Search

Diatoms are an important group of algae, contributing nearly 40% of total marine photosynthetic activity. However, the specific molecular agents and transporters underpinning the metabolic efficiency of the diatom plastid remain to be revealed. We performed in silico analyses of 70 predicted plastid transporters identified by genome-wide searches of Phaeodactylum tricornutum. We considered similarity with Arabidopsis thaliana plastid transporters, transcriptional co-regulation with genes encoding core plastid metabolic pathways and with genes encoded in the mitochondrial genomes, inferred evolutionary histories using single-gene phylogeny, and environmental expression trends using Tara Oceans meta-transcriptomics and meta-genomes data. Our data reveal diatoms conserve some of the ion, nucleotide and sugar plastid transporters associated with plants, such as non-specific triose phosphate transporters implicated in the transport of phosphorylated sugars, NTP/NDP and cation exchange transporters. However, our data also highlight the presence of diatom-specific transporter functions, such as carbon and amino acid transporters implicated in intricate plastid-mitochondria crosstalk events. These confirm previous observations that substrate non-specific triose phosphate transporters (TPT) may exist as principal transporters of phosphorylated sugars into and out of the diatom plastid, alongside suggesting probable agents of NTP exchange. Carbon and amino acid transport may be related to intricate metabolic plastid-mitochondria crosstalk. We additionally provide evidence from environmental meta-transcriptomic/metagenomic data that plastid transporters may underpin diatom sensitivity to ocean warming, and identify a diatom plastid transporter (J43171) whose expression may be positively correlated with temperature. [ABSTRACT FROM AUTHOR]

Summary: Diatoms are successful phytoplankton clades able to acclimate to changing environmental conditions, including e.g. variable light intensity. Diatoms are outstanding at dissipating light energy exceeding the maximum photosynthetic electron transfer (PET) capacity via the nonphotochemical quenching (NPQ) process. While the molecular effectors of NPQ as well as the involvement of the proton motive force (PMF) in its regulation are known, the regulators of the PET/PMF relationship remain unidentified in diatoms.We generated mutants of the H+/K+ antiporter KEA3 in the model diatom Phaeodactylum tricornutum.Loss of KEA3 activity affects the PET/PMF coupling and NPQ responses at the onset of illumination, during transients and in steady‐state conditions. Thus, this antiporter is a main regulator of the PET/PMF coupling. Consistent with this conclusion, a parsimonious model including only two free components, KEA3 and the diadinoxanthin de‐epoxidase, describes most of the feedback loops between PET and NPQ.This simple regulatory system allows for efficient responses to fast (minutes) or slow (e.g. diel) changes in light environment, thanks to the presence of a regulatory calcium ion (Ca2+)‐binding domain in KEA3 modulating its activity. This circuit is likely tuned by the NPQ‐effector proteins, LHCXs, providing diatoms with the required flexibility to thrive in different ocean provinces. [ABSTRACT FROM AUTHOR]

Light is the ultimate source of energy for photosynthetic organisms, but respiration is fundamental for supporting metabolism during the night or in heterotrophic tissues. In this work, we isolated Physcomitrella (Physcomitrium patens) plants with altered respiration by inactivating Complex I (CI) of the mitochondrial electron transport chain by independently targeting on two essential subunits. Inactivation of CI caused a strong growth impairment even in fully autotrophic conditions in tissues where all cells are photosynthetically active, demonstrating that respiration is essential for photosynthesis. CI mutants showed alterations in the stoichiometry of respiratory complexes while the composition of photosynthetic apparatus was substantially unaffected. CI mutants showed altered photosynthesis with high activity of both Photosystems I and II, likely the result of high chloroplast ATPase activity that led to smaller ΔpH formation across thylakoid membranes, decreasing photosynthetic control on cytochrome b6f in CI mutants. These results demonstrate that alteration of respiratory activity directly impacts photosynthesis in P. patens and that metabolic interaction between organelles is essential in their ability to use light energy for growth. [ABSTRACT FROM AUTHOR]

Algae belonging to the Microchloropsis genus are promising organisms for biotech purposes, being able to accumulate large amounts of lipid reserves. These organisms adapt to different trophic conditions, thriving in strict photoautotrophic conditions, as well as in the concomitant presence of light plus reduced external carbon as energy sources (mixotrophy). In this work, we investigated the mixotrophic responses of Microchloropsis gaditana (formerly Nannochloropsis gaditana). Using the Biolog growth test, in which cells are loaded into multiwell plates coated with different organic compounds, we could not find a suitable substrate for Microchloropsis mixotrophy. By contrast, addition of the Lysogeny broth (LB) to the inorganic growth medium had a benefit on growth, enhancing respiratory activity at the expense of photosynthetic performances. To further dissect the role of respiration in Microchloropsis mixotrophy, we focused on the mitochondrial alternative oxidase (AOX), a protein involved in energy management in other algae prospering in mixotrophy. Knocking-out the AOX1 gene by transcription activator-like effector nuclease (TALE-N) led to the loss of capacity to implement growth upon addition of LB supporting the hypothesis that the effect of this medium was related to a provision of reduced carbon. We conclude that mixotrophic growth in Microchloropsis is dominated by respiratory rather than by photosynthetic energetic metabolism and discuss the possible reasons for this behavior in relationship with fatty acid breakdown via β-oxidation in this oleaginous alga. [ABSTRACT FROM AUTHOR]

Alternative electron pathways contribute to regulation of photosynthetic light reactions to adjust to metabolic demands in dynamic environments. The chloroplast NADH dehydrogenase-like (NDH) complex mediates the cyclic electron transport pathway around PSI in different cyanobacteria, algae, and plant species, but it is not fully conserved in all photosynthetic organisms. In order to assess how the physiological role of this complex changed during plant evolution, we isolated Physcomitrella patens lines knocked out for the NDHM gene that encodes a subunit fundamental for the activity of the complex. ndhm knockout mosses indicated high PSI acceptor side limitation upon abrupt changes in illumination. In P. patens , pseudo-cyclic electron transport mediated by flavodiiron proteins (FLVs) was also shown to prevent PSI over-reduction in plants exposed to light fluctuations. flva ndhm double knockout mosses had altered photosynthetic performance and growth defects under fluctuating light compared with the wild type and single knockout mutants. The results showed that while the contribution of NDH to electron transport is minor compared with FLV, NDH still participates in modulating photosynthetic activity, and it is critical to avoid PSI photoinhibition, especially when FLVs are inactive. The functional overlap between NDH- and FLV-dependent electron transport supports PSI activity and prevents its photoinhibition under light variations. [ABSTRACT FROM AUTHOR]

The regulation of photosynthesis is crucial to efficiently support the assimilation of carbon dioxide and to prevent photodamage. One key regulatory mechanism is the pseudo-cyclic electron flow (PCEF) mediated by class-C flavodiiron proteins (FLVs). These enzymes use electrons coming from Photosystem I (PSI) to reduce oxygen to water, preventing over-reduction in the acceptor side of PSI. FLVs are widely distributed among organisms performing oxygenic photosynthesis and they have been shown to be fundamental in many different conditions such as fluctuating light, sulfur deprivation and plant submersion. Moreover, since FLVs reduce oxygen they can help controlling the redox status of the cell and maintaining the microoxic environment essential for processes such as nitrogen fixation in cyanobacteria. Despite these important roles identified in various species, the genes encoding for FLV proteins have been lost in angiosperms where their activity could have been at least partially compensated by a more efficient cyclic electron flow (CEF). The present work reviews the information emerged on FLV function, analyzing recent structural data that suggest FLV could be regulated through a conformational change. [ABSTRACT FROM AUTHOR]

Photosynthetic organisms support cell metabolism by harvesting sunlight and driving the electron transport chain at the level of thylakoid membranes. Excitation energy and electron flow in the photosynthetic apparatus is continuously modulated in response to dynamic environmental conditions. Alternative electron flow around photosystem I plays a seminal role in this regulation contributing to photoprotection by mitigating overreduction of the electron carriers. Different pathways of alternative electron flow coexist in the moss Physcomitrella patens, including cyclic electron flow mediated by the PGRL1/PGR5 complex and pseudo‐cyclic electron flow mediated by the flavodiiron proteins FLV. In this work, we generated P. patens plants carrying both pgrl1 and flva knock‐out mutations. A comparative analysis of the WT, pgrl1, flva, and pgrl1 flva lines suggests that cyclic and pseudo‐cyclic processes have a synergic role in the regulation of photosynthetic electron transport. However, although both contribute to photosystem I protection from overreduction by modulating electron flow following changes in environmental conditions, FLV activity is particularly relevant in the first seconds after a light change whereas PGRL1 has a major role upon sustained strong illumination. Photosynthesis is continuously modulated in response to dynamic environmental conditions also through modulation of electron transport. In this work, we applied a multidisciplinary approach to demonstrate the fundamental role of mechanisms for regulation of photosynthetic electron transport in plant response to light dynamics. In their absence, photosynthetic apparatus is damaged with strong negative consequences on growth. [ABSTRACT FROM AUTHOR]

ContentsSummary105I.Introduction105II.Diversity of molecular mechanisms for regulation of photosynthetic electron transport106III.Role of FLVs in the regulation of photosynthesis in eukaryotes107IV.Why were FLVs lost in angiosperms?108V.Conclusions108Acknowledgements109References109 Summary: Photosynthetic electron transport requires continuous modulation to maintain the balance between light availability and metabolic demands. Multiple mechanisms for the regulation of electron transport have been identified and are unevenly distributed among photosynthetic organisms. Flavodiiron proteins (FLVs) influence photosynthetic electron transport by accepting electrons downstream of photosystem I to reduce oxygen to water. FLV activity has been demonstrated in cyanobacteria, green algae and mosses to be important in avoiding photosystem I overreduction upon changes in light intensity. FLV‐encoding sequences were nevertheless lost during evolution by angiosperms, suggesting that these plants increased the efficiency of other mechanisms capable of accepting electrons from photosystem I, making the FLV activity for protection from overreduction superfluous or even detrimental for photosynthetic efficiency. [ABSTRACT FROM AUTHOR]

The adaptation to dehydration and rehydration cycles represents a key step in the evolution of photosynthetic organisms and requires the development of mechanisms by which to sense external stimuli and translate them into signaling components. In this study, we used genetically encoded fluorescent sensors to detect specific transient increases in the Ca2+ concentration in the moss Physcomitrella patens upon dehydration and rehydration treatment. Observation of the entire plant in a single time-series acquisition revealed that various cell types exhibited different sensitivities to osmotic stress and that Ca2+ waves originated from the basal part of the gametophore and were directionally propagated towards the top of the plant. Under similar conditions, the vascular plant Arabidopsis thaliana exhibited Ca2+ waves that propagated at a higher speed than those of P. patens. Our results suggest that systemic Ca2+ propagation occurs in plants even in the absence of vascular tissue, even though the rates can be different. [ABSTRACT FROM AUTHOR]

Diatoms are an important group of algae, contributing nearly 40% of total marine photosynthetic activity. However, the specific molecular agents and transporters underpinning the metabolic efficiency of the diatom plastid remain to be revealed. We performed in silico analyses of 70 predicted plastid transporters identified by genome-wide searches of Phaeodactylum tricornutum . We considered similarity with Arabidopsis thaliana plastid transporters, transcriptional co-regulation with genes encoding core plastid metabolic pathways and with genes encoded in the mitochondrial genomes, inferred evolutionary histories using single-gene phylogeny, and environmental expression trends using Tara Oceans meta-transcriptomics and meta-genomes data. Our data reveal diatoms conserve some of the ion, nucleotide and sugar plastid transporters associated with plants, such as non-specific triose phosphate transporters implicated in the transport of phosphorylated sugars, NTP/NDP and cation exchange transporters. However, our data also highlight the presence of diatom-specific transporter functions, such as carbon and amino acid transporters implicated in intricate plastid-mitochondria crosstalk events. These confirm previous observations that substrate non-specific triose phosphate transporters (TPT) may exist as principal transporters of phosphorylated sugars into and out of the diatom plastid, alongside suggesting probable agents of NTP exchange. Carbon and amino acid transport may be related to intricate metabolic plastid-mitochondria crosstalk. We additionally provide evidence from environmental meta-transcriptomic/meta- genomic data that plastid transporters may underpin diatom sensitivity to ocean warming, and identify a diatom plastid transporter (J43171) whose expression may be positively correlated with temperature., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2022 Liu, Storti, Finazzi, Bowler and Dorrell.)