Aihara et al, 2016) have indicated the possibility that singlet oxygen production is generated when PQ pool is reduced, i.e., the relative size of oxidized PQ pool is smaller (and thus charge recombination in PSII reaction centers is promoted), which may be a primary factor in coral bleaching (Vass, 2012;Rehman et al, 2016). Nevertheless, these effects have to be documented individually in corals, where it is known that there are varied responses to similar acute thermal stress scenarios (Downs et al, 2013;Gardner et al, 2017).…”

“…For Symbiodinium, these processes are much less characterized than in higher plants or green algae (Warner and Suggett, 2016), but evidence suggests that alternative electron transport can manifest itself in Abbreviations: DCMU, 3-(3,4-dichlorophenyl)-1,1-dimethyl-urea; FR, far red light; F o , intrinsic fluorescence signal with fully oxidized Q A in the dark; F m , maximal fluorescence signal with fully reduced Q A ; F v , Variable fluorescence in the dark (proportional to reducible Q A ); GA, glycolaldehyde; F v /F m , Maximum quantum efficiency of open PSII centers in the dark based on full Q A reduction; MT, multiple turnover; LIFT-FRRF, laser-induced fluorescence transient fast repetition rate fluorometry; PAR, photosynthetically active radiation (400-700 nm); PSII, photosystem II; PSI, photosystem I; P700, special chlorophyll dimer acting as the primary electron donor in PSI; P700 + , oxidized state of P700; P m , maximum P700 + signal in weak FR light; PQ, plastoquinone pool σ PSIIfunctional absorption cross section of PSII in the dark; Q A , primary quinone electron acceptor in PSII; Q B , secondary quinone electron acceptor in PS II; NIR, near infrared light; ST, single turnover. the form of cyclic electron flow (CEF) operating between PSI and the cytochrome b 6 /f complex possibly via the ferredoxindependent pathway (Aihara et al, 2016), or pseudo-cyclic electron flow of Mehler reaction, that plays a significant role in excess energy dissipation (Roberty et al, 2014). Expression of these pathways, however, may differ significantly between different Symbiodinium genotypes (Aihara et al, 2016;Warner and Suggett, 2016).…”

“…Whilst past studies have applied a combination of biophysical/photobiological methods (e.g., oxygen evolution and uptake measurements, variable chlorophyll a fluorescence and PSI reaction center (P700) redox kinetics) to evaluate the mechanisms underpinning photobiological operation (e.g., Suggett et al, 2008;Roberty et al, 2014;Aihara et al, 2016), most of these measurements require invasive treatment that is impractical on intact corals. Simultaneous measurements of Photosystems I and II electron transport rates [ETR(I) and ETR(II), respectively] in intact corals have been reported (Hoogenboom et al, 2012).…”

Trade-Offs Associated with Photoprotective Green Fluorescent Protein Expression as Potential Drivers of Balancing Selection for Color Polymorphism in Reef Corals

“…Yet, the causes for the reduced growth rates under the two light levels are likely to be very different. A supply of excess light may require an increased investment in several forms of photoprotection, for example in the synthesis of mycosporine-like amino acids (Shick, 2004;Starcevic et al, 2010), antioxidant defense (Lesser and Shick, 1990), or alternative electron transport pathways such as the Mehler reaction (Roberty et al, 2014). Energy may also be invested in repair processes of the photosynthetic apparatus of the symbionts due to photoinhibition and subsequent damage to the D1 protein (Aro et al, 1993;Warner et al, 1999;Gorbunov et al, 2001;Hill and Takahashi, 2014), although it has been suggested that photoinhibiton may protect against oxidative damage caused by excess light (Adams et al, 2008).…”