Symbioses with the dinoflagellate Symbiodinium form the foundation of tropical coral reef communities. Symbiodinium photosynthesis fuels the growth of an array of marine invertebrates, including cnidarians such as scleractinian corals and octocorals (e.g., gorgonian and soft corals). Studies examining the symbioses between Caribbean gorgonian corals and Symbiodinium are sparse, even though gorgonian corals blanket the landscape of Caribbean coral reefs. The objective of this study was to compare photosynthetic characteristics of Symbiodinium in four common Caribbean gorgonian species: Pterogorgia anceps, Eunicea tourneforti, Pseudoplexaura porosa, and Pseudoplexaura wagenaari. Symbiodinium associated with these four species exhibited differences in Symbiodinium density, chlorophyll a per cell, light absorption by chlorophyll a, and rates of photosynthetic oxygen production. The two Pseudoplexaura species had higher Symbiodinium densities and chlorophyll a per Symbiodinium cell but lower chlorophyll a specific absorption compared to P. anceps and E. tourneforti. Consequently, P. porosa and P. wagenaari had the highest average photosynthetic rates per cm2 but the lowest average photosynthetic rates per Symbiodinium cell or chlorophyll a. With the exception of Symbiodinium from E. tourneforti, isolated Symbiodinium did not photosynthesize at the same rate as Symbiodinium in hospite. Differences in Symbiodinium photosynthetic performance could not be attributed to Symbiodinium type. All P. anceps (n = 9) and P. wagenaari (n = 6) colonies, in addition to one E. tourneforti and three P. porosa colonies, associated with Symbiodinium type B1. The B1 Symbiodinium from these four gorgonian species did not cluster with lineages of B1 Symbiodinium from scleractinian corals. The remaining eight E. tourneforti colonies harbored Symbiodinium type B1L, while six P. porosa colonies harbored type B1i. Understanding the symbioses between gorgonian corals and Symbiodinium will aid in deciphering why gorgonian corals dominate many Caribbean reefs.

The diversity of extrasolar planets discovered in the last decade shows that we should not be constrained to look for life in environments similar to early or present-day Earth. Super-Earth exoplanets are being discovered with increasing frequency, and some will be able to retain a stable, hydrogen-dominated atmosphere. We explore the possibilities for photosynthesis on a rocky planet with a thin H2-dominated atmosphere. If a rocky, H2-dominated planet harbors life, then that life is likely to convert atmospheric carbon into methane. Outgassing may also build an atmosphere in which methane is the principal carbon species. We describe the possible chemical routes for photosynthesis starting from methane and show that less energy and lower energy photons could drive CH4-based photosynthesis as compared with CO2-based photosynthesis. We find that a by-product biosignature gas is likely to be H2, which is not distinct from the hydrogen already present in the environment. Ammonia is a potential biosignature gas of hydrogenic photosynthesis that is unlikely to be generated abiologically. We suggest that the evolution of methane-based photosynthesis is at least as likely as the evolution of anoxygenic photosynthesis on Earth and may support the evolution of complex life.

Hygrophila polysperma is a heterophyllous amphibious plant. The growth of H. polysperma in submerged conditions is challenging due to the low CO2 environment, increased resistance to gas diffusion, and bicarbonate ion (HCO3 -) being the dominant dissolved inorganic carbon source. The submerged leaves of H. polysperma have significantly higher rates of underwater photosynthesis compared with the terrestrial leaves. 4,4'-Diisothiocyanatostilbene-2,2'-disulfonate (DIDS), an anion exchanger protein inhibitor, and ethoxyzolamide (EZ), an inhibitor of internal carbonic anhydrase, repressed underwater photosynthesis by the submerged leaves. These results suggested that H. polysperma acclimates to the submerged condition by using HCO3 - for photosynthesis. H. polysperma transports HCO3 - into the leaf by a DIDS-sensitive HCO3 - transporter and converted to CO2 by carbonic anhydrase. Additionally, proteome analysis revealed that submerged leaves accumulated fewer proteins associated with C4 photosynthesis compared with terrestrial leaves. This finding suggested that H. polysperma is capable of C4 and C3 photosynthesis in the terrestrial and submerged leaves, respectively. The ratio of phosphoenol pyruvate carboxylase to ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) in the submerged leaves was less than that in the terrestrial leaves. Upon anatomical observation, the terrestrial leaves exhibited a phenotype similar to the Kranz anatomy found among C4 plants; however, chloroplasts in the bundle sheath cells were not located adjacent to the vascular bundles, and the typical Kranz anatomy was absent in submerged leaves. These results suggest that H. polysperma performs proto-Kranz type photosynthesis in a terrestrial environment and shifts from a proto-Kranz type in terrestrial leaves to a HCO3 - use photosynthesis in the submerged environments.

Global estimates of terrestrial gross primary production (GPP) remain highly uncertain, despite decades of satellite measurements and intensive in situ monitoring. We report a new approach for quantifying the near-infrared reflectance of terrestrial vegetation (NIRV). NIRV provides a foundation for a new approach to estimate GPP that consistently untangles the confounding effects of background brightness, leaf area, and the distribution of photosynthetic capacity with depth in canopies using existing moderate spatial and spectral resolution satellite sensors. NIRV is strongly correlated with solar-induced chlorophyll fluorescence, a direct index of photons intercepted by chlorophyll, and with site-level and globally gridded estimates of GPP. NIRV makes it possible to use existing and future reflectance data as a starting point for accurately estimating GPP.

Photosynthesis is a crucial biological process that depends on the interplay of many components. This work analyzed the gene targets for 4 transcription factors: FnrL, PrrA, CrpK and MppG (RSP_2888), which are known or predicted to control photosynthesis in Rhodobacter sphaeroides. Chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-seq) identified 52 operons under direct control of FnrL, illustrating its regulatory role in photosynthesis, iron homeostasis, nitrogen metabolism and regulation of sRNA synthesis. Using global gene expression analysis combined with ChIP-seq, we mapped the regulons of PrrA, CrpK and MppG. PrrA regulates ∼34 operons encoding mainly photosynthesis and electron transport functions, while CrpK, a previously uncharacterized Crp-family protein, regulates genes involved in photosynthesis and maintenance of iron homeostasis. Furthermore, CrpK and FnrL share similar DNA binding determinants, possibly explaining our observation of the ability of CrpK to partially compensate for the growth defects of a ΔFnrL mutant. We show that the Rrf2 family protein, MppG, plays an important role in photopigment biosynthesis, as part of an incoherent feed-forward loop with PrrA. Our results reveal a previously unrealized, high degree of combinatorial regulation of photosynthetic genes and significant cross-talk between their transcriptional regulators, while illustrating previously unidentified links between photosynthesis and the maintenance of iron homeostasis.

To conserve water in arid environments, numerous plant lineages have independently evolved Crassulacean Acid Metabolism (CAM). Interestingly, Isoetes, an aquatic lycophyte, can also perform CAM as an adaptation to low CO2 availability underwater. However, little is known about the evolution of CAM in aquatic plants and the lack of genomic data has hindered comparison between aquatic and terrestrial CAM. Here, we investigate underwater CAM in Isoetes taiwanensis by generating a high-quality genome assembly and RNA-seq time course. Despite broad similarities between CAM in Isoetes and terrestrial angiosperms, we identify several key differences. Notably, Isoetes may have recruited the lesser-known 'bacterial-type' PEPC, along with the 'plant-type' exclusively used in other CAM and C4 plants for carboxylation of PEP. Furthermore, we find that circadian control of key CAM pathway genes has diverged considerably in Isoetes relative to flowering plants. This suggests the existence of more evolutionary paths to CAM than previously recognized.

Bradyrhizobium comprises a diverse group of bacteria with various lifestyles. Although best known for their nodule-based nitrogen-fixation in symbiosis with legumes, a select group of bradyrhizobia are also capable of photosynthesis. This ability seems to be rare among rhizobia, and its origin and evolution in these bacteria remain a subject of substantial debate. Therefore, our aim here was to investigate the distribution and evolution of photosynthesis in Bradyrhizobium using comparative genomics and representative genomes from closely related taxa in the families Nitrobacteraceae, Methylobacteriaceae, Boseaceae and Paracoccaceae. We identified photosynthesis gene clusters (PGCs) in 25 genomes belonging to three different Bradyrhizobium lineages, notably the so-called Photosynthetic, B. japonicum and B. elkanii supergroups. Also, two different PGC architectures were observed. One of these, PGC1, was present in genomes from the Photosynthetic supergroup and in three genomes from a species in the B. japonicum supergroup. The second cluster, PGC2, was also present in some strains from the B. japonicum supergroup, as well as in those from the B. elkanii supergroup. PGC2 was largely syntenic to the cluster found in Rhodopseudomonas palustris and Tardiphaga . Bayesian ancestral state reconstruction unambiguously showed that the ancestor of Bradyrhizobium lacked a PGC and that it was acquired horizontally by various lineages. Maximum-likelihood phylogenetic analyses of individual photosynthesis genes also suggested multiple acquisitions through horizontal gene transfer, followed by vertical inheritance and gene losses within the different lineages. Overall, our findings add to the existing body of knowledge on Bradyrhizobium ’s evolution and provide a meaningful basis from which to explore how these PGCs and the photosynthesis itself impact the physiology and ecology of these bacteria.

Photosynthesis is a unique process that allows independent colonization of the land by plants and of the oceans by phytoplankton. Although the photosynthesis process is well understood in plants, we are still unlocking the mechanisms evolved by phytoplankton to achieve extremely efficient photosynthesis. Here, we combine biochemical, structural and in vivo physiological studies to unravel the structure of the plastid in diatoms, prominent marine eukaryotes. Biochemical and immunolocalization analyses reveal segregation of photosynthetic complexes in the loosely stacked thylakoid membranes typical of diatoms. Separation of photosystems within subdomains minimizes their physical contacts, as required for improved light utilization. Chloroplast 3D reconstruction and in vivo spectroscopy show that these subdomains are interconnected, ensuring fast equilibration of electron carriers for efficient optimum photosynthesis. Thus, diatoms and plants have converged towards a similar functional distribution of the photosystems although via different thylakoid architectures, which likely evolved independently in the land and the ocean.

Evolution of C4 photosynthesis is not distributed evenly in the plant kingdom. Particularly interesting is the situation in the Brassicaceae, because the family contains no C4 species, but several C3-C4 intermediates, mainly in the genus Moricandia Investigation of leaf anatomy, gas exchange parameters, the metabolome, and the transcriptome of two C3-C4 intermediate Moricandia species, M. arvensis and M. suffruticosa, and their close C3 relative M. moricandioides enabled us to unravel the specific C3-C4 characteristics in these Moricandia lines. Reduced CO2 compensation points in these lines were accompanied by anatomical adjustments, such as centripetal concentration of organelles in the bundle sheath, and metabolic adjustments, such as the balancing of C and N metabolism between mesophyll and bundle sheath cells by multiple pathways. Evolution from C3 to C3-C4 intermediacy was probably facilitated first by loss of one copy of the glycine decarboxylase P-protein, followed by dominant activity of a bundle sheath-specific element in its promoter. In contrast to recent models, installation of the C3-C4 pathway was not accompanied by enhanced activity of the C4 cycle. Our results indicate that metabolic limitations connected to N metabolism or anatomical limitations connected to vein density could have constrained evolution of C4 in Moricandia.

Since the basic biochemical mechanisms of photosynthesis are remarkably conserved among plant species, genetic modification approaches have so far been the main route to improve the photosynthetic performance of crops. Yet, phenotypic variation observed in wild species and between varieties of crop species implies there is standing natural genetic variation for photosynthesis, offering a largely unexplored resource to use for breeding crops with improved photosynthesis and higher yields. The reason this has not yet been explored is that the variation probably involves thousands of genes, each contributing only a little to photosynthesis, making them hard to identify without proper phenotyping and genetic tools. This is changing, though, and increasingly studies report on quantitative trait loci for photosynthetic phenotypes. So far, hardly any of these quantitative trait loci have been used in marker assisted breeding or genomic selection approaches to improve crop photosynthesis and yield, and hardly ever have the underlying causal genes been identified. We propose to take the genetics of photosynthesis to a higher level, and identify the genes and alleles nature has used for millions of years to tune photosynthesis to be in line with local environmental conditions. We will need to determine the physiological function of the genes and alleles, and design novel strategies to use this knowledge to improve crop photosynthesis through conventional plant breeding, based on readily available crop plant germplasm. In this work, we present and discuss the genetic methods needed to reveal natural genetic variation, and elaborate on how to apply this to improve crop photosynthesis.

Photosynthesis is involved in the essential process of transforming light energy into chemical energy. Although the interaction between photosynthesis and the circadian clock has been confirmed, the mechanism of how light intensity affects photosynthesis through the circadian clock remains unclear. Here, we propose a first computational model for circadian-clock-controlled photosynthesis, which consists of the light-sensitive protein P, the core oscillator, photosynthetic genes, and parameters involved in the process of photosynthesis. The model parameters were determined by minimizing the cost function ( [Formula: see text]), which is defined by the errors of expression levels, periods, and phases of the clock genes (CCA1, PRR9, TOC1, ELF4, GI, and RVE8). The model recapitulates the expression pattern of the core oscillator under moderate light intensity (100 μmol m -2 s-1). Further simulation validated the dynamic behaviors of the circadian clock and photosynthetic outputs under low (62.5 μmol m-2 s-1) and normal (187.5 μmol m-2 s-1) intensities. When exposed to low light intensity, the peak times of clock and photosynthetic genes were shifted backward by 1-2 hours, the period was elongated by approximately the same length, and the photosynthetic parameters attained low values and showed delayed peak times, which confirmed our model predictions. Our study reveals a potential mechanism underlying the circadian regulation of photosynthesis by the clock under different light intensities in tomato.

Microbial phototrophs, key primary producers on Earth, use H2O, H2, H2S and other reduced inorganic compounds as electron donors. Here we describe a form of metabolism linking anoxygenic photosynthesis to anaerobic respiration that we call 'syntrophic anaerobic photosynthesis'. We show that photoautotrophy in the green sulfur bacterium Prosthecochloris aestaurii can be driven by either electrons from a solid electrode or acetate oxidation via direct interspecies electron transfer from a heterotrophic partner bacterium, Geobacter sulfurreducens. Photosynthetic growth of P. aestuarii using reductant provided by either an electrode or syntrophy is robust and light-dependent. In contrast, P. aestuarii does not grow in co-culture with a G. sulfurreducens mutant lacking a trans-outer membrane porin-cytochrome protein complex required for direct intercellular electron transfer. Syntrophic anaerobic photosynthesis is therefore a carbon cycling process that could take place in anoxic environments. This process could be exploited for biotechnological applications, such as waste treatment and bioenergy production, using engineered phototrophic microbial communities.

Photosynthesis shapes the symbiotic relationships between cnidarians and Symbiodiniaceae algae-with many cnidarian hosts requiring symbiont photosynthate for survival-but little is known about how photosynthesis impacts symbiosis establishment. Here, we show that during symbiosis establishment, infection, proliferation, and maintenance can proceed without photosynthesis, but the ability to do so is dependent on specific cnidarian-Symbiodiniaceae relationships. The evaluation of 31 pairs of symbiotic relationships (five species of Symbiodiniaceae in sea anemone, coral, and jellyfish hosts) revealed that infection can occur without photosynthesis. A UV mutagenesis method for Symbiodiniaceae was established and used to generate six photosynthetic mutants that can infect these hosts. Without photosynthesis, Symbiodiniaceae cannot proliferate in the sea anemone Aiptasia or jellyfish Cassiopea but can proliferate in the juvenile polyps of the coral Acropora. After 6 months of darkness, Breviolum minutum is maintained within Aiptasia, indicating that Symbiodiniaceae maintenance can be independent of photosynthesis. Manipulating photosynthesis provides insights into cnidarian-Symbiodiniaceae symbiosis.

Oxygenic photosynthesis starts with the oxidation of water to O2, a light-driven reaction catalysed by photosystem II. Cyanobacteria are the only prokaryotes capable of water oxidation and therefore, it is assumed that the origin of oxygenic photosynthesis is a late innovation relative to the origin of life and bioenergetics. However, when exactly water oxidation originated remains an unanswered question. Here we use phylogenetic analysis to study a gene duplication event that is unique to photosystem II: the duplication that led to the evolution of the core antenna subunits CP43 and CP47. We compare the changes in the rates of evolution of this duplication with those of some of the oldest well-described events in the history of life: namely, the duplication leading to the Alpha and Beta subunits of the catalytic head of ATP synthase, and the divergence of archaeal and bacterial RNA polymerases and ribosomes. We also compare it with more recent events such as the duplication of Cyanobacteria-specific FtsH metalloprotease subunits and the radiation leading to Margulisbacteria, Sericytochromatia, Vampirovibrionia, and other clades containing anoxygenic phototrophs. We demonstrate that the ancestral core duplication of photosystem II exhibits patterns in the rates of protein evolution through geological time that are nearly identical to those of the ATP synthase, RNA polymerase, or the ribosome. Furthermore, we use ancestral sequence reconstruction in combination with comparative structural biology of photosystem subunits, to provide additional evidence supporting the premise that water oxidation had originated before the ancestral core duplications. Our work suggests that photosynthetic water oxidation originated closer to the origin of life and bioenergetics than can be documented based on phylogenetic or phylogenomic species trees alone.

European mistletoe (Viscum album) is known for its special mode of cellular respiration. It lacks the mitochondrial NADH dehydrogenase complex (Complex I of the respiratory chain) and has restricted capacities to generate mitochondrial adenosine triphosphate (ATP). Here, we present an investigation of the V. album energy metabolism taking place in chloroplasts. Thylakoids were purified from young V. album leaves, and membrane-bound protein complexes were characterized by Blue native polyacrylamide gel electrophoresis as well as by the complexome profiling approach. Proteins were systematically identified by label-free quantitative shotgun proteomics. We identified >1,800 distinct proteins (accessible at https://complexomemap.de/va_leaves), including nearly 100 proteins forming part of the protein complexes involved in the light-dependent part of photosynthesis. The photosynthesis apparatus of V. album has distinct features: (1) comparatively low amounts of Photosystem I; (2) absence of the NDH complex (the chloroplast pendant of mitochondrial Complex I involved in cyclic electron transport (CET) around Photosystem I); (3) reduced levels of the proton gradient regulation 5 (PGR5) and proton gradient regulation 5-like 1 (PGRL1) proteins, which offer an alternative route for CET around Photosystem I; (4) comparable amounts of Photosystem II and the chloroplast ATP synthase complex to other seed plants. Our data suggest a restricted capacity for chloroplast ATP biosynthesis by the photophosphorylation process. This is in addition to the limited ATP supply by the mitochondria. We propose a view on mistletoe's mode of life, according to which its metabolism relies to a greater extent on energy-rich compounds provided by the host trees.

The impact of the combined effects of heat stress, increased vapor pressure deficit (VPD) and water deficit on the physiology of major crops needs to be better understood to help identifying the expected negative consequences of climate change and heat waves on global agricultural productivity. To address this issue, rice, wheat, and maize plants were grown under control temperature (CT, 25°C, VPD 1.8 kPa), and a high temperature (HT, 38°C, VPD 3.5 kPa), both under well-watered (WW) and water deficit (WD) conditions. Gas-exchange measurements showed that, in general, WD conditions affected the leaf conductance to CO2, while growth at HT had a more marked effect on the biochemistry of photosynthesis. When combined, HT and WD had an additive effect in limiting photosynthesis. The negative impacts of the imposed treatments on the processes governing leaf gas-exchange were species-dependent. Wheat presented a higher sensitivity while rice and maize showed a higher acclimation potential to increased temperature. Rubisco and PEPC kinetic constants determined in vitro at 25°C and 38°C were used to estimate Vcmax, Jmax, and Vpmax in the modeling of C3 and C4 photosynthesis. The results here obtained reiterate the need to use species-specific and temperature-specific values for Rubisco and PEPC kinetic constants for a precise parameterization of the photosynthetic response to changing environmental conditions in different crop species.

During the diversification of living organisms, novel adaptive traits usually evolve through the co-option of preexisting genes. However, most enzymes are encoded by gene families, whose members vary in their expression and catalytic properties. Each may therefore differ in its suitability for recruitment into a novel function. In this work, we test for the presence of such a gene recruitment bias using the example of C4 photosynthesis, a complex trait that evolved recurrently in flowering plants as a response to atmospheric CO2 depletion. We combined the analysis of complete nuclear genomes and high-throughput transcriptome data for three grass species that evolved the C4 trait independently. For five of the seven enzymes analyzed, the same gene lineage was recruited across the independent C4 origins, despite the existence of multiple copies. The analysis of a closely related C3 grass confirmed that C4 expression patterns were not present in the C3 ancestors but were acquired during the evolutionary transition to C4 photosynthesis. The significant bias in gene recruitment indicates that some genes are more suitable for a novel function, probably because the mutations they accumulated brought them closer to the characteristics required for the new function.

The D1 protein of Photosystem II (PSII), encoded by the psbA genes, is an indispensable component of oxygenic photosynthesis. Due to strongly oxidative chemistry of PSII water splitting, the D1 protein is prone to constant photodamage requiring its replacement, whereas most of the other PSII subunits remain ordinarily undamaged. In cyanobacteria, the D1 protein is encoded by a psbA gene family, whose members are differentially expressed according to environmental cues. Here, the regulation of the psbA gene expression is first discussed with emphasis on the model organisms Synechococcus sp. and Synechocystis sp. Then, a general classification of cyanobacterial D1 isoforms in various cyanobacterial species into D1m, D1:1, D1:2, and D1' forms depending on their expression pattern under acclimated growth conditions and upon stress is discussed, taking into consideration the phototolerance of different D1 forms and the expression conditions of respective members of the psbA gene family.

Light-driven biocatalysis in recombinant cyanobacteria provides highly atom-efficient cofactor regeneration via photosynthesis, thereby remediating constraints associated with sacrificial cosubstrates. However, despite the remarkable specific activities of photobiocatalysts, self-shading at moderate-high cell densities limits efficient space-time-yields of heterologous enzymatic reactions. Moreover, efficient integration of an artificial electron sink into the tightly regulated network of cyanobacterial electron pathways can be highly challenging. Here, we used C=C bond reduction of 2-methylmaleimide by the NADPH-dependent ene-reductase YqjM as a model reaction for light-dependent biotransformations. Time-resolved NADPH fluorescence spectroscopy allowed direct monitoring of in-cell YqjM activity and revealed differences in NADPH steady-state levels and oxidation kinetics between different genetic constructs. This effect correlates with specific activities of whole-cells, which demonstrated conversions of >99%. Further channelling of electrons toward heterologous YqjM by inactivation of the flavodiiron proteins (Flv1/Flv3) led to a 2-fold improvement in specific activity at moderate cell densities, thereby elucidating the possibility of accelerating light-driven biotransformations by the removal of natural competing electron sinks. In the best case, an initial product formation rate of 18.3 mmol h-1 L-1 was reached, allowing the complete conversion of a 60 mM substrate solution within 4 h.

The practical applications of solar-driven water splitting pivot on significant advances that enable scalable production of robust photoactive films. Here, we propose a proof-of-concept for fabricating robust photoactive films by a particle-implanting technique (PiP) which embeds semiconductor photoabsorbers in the liquid metal. The strong semiconductor/metal interaction enables resulting films efficient collection of photogenerated charges and superior photoactivity. A photoanode of liquid-metal embraced BiVO4 can stably operate over 120 h and retain ~ 70% of activity when scaled from 1 to 64 cm2. Furthermore, a Z-scheme photocatalyst film of liquid-metal embraced BiVO4 and Rh-doped SrTiO3 particles can drive overall water splitting under visible light, delivering an activity 2.9 times higher than that of the control film with gold support and a 110 h stability. These results demonstrate the advantages of the PiP technique in constructing robust and efficient photoactive films for artificial photosynthesis.