Diatoms possess an impressive capacity for rapidly inducible thermal dissipation of excess absorbed energy (qE), provided by the xanthophyll diatoxanthin and Lhcx proteins. By knocking out the Lhcx1 ...and Lhcx2 genes individually in Phaeodactylum tricornutum strain 4 and complementing the knockout lines with different Lhcx proteins, multiple mutants with varying qE capacities are obtained, ranging from zero to high values. We demonstrate that qE is entirely dependent on the concerted action of diatoxanthin and Lhcx proteins, with Lhcx1, Lhcx2 and Lhcx3 having similar functions. Moreover, we establish a clear link between Lhcx1/2/3 mediated inducible thermal energy dissipation and a reduction in the functional absorption cross-section of photosystem II. This regulation of the functional absorption cross-section can be tuned by altered Lhcx protein expression in response to environmental conditions. Our results provide a holistic understanding of the rapidly inducible thermal energy dissipation process and its mechanistic implications in diatoms.
The West Antarctic Peninsula (WAP) is a highly productive polar ecosystem where phytoplankton dynamics are regulated by intense bottom-up control from light and iron availability. Rapid climate ...change along the WAP is driving shifts in the mixed layer depth and iron availability. Elucidating the relative role of each of these controls and their interactions is crucial for understanding of how primary productivity will change in coming decades. Using a combination of ultra-high-resolution variable chlorophyll fluorescence together with fluorescence lifetime analyses on the 2017 Palmer Long Term Ecological Research cruise, we mapped the temporal and spatial variability in phytoplankton photophysiology across the WAP. Highest photosynthetic energy conversion efficiencies and lowest fluorescence quantum yields were observed in iron replete coastal regions. Photosynthetic energy conversion efficiencies decreased by ~ 60% with a proportional increase in quantum yields of thermal dissipation and fluorescence on the outer continental shelf and slope. The combined analysis of variable fluorescence and lifetimes revealed that, in addition to the decrease in the fraction of inactive reaction centers, up to 20% of light harvesting chlorophyll-protein antenna complexes were energetically uncoupled from photosystem II reaction centers in iron-limited phytoplankton. These biophysical signatures strongly suggest severe iron limitation of photosynthesis in the surface waters along the continental slope of the WAP.
Phytoplankton in the ocean account for less than 1% of the global photosynthetic biomass, but contribute about 45% of the photosynthetically fixed carbon on Earth. This amazing production/biomass ...ratio implies a very high photosynthetic efficiency. But, how efficiently is the absorbed light used in marine photosynthesis? The introduction of picosecond and then femtosecond lasers for kinetic measurements in mid 1970s to 90 s was a revolution in basic photosynthesis research that vastly improved our understanding of the energy conversion processes in photosynthetic reactions. Until recently, the use of this technology in the ocean was not feasible due to the complexity of related instrumentation and the lack of picosecond lasers suitable for routine operation in the field. However, recent advances in solid-state laser technology and the development of compact data acquisition electronics led to the application of picosecond fluorescence lifetime analyses in the field. Here, we review the development of operational ultrasensitive picosecond fluorescence instruments to infer photosynthetic energy conversion processes in ocean ecosystems. This analysis revealed that, in spite of the high production/biomass ratio in marine phytoplankton, the photosynthetic energy conversion efficiency is exceptionally low—on average, ca. 50% of its maximum potential, suggesting that most of the contemporary open ocean surface waters are extremely nutrient deficient.
Approximately 45% of the photosynthetically fixed carbon on Earth occurs in the oceans in phytoplankton, which account for less than 1% of the world's photosynthetic biomass. This amazing empirical ...observation implies a very high photosynthetic energy conversion efficiency, but how efficiently is the solar energy actually used? The photon energy budget of photosynthesis can be divided into three terms: the quantum yields of photochemistry, fluorescence, and heat. Measuring two of these three processes closes the energy budget. The development of ultrasensitive, seagoing chlorophyll variable fluorescence and picosecond fluorescence lifetime instruments has allowed independent closure on the first two terms. With this closure, we can understand how phytoplankton respond to nutrient supplies on timescales of hours to months and, over longer timescales, to changes in climate.
Constraining photosynthetic energy conversion efficiency in nature is challenging. In principle, two yield measurements must be made simultaneously: photochemistry, fluorescence and/or thermal ...dissipation. We constructed two different, extremely sensitive and precise active fluorometers: one measures the quantum yield of photochemistry from changes in variable fluorescence, the other measures fluorescence lifetimes in the picosecond time domain. By deploying the pair of instruments on eight transoceanic cruises over six years, we obtained over 200 000 measurements of fluorescence yields and lifetimes from surface waters in five ocean basins. Our results revealed that the average quantum yield of photochemistry was approximately 0.35 while the average quantum yield of fluorescence was approximately 0.07. Thus, closure on the energy budget suggests that, on average, approximately 58% of the photons absorbed by phytoplankton in the world oceans are dissipated as heat. This extraordinary inefficiency is associated with the paucity of nutrients in the upper ocean, especially dissolved inorganic nitrogen and iron. Our results strongly suggest that, in nature, most of the time, most of the phytoplankton community operates at approximately half of its maximal photosynthetic energy conversion efficiency because nutrients limit the synthesis or function of essential components in the photosynthetic apparatus.
This article is part of the themed issue ‘Enhancing photosynthesis in crop plants: targets for improvement’.
The Southern Ocean contributes substantially to the global biological carbon pump (BCP). Salps in the Southern Ocean, in particular Salpa thompsoni, are important grazers that produce large, ...fast-sinking fecal pellets. Here, we quantify the salp bloom impacts on microbial dynamics and the BCP, by contrasting locations differing in salp bloom presence/absence. Salp blooms coincide with phytoplankton dominated by diatoms or prymnesiophytes, depending on water mass characteristics. Their grazing is comparable to microzooplankton during their early bloom, resulting in a decrease of ~1/3 of primary production, and negative phytoplankton rates of change are associated with all salp locations. Particle export in salp waters is always higher, ranging 2- to 8- fold (average 5-fold), compared to non-salp locations, exporting up to 46% of primary production out of the euphotic zone. BCP efficiency increases from 5 to 28% in salp areas, which is among the highest recorded in the global ocean.
When diatoms are stressed for inorganic nitrogen they remodel their intermediate metabolism and redirect carbon towards lipid biosynthesis. However, this response comes at a significant cost ...reflected in decreased photosynthetic energy conversion efficiency and growth. Here we explore a molecular genetics approach to restrict the assimilation of inorganic nitrogen by knocking down nitrate reductase (NR). The transformant strain, NR21, exhibited about 50% lower expression and activity of the enzyme but simultaneously accumulated over 40% more fatty acids. However, in contrast to nitrogen‐stressed wild‐type (WT) cells, which grow at about 20% of the rate of nitrogen‐replete cells, growth of NR21 was only reduced by about 30%. Biophysical analyses revealed that the photosynthetic energy conversion efficiency of photosystem II was unaffected in NR21; nevertheless, the plastoquinone pool was reduced by 50% at the optimal growth irradiance while in the WT it was over 90% oxidized. Further analyses reveal a 12‐fold increase in the glutamate/glutamine ratio and an increase NADPH and malonyl‐CoA pool size. Transcriptomic analyses indicate that the knock down resulted in changes in the expression of genes for lipid biosynthesis, as well as the expression of specific transcription factors. Based on these observations, we hypothesize that the allocation of carbon and reductants in diatoms is controlled by a feedback mechanism between intermediate metabolites, the redox state of the plastid and the expression and binding of transcription factors related to stress responses.
During the past several decades, numerous reports from disparate geographical areas have documented an increased frequency of "bleaching" in reef-forming corals. The phenomenon, triggered by ...increased sea surface temperatures, occurs when the cnidarian hosts digest and/or expel their intracellular, photosynthetic dinoflagellate symbionts ("zooxanthellae" in the genus Symbiodinium). Although coral bleaching is often followed by the death of the animal hosts, in some cases, the animal survives and can be repopulated with viable zooxanthellae. The physiological factors determining the ability of the coral to survive bleaching events are poorly understood. In this study, we experimentally established that bleaching and death of the host animal involve a caspase-mediated apoptotic cascade induced by reactive oxygen species produced primarily by the algal symbionts. In addition, we demonstrate that, although some corals naturally suppress caspase activity and significantly reduce caspase concentration under high temperatures as a mechanism to prevent colony death from apoptosis, even sensitive corals can be prevented from dying by application of exogenous inhibitors of caspases. Our results indicate that variability in response to thermal stress in corals is determined by a four-element, combinatorial genetic matrix intrinsic to the specific symbiotic association. Based on our experimental data, we present a working model in which the phenotypic expression of this symbiont/host relationship places a selective pressure on the symbiotic association. The model predicts the survival of the host animals in which the caspase-mediated apoptotic cascade is down-regulated.
Solar radiation absorbed by marine phytoplankton can follow three possible paths. By simultaneously measuring the quantum yields of photochemistry and chlorophyll fluorescence in situ, we calculate ...that, on average, ~60% of absorbed photons are converted to heat, only 35% are directed toward photochemical water splitting, and the rest are reemitted as fluorescence. The spatial pattern of fluorescence yields and lifetimes strongly suggests that photochemical energy conversion is physiologically limited by nutrients. Comparison of in situ fluorescence lifetimes with satellite retrievals of solar-induced fluorescence yields suggests that the mean values of the latter are generally representative of the photophysiological state of phytoplankton; however, the signal-to-noise ratio is unacceptably low in extremely oligotrophic regions, which constitute 30% of the open ocean.
Solar radiation absorbed by marine phytoplankton can follow three possible paths. By simultaneously measuring the quantum yields of photochemistry and chlorophyll fluorescence in situ, we calculate ...that, on average, ~60% of absorbed photons are converted to heat, only 35% are directed toward photochemical water splitting, and the rest are reemitted as fluorescence. The spatial pattern of fluorescence yields and lifetimes strongly suggests that photochemical energy conversion is physiologically limited by nutrients. Comparison of in situ fluorescence lifetimes with satellite retrievals of solar-induced fluorescence yields suggests that the mean values of the latter are generally representative of the photophysiological state of phytoplankton; however, the signal-to-noise ratio is unacceptably low in extremely oligotrophic regions, which constitute 30% of the open ocean.
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