Physiological Photoprotection Research Articles

Crawl away from the light! Assessing behavioral and physiological photoprotective mechanisms in tropical solar-powered sea slugs exposed to natural light intensities

Photosynthesizers face a trade-off regarding light: they need enough to maintain high photosynthetic rates, yet excess leads to oxidative stress. Despite this, light and its detrimental effects are chronically underestimated. Solar-powered sea slugs (Sacoglossa: Gastropoda) provide the ideal lens with which to study this trade-off, since they steal chloroplasts from algae but do not inherit photoacclimation and photorepair capacities. We collected three slug species in Curaçao during March and December 2022, comparing the amount of light they received in nature to their optimal light intensities for photosynthesis, and their preferred light intensities. We then investigated behavioral and physiological photoprotection mechanisms to determine if and how they limit light. Finally, we examined oxidative activity under optimal and excess light. All three species were naturally exposed to more light (> 1000 µmol m−2 s−1) than is optimal or preferred. Elysia crispata (kleptoplast retention for > 3 months) is fully exposed to light in nature but reduces the light reaching its kleptoplasts via parapodial shading. Elysia velutinus retains kleptoplasts for ~ 2 weeks and hides in its macroalgal food, limiting light exposure. Both species displayed low amounts of oxidative activity under optimal light, which increased slightly under excess light. Elysia ornata retained chloroplasts for ~ 3 days, lacked observable photoprotection and always displayed high levels of oxidative activity, potentially explaining its limited capacity for kleptoplast retention. Furthermore, both E. velutinus and E. ornata display strong light-avoidance behaviors. This study clearly demonstrates links between high light intensities, photoprotection, and oxidative stress, highlighting the need for future studies that examine aquatic photosynthesizers under natural lighting.

Ecophysiological adjustments of a pine forest to enhance early spring activity in hot and dry climate

Climate change can impose large offsets between the seasonal cycle of photosynthesis and that in solar radiation and temperature which drive it. Ecophysiological adjustments to such offsets in forests growing under hot and dry conditions are critical for maintaining carbon uptake and survival. Here, we investigate the adjustments that underlie the unusually short and intense early spring productive season, under suboptimal radiation and temperature conditions in a semi-arid pine forest.We used eddy covariance flux, meteorological, and close-range sensing measurements, together with leaf chlorophyll content over four years in a semi-arid pine forest to identify the canopy-scale ecophysiological adjustments to the short active season, and long seasonal drought.The results reveal a range of processes that intricately converge to support the early spring peak (March) in photosynthetic activity, including peaks in light use efficiency, leaf chlorophyll content, increase in the absorption of solar radiation, and high leaf scattering properties (indicating optimizing leaf orientation). These canopy-scale adjustments exploit the tradeoffs between the yet increasing temperature and solar radiation, but the concurrently rapidly diminishing soil moisture. In contrast, during the long dry stressful period with rapidly declining photosynthesis under high and potentially damaging solar radiation, physiological photoprotection was conferred by strongly relaxing the early spring adjustments.The results provide evidence for canopy-scale ecophysiological adjustments, detectable by spectral measurements, that support the survival and productivity of a pine forest under the hot and dry conditions, which may apply to large areas in the Mediterranean and other regions in the next few decades due to the current warming and drying trends.

Effect of Light Intensity and Light Quality on Diatom Behavioral and Physiological Photoprotection

In this study, we investigated the different photoregulation responses of diatom dominated natural biofilms to different light intensities and wavelengths, over a tidal cycle in the laboratory. We compared the overall effect of light spectral quality from its light absorption (Qphar) dependent effect. Two different conditions were compared to study photoprotective strategies: sediment (migrational) and without sediment (non-migrational). Three different colors (blue, green and red) and two light intensities (low light, LL at 210 μmol.photons.m-2.s-1and high light, HL at 800 μmol.photons.m-2.s-1) showed strong interactions in inducing behavioral and physiological photoprotection. Non-migrational biofilm non-photochemical quenching (NPQ) was much more reactive to blue HL than red HL while it did not differ in LL. We observed a biphasic NPQ response with a light threshold between 200 and 250 μmol.photons.m-2.s-1 of Qphar that elicited the onset of physiological photoprotection. Similar HL differences were not observed in migrational biofilms due to active vertical migration movements that compensated light saturating effects. Our results showed that within migrational biofilms there was an interaction between light quality and light intensity on cell accumulation pattern at the sediment surface. This interaction led to inverse diatom accumulation patterns between blue and red light at the same intensity: LL (blue +200.67%, red +123.96%), HL (blue +109.15%, red +150.34%). These differences were largely related to the differential amount of light absorbed at different wavelengths and highlighted the importance of using wavelength standardized intensities. Different vertical migration patterns significantly affected the total pigment content measured at the surface, suggesting that cell could migrate downward more than 2mm as a photoregulatory response. Colloidal carbohydrates patterns paralleled the vertical migration movements, highlighting their possible role in diatom motility. Our data strongly suggests a wavelength and Qphar dependent light stress threshold that triggers upward and downward movements to position microphytobenthic diatoms at their optimal depth.

Photoinactivation, repair and the motility-physiology trade-off in microphytobenthos

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 601:41-57 (2018) - DOI: https://doi.org/10.3354/meps12670 Photoinactivation, repair and the motility-physiology trade-off in microphytobenthos Silja Frankenbach*, William Schmidt, Jörg C. Frommlet, João Serôdio Departamento de Biologia and CESAM - Centro de Estudos do Ambiente e do Mar, Universidade de Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal *Corresponding author: s.frankenbach@ua.pt ABSTRACT: Microphytobenthos (MPB) inhabiting intertidal flats of estuaries form highly productive diatom-dominated biofilms. The capacity to sustain such high photosynthetic activity under conditions prone to cause photoinhibition is thought to be enabled by efficient photoprotective mechanisms, the main ones being the xanthophyll cycle (XC) and vertical migration (VM). This study compared the photoprotective capacity of 2 MPB communities inhabiting contrasting sedimentary habitats and relying on distinct light responses: epipelic communities, colonizing muddy sediments and using motility (VM) to regulate light exposure; and epipsammic communities, inhabiting sandier sediments and relying solely on physiological photoprotection (XC). The efficiency of physiological photoprotection of the 2 communities was compared regarding Photosystem II (PSII) photoinactivation caused by light stress. Lincomycin was used to distinguish photoinactivation from counteracting repair. Rate constants of PSII photoinactivation (kPI) and repair (kREC) were determined on cell suspensions, based on the light and time dependence of maximum quantum yield of PSII, Fv/Fm, as measured using multi-actinic imaging fluorometry. The results show that motile species, in comparison to epipsammic ones, are inherently more susceptible to photoinactivation (higher kPI), less dependent on the XC for preventing photodamage (smaller increase of kPI induced by nigericin) and more efficient regarding repair capacity (higher kREC). The distinct strategies exhibited by epipelic and epipsammic communities to cope with light stress support the hypothesized trade-off between photoprotective motility and photophysiology. Motile forms have a diminished physiological capacity for preventing photodamage and compensate using VM and a better repair capacity. Non-motile epipsammic forms rely mostly on physiological mechanisms to optimize photoprotection capacity. KEY WORDS: Microphytobenthos · Diatoms · Photoinactivation · Photoprotection · Repair · Vertical migration · Photoinhibition Full text in pdf format PreviousNextCite this article as: Frankenbach S, Schmidt W, Frommlet JC, Serôdio J (2018) Photoinactivation, repair and the motility-physiology trade-off in microphytobenthos. Mar Ecol Prog Ser 601:41-57. https://doi.org/10.3354/meps12670 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 601. Online publication date: August 09, 2018 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2018 Inter-Research.

Behavioural versus physiological photoprotection in epipelic and epipsammic benthic diatoms

ABSTRACTBenthic diatoms are dominant primary producers in intertidal marine sediments, which are characterized by widely fluctuating and often extreme light conditions. To cope with sudden increases in light intensity, benthic diatoms display both behavioural and physiological photoprotection mechanisms. Behavioural photoprotection is restricted to raphid pennate diatoms, which possess a raphe system that enables motility and hence positioning in sediment light gradients (e.g. via vertical migration into the sediment). The main physiological photoprotection mechanism is to dissipate excess light energy as heat, measured as Non-Photochemical Quenching (NPQ) of chlorophyll fluorescence. A trade-off between vertical migration and physiological photoprotection (NPQ) in benthic diatoms has been hypothesized before, but this has never been formally tested. We exposed five epipelic diatom species (which move in between sediment particles) and four epipsammic diatom species (which live in close association with individual sand grains) to high light conditions, and characterized both NPQ and the relative magnitude of the migratory response to high light. Our results reveal the absence of a significant downward migratory response in an araphid diatom, but also in several raphid epipsammic diatoms, while all epipelic species showed a significant migratory response upon high light exposure. In all epipsammic species the upregulation of NPQ was rapid and pronounced; NPQ relaxation in low light conditions, however, occurred faster in the araphid diatom, compared with the raphid epipsammic species. In contrast, all epipelic species lacked a strong and flexible NPQ response and showed higher susceptibility to photodamage when not able to migrate. While overall our results support the vertical migration-NPQ trade-off, the lack of strong relationships between the capacity for vertical migration and NPQ within the epipsammic and epipelic groups suggests that other factors as well, such as cell size, substrate type and photoacclimation, may influence photoprotective strategies.

Behavioral and physiological photoresponses to light intensity by intertidal microphytobenthos

Behavioral and physiological responses to light are the two major mechanisms by which natural microphytobenthic assemblages adapt to the intertidal environment and protect themselves from light stress. The present study investigated these photoresponses with different light intensities over 8 h of illumination, and used a specific inhibitor (Latrunculin A, Lat A) for migration to compare migratory and non-migratory microphytobenthos (MPB). Photosynthetic activity was detected using rapid light curves and induction curves by chlorophyll fluorescence. It showed distinct variation in migratory responses to different light intensities; high light induced downward migration to avoid photoinhibition, and low and medium light (50–250 μmol/(m2·s)) promoted upward migration followed by downward migration after certain period of light exposure. No significant difference in non-photochemical quenching (NPQ) or PSII maximal quantum yield (Fv/Fm) was detected between low and medium light irradiance, possibly indicating that only high light influences the photosynthetic capability of MPB. Decreased photosynthetic activity, indicated by three parameters, the maximum relative electron transport rate (rETR max), minimum saturating irradiance (Ek) and light utilization coefficient (α), was observed in MPB after exposure to prolonged illumination under low and medium light. Lat A effectively inhibited the migration of MPB in all light treatments and induced lower Fv/Fm under high light (500 and 100 μmol/(m2·s)) and prolonged illumination at 250 μmol/(m2·s), but did not significantly influence Fv/Fm under low light (0–100 μmol/(m2·s)) or NPQ. The increase of NPQ in Lat A treatments with time implied that the MPB assemblages can recover their physiological photoprotection capacity to adapt to light stress. Non-migratory MPB exhibited lower light use efficiency (lower α) and lower maximum photosynthetic capacity (lower rETR max) than migratory MPB under light intensities above 250 μmol/(m2·s) after 4.0 h illumination.

Regulation of Intertidal Microphytobenthos Photosynthesis Over a Diel Emersion Period Is Strongly Affected by Diatom Migration Patterns.

Changes in biomass and photosynthesis of a diatom-dominated microphytobenthos (MPB) intertidal community were studied over a diel emersion period using a combination of O2 and scalar irradiance microprofiling, variable chlorophyll (Chl) fluorescence, and pigment analysis. The MPB biomass in the photic zone (0–0.5 mm) of the sediment exposed to low irradiance (150 μmol photons m-2 s-1) showed a >2-fold increase during the first hours of the emersion period, reaching >0.2 mg Chl a cm-3. Concentrations of Chl a started to decrease half-way through the emersion period, almost 2 h before tidal inundation. Similarly, O2 concentrations and volumetric gross photosynthesis in the photic zone increased during the first half of the emersion period and then decreased toward the timing of incoming tide/darkness. The results suggest that intertidal MPB community-level photosynthesis is mainly controlled by changes in the productive biomass of the photic zone determined by cell migration. A diel pattern in the photosynthesis vs. irradiance parameters α (photosynthetic efficiency at limiting irradiance) and ETRmax (photosynthetic capacity at saturating irradiance) was also observed, suggesting photoacclimation of MPB. Under high light exposure (2000 μmol photons m-2 s-1), lower α, ETRmax and sediment O2 concentrations were observed when cell migration was inhibited with the diatom motility inhibitor latrunculin A (Lat A), showing that migration is also used by MPB to maximize photosynthesis by reducing exposure to potentially photoinhibitory light levels. A higher de-epoxidation state in sediment treated with Lat A indicates that the involvement of the xanthophyll cycle in physiological photoprotection is more relevant in MPB when cells are inhibited from migrating. In the studied diatom-dominated MPB intertidal community, cell migration seems to be the key factor regulating photosynthesis over a diel emersion period and upon changes in light exposure.

Microambientes lumínico y morfología y fisiología foliar de Bromelia karatas (Bromeliaceae) en una selva baja caducifolia de Yucatán, México

El metabolismo ácido de las crasuláceas es una adaptación de algunas plantas a condiciones de escasez de agua o bióxido de carbono y está relacionado con mecanismos de respuesta anatómicos, morfológicos y fi siológicos para tolerar períodos prolongados de sequía. La luz puede afectar diferentes procesos metabólicos, fisiológicos y estructurales de las plantas cuando es excesiva, por lo que en ambientes cambiantes, como en las selvas caducifolias, las hojas presentan respuestas de fotoprotección. El objetivo de este trabajo fue determinar esas respuestas, en dos microambientes de luz y dos temporadas del año, en una bromeliácea terrestre (Bromelia karatas) de la selva baja caducifolia en el Parque Nacional Dzibilchaltún, Yucatán. Las características morfológicas y fisiológicas de las hojas refl ejaron la influencia del ambiente, lo que les permitió conservar potenciales hídricos diurnos elevados y minimizar la pérdida de agua para mantener la fotosíntesis. Estas características, en conjunto con las espinas foliares y el crecimiento asexual de esta especie, pueden ayudar a explicar su alto valor de importancia ecológica en esta selva baja caducifolia.

On the relationship between non-photochemical quenching and photoprotection of Photosystem II

Non-photochemical quenching (NPQ) of chlorophyll fluorescence is thought to be an indicator of an essential regulation and photoprotection mechanism against high-light stress in photosynthetic organisms. NPQ is typically characterized by modulated pulse fluorometry and it is often assumed implicitly to be a good proxy for the actual physiological photoprotection capacity of the organism. Using the results of previously published ultrafast fluorescence measurements on intact leaves of w.t. and mutants of Arabidopsis (Holzwarth et al. 2009) we have developed exact relationships for the fluorescence quenching and the corresponding Photosystem II acceptor side photoprotection effects under NPQ conditions. The approach based on the exciton–radical pair equilibrium model assumes that photodamage results from triplet states generated in the reaction center. The derived relationships allow one to distinguish and determine the individual and combined quenching as well as photoprotection contributions of each of the multiple NPQ mechanisms. Our analysis shows inter alia that quenching and photoprotection are not linearly related and that antenna detachment, which can be identified with the so-called qE mechanism, contributes largely to the measured fluorescence quenching but does not correspond to the most efficient photoprotective response. Conditions are formulated which allow simultaneously the maximal photosynthetic electron flow as well as maximal acceptor side photoprotection. It is shown that maximal photoprotection can be achieved if NPQ is regulated in such a way that PSII reaction centers are open under given light conditions. The results are of fundamental importance for a proper interpretation of the physiological relevance of fluorescence-based NPQ data.

Evidence for leaf fold to remedy the deficiency of physiological photoprotection for photosystem II

An interesting phenomenon is that some light-demanding plants fold their leaves when exposed to high light. Since high light could induce selective photodamage to photosystem II (PSII), we suggest that the leaves fold themselves to diminish the absorption of light energy and remedy the deficiency of physiological photoprotection for PSII. To test this hypothesis, we determined light responses of non-photochemical quenching (NPQ) and cyclic electron flow (CEF) and the effect of high light on PSII activity in Microcos paniculata (non-foldable species) and Bauhinia tenuiflora (foldable species). Under high light B. tenuiflora showed much lower NPQ and CEF than M. paniculata. Meanwhile, the excess light energy that cannot be harmlessly dissipated in B. tenuiflora was more compared with that in M. paniculata. After exposure to a high light of 1,900μmol photons m(-2)s(-1) for 2h, the maximum quantum yield of PSII, as estimated by variable to maximal fluorescence (F (v) /F (m)) decreased from 0.7 to 0.52 in the foldable species B. tenuiflora but was stable at 0.7 in the nonfoldable species M. paniculata. These results indicate that the foldable species B. tenuiflora has more sensitivity of PSII to high light stress than the nonfoldable species M. paniculata, partly as a result of less CEF and NPQ in B. tenuiflora. Our results suggest that sun leaves fold themselves under high light to remedy the deficiency of physiological photoprotection for PSII.

Effects of short-term manipulations in iron nutrition of Nodularia spumigena from near-coast blooms (southern Baltic Sea)

Randomly collected, dense cyanobacterial bloom material of coastal origin showed a differential response to short-term manipulations of iron availability in microcosms under natural light conditions. Temporally significant iron-mediated promotion of net photosynthetic performance was detected by oxygen saturation and pH measurements in two experiments, although surplus iron was rapidly transformed to insoluble forms even during short incubation periods of 2 days. Stimulating effects of added iron were more pronounced at continuously high incident irradiance. A bi-directional approach of iron manipulation comprising either iron or siderophore addition revealed a medium level of iron starvation in near-coast Nodularia bloom material. Significant stimulation of the quantum efficiency of photosystem II (up to 100%) also indicated photosynthetic performance as a main target of iron fertilization. Missing treatment effects in two other experiments coincided with partially decaying bloom material. Sunscreen effects of iron minerals in fertilized microcosms were unlikely due to insignificant shifts of cellular chlorophyll:carotenoid ratios. The stimulation by iron was most probably linked to physiological photoprotection mechanisms. This link can support the understanding of less consistent iron fertilization effects on the toxic cyanobacterium Nodularia spumigena among the few studies on summer phytoplankton of the Baltic Sea.

Tradeoffs Between Irradiance Capture and Avoidance in Semi-arid Environments Assessed with a Crown Architecture Model

Plants in arid environments cope with stress from excessive irradiance by physiological photoprotection of the photosynthetic apparatus and by structurally reducing the leaf area exposed to the sun (structural photoprotection). We assessed the ecological relevance of structural photoprotection in two plants of contrasting architecture co-occurring in a semi-arid environment, using the three-dimensional canopy model YPLANT. We compared the role of crown geometry in avoiding excessive radiation, analysed the costs of structural photoprotection in terms of reduction of potential carbon gain, and compared these costs with those due to seasonal constraints of photosynthesis and tissue ageing. The results of the model simulations indicated that canopy architecture ofStipa tenacissima(a tussock grass) andRetama sphaerocarpa(a leafless leguminous shrub) minimized the risk of overheating and photo-oxidative destruction of the photosynthetic apparatus with steeply oriented foliage and moderate self-shading. But this structural photoprotection imposed an increased cost in terms of potential carbon gain. Diurnal and seasonal patterns of light interception by the crown of these plants translated into a simulated potential carbon gain only half that of an equivalent, horizontal photosynthetic surface. This reduction in potential carbon gain, due to irradiance avoidance, was similar to that imposed by water shortage.S. tenacissima,which ceases photosynthetic activity during periods of drought, exhibited more structural avoidance of irradiance thanR. sphaerocarpa,which remains active throughout the year. This illustrates the influence of the capacity of plants to utilize light for carbon fixation on the trade-offs between irradiance capture and avoidance. Structural avoidance of excessive radiation efficiently prevents the risk of damage by intense irradiance, has no special maintenance costs, and is biomechanically cheaper than enhanced light harvesting by a horizontal canopy, which points to structural photoprotection as a very effective strategy to cope with high irradiance stress in poor and adverse habitats.