Trophic state alters the mechanism whereby energetic coupling between photosynthesis and respiration occurs in Euglena gracilis.

The coupling between mitochondrial respiration and photosynthesis plays an important role in the energetic physiology of green plants and some secondary-red photosynthetic eukaryotes (diatoms), allowing an efficient CO2 assimilation and optimal growth. Using the flagellate Euglena gracilis, we first tested if photosynthesis-respiration coupling occurs in this species harbouring secondary green plastids (i.e. originated from an endosymbiosis between a green alga and a phagotrophic euglenozoan). Second, we tested how the trophic state (mixotrophy and photoautotrophy) of the cell alters the mechanisms involved in the photosynthesis-respiration coupling. Energetic coupling between photosynthesis and respiration was determined by testing the effect of respiratory inhibitors on photosynthesis, and measuring the simultaneous variation of photosynthesis and respiration rates as a function of temperature (i.e. thermal response curves). The mechanism involved in the photosynthesis-respiration coupling was assessed by combining proteomics, biophysical and cytological analyses. Our work shows that there is photosynthesis-respiration coupling and membrane contacts between mitochondria and chloroplasts in E. gracilis. However, whereas in mixotrophy adjustment of the chloroplast ATP/NADPH ratio drives the interaction, in photoautotrophy the coupling is conditioned by CO2 limitation and photorespiration. This indicates that maintenance of photosynthesis-respiration coupling, through plastic metabolic responses, is key to E. gracilis functioning under changing environmental conditions.

Different levels of energetic coupling between photosynthesis and respiration do not determine the occurrence of adaptive responses of Symbiodiniaceae to global warming.

Disentangling the metabolic functioning of corals' endosymbionts (Symbiodiniaceae) is relevant to understanding the response of coral reefs to warming oceans. In this work, we first question whether there is an energetic coupling between photosynthesis and respiration in Symbiodiniaceae (Symbiodinium, Durusdinium and Effrenium), and second, how different levels of energetic coupling will affect their adaptive responses to global warming. Coupling between photosynthesis and respiration was established by determining the variation of metabolic rates during thermal response curves, and how inhibition of respiration affects photosynthesis. Adaptive (irreversible) responses were studied by exposing two Symbiodinium species with different levels of photosynthesis-respiration interaction to high temperature conditions (32°C) for 1 yr. We found that some Symbiodiniaceae have a high level of energetic coupling; that is, photosynthesis and respiration have the same temperature dependency, and photosynthesis is negatively affected when respiration is inhibited. Conversely, photosynthesis and respiration are not coupled in other species. In any case, prolonged exposure to high temperature caused adjustments in both photosynthesis and respiration, but these changes were fully reversible. We conclude that energetic coupling between photosynthesis and respiration exhibits wide variation amongst Symbiodiniaceae and does not determine the occurrence of adaptive responses in Symbiodiniaceae to temperature increase.

Light and Dehydration but Not Temperature Drive Photosynthetic Adaptations of Basal Streptophytes (Hormidiella, Streptosarcina and Streptofilum) Living in Terrestrial Habitats.

Streptophyte algae are the ancestors of land plants, and several classes contain taxa that are adapted to an aero-terrestrial lifestyle. In this study, four basal terrestrial streptophytes from the class Klebsormidiophyceae, including Hormidiella parvula; two species of the newly described genus Streptosarcina (S. costaricana and S. arenaria); and the newly described Streptofilum capillatum were investigated for their responses to radiation, desiccation and temperature stress conditions. All the strains showed low-light adaptation (Ik < 70 µmol photons m-2 s-1) but differed in photoprotective capacities (such as non-photochemical quenching). Acclimation to enhanced photon fluence rates (160 µmol photons m-2 s-1) increased photosynthetic performance in H. parvula and S. costaricana but not in S. arenaria, showing that low-light adaptation is a constitutive trait for S. arenaria. This lower-light adaptation of S. arenaria was coupled with a higher desiccation tolerance, providing further evidence that dehydration is a selective force shaping species occurrence in low light. For protection against ultraviolet radiation, all species synthesised and accumulated different amounts of mycosporine-like amino acids (MAAs). Biochemically, MAAs synthesised by Hormidiella and Streptosarcina were similar to MAAs from closely related Klebsormidium spp. but differed in retention time and spectral characteristics in S. capillatum. Unlike the different radiation and dehydration tolerances, Hormidiella, Streptosarcina and Streptofilum displayed preferences for similar thermal conditions. These species showed a temperature dependence of photosynthesis similar to respiration, contrasting with Klebsormidium spp. and highlighting an interspecific diversity in thermal requirements, which could regulate species distributions under temperature changes.

Terrestrial adaptation of green algae Klebsormidium and Zygnema (Charophyta) involves diversity in photosynthetic traits but not in CO2 acquisition.

MAIN CONCLUSION: The basal streptophyte Klebsormidium and the advanced Zygnema show adaptation to terrestrialization. Differences are found in photoprotection and resistance to short-term light changes, but not in CO 2 acquisition. Streptophyte green algae colonized land about 450-500 million years ago giving origin to terrestrial plants. We aim to understand how their physiological adaptations are linked to the ecological conditions (light, water and CO2) characterizing modern terrestrial habitats. A new Klebsormidium isolate from a strongly acidic environment of a former copper mine (Schwarzwand, Austria) is investigated, in comparison to Klebsormidium cf. flaccidum and Zygnema sp. We show that these genera possess different photosynthetic traits and water requirements. Particularly, the Klebsormidium species displayed a higher photoprotection capacity, concluded from non-photochemical quenching (NPQ) and higher tolerance to high light intensity than Zygnema. However, Klebsormidium suffered from photoinhibition when the light intensity in the environment increased rapidly, indicating that NPQ is involved in photoprotection against strong and stable irradiance. Klebsormidium was also highly resistant to cellular water loss (dehydration) under low light. On the other hand, exposure to relatively high light intensity during dehydration caused a harmful over-reduction of the electron transport chain, leading to PSII damages and impairing the ability to recover after rehydration. Thus, we suggest that dehydration is a selective force shaping the adaptation of this species towards low light. Contrary to the photosynthetic characteristics, the inorganic carbon (C i ) acquisition was equivalent between Klebsormidium and Zygnema. Despite their different habitats and restriction to hydro-terrestrial environment, the three organisms showed similar use of CO2 and HCO3- as source of Ci for photosynthesis, pointing out a similar adaptation of their CO2-concentrating mechanisms to terrestrial life.

The relative availability of inorganic carbon and inorganic nitrogen influences the response of the dinoflagellate Protoceratium reticulatum to elevated CO2.

This work originates from three facts: (i) changes in CO2 availability influence metabolic processes in algal cells; (ii) Spatial and temporal variations of nitrogen availability cause repercussions on phytoplankton physiology; (iii) Growth and cell composition are dependent on the stoichiometry of nutritional resources. In this study, we assess whether the impact of rising pCO2 is influenced by N availability, through the impact that it would have on the C/N stoichiometry, in conditions of N sufficiency. Our experiments used the dinoflagellate Protoceratium reticulatum, which we cultured under three CO2 regimes (400, 1,000, and 5,000 ppmv, pH of 8.1) and either variable (the NO3- concentration was always 2.5 mmol · L-1 ) or constant (NO3- concentration varied to maintain the same Ci /NO3- ratio at all pCO2 ) Ci /NO3- ratio. Regardless of N availability, cells had higher specific growth rates, but lower cell dry weight and C and N quotas, at elevated CO2 . The carbohydrate pool size and the C/N was unaltered in all treatments. The lipid content only decreased at high pCO2 at constant Ci /NO3- ratio. In the variable Ci /NO3- conditions, the relative abundance of Rubisco (and other proteins) also changed; this did not occur at constant Ci /NO3- . Thus, the biomass quality of P. reticulatum for grazers was affected by the Ci /NO3- ratio in the environment and not only by the pCO2 , both with respect to the size of the main organic pools and the composition of the expressed proteome.

Constitutive cylindrospermopsin pool size in Cylindrospermopsis raciborskii under different light and CO2 partial pressure conditions.

Cylindrospermopsin (CYN) and 7-deoxy-cylindrospermopsin (dCYN) are potent hepatotoxic alkaloids produced by numerous species of cyanobacteria, including the freshwater Cylindrospermopsis raciborskii. C. raciborskii is an invasive cyanobacterium, and the study of how environmental parameters drive CYN production has received significant interest from water managers and health authorities. Light and CO2 affect cell growth and physiology in photoautotrophs, and these are potential regulators of cyanotoxin biosynthesis. In this study, we investigated how light and CO2 affect CYN and dCYN pool size as well as the expression of the key genes, cyrA and cyrK, involved in CYN biosynthesis in a toxic C. raciborskii strain. For cells growing at different light intensities (10 and 100 µmol photons m(-2) s(-1)), we observed that the rate of CYN pool size production (µCYN) was coupled to the cell division rate (µc) during batch culture. This indicated that CYN pool size under our experimental conditions is constant and cell quotas of CYN (QCYN) and dCYN (QdCYN) are fixed. Moreover, a lack of correlation between expression of cyrA and total CYN cell quotas (QCYNs) suggests that the CYN biosynthesis is regulated posttranscriptionally. Under elevated CO2 (1,300 ppm), we observed minor effects on QCYN and no effects on expression of cyrA and cyrK. We conclude that the CYN pool size is constitutive and not affected by light and CO2 conditions. Thus, C. raciborskii bloom toxicity is determined by the absolute abundance of C. raciborskii cells within the water column and the relative abundance of toxic and nontoxic strains.

Photosynthetic characteristics of two Cylindrospermopsis raciborskii strains differing in their toxicity.

We studied the growth and photosynthetic characteristics of a toxic (CS506) and a nontoxic strain (CS509) of the bloom-forming cyanobacterium Cylindrospermopsis raciborskii grown under identical experimental conditions. When exposed to light-saturating growth conditions (100 µmol photons · m(-2)  · s(-1) ), values for maximal photosynthetic capacity (Pmax ) and maximum quantum yield (Fv /Fm ) indicated that both strains had an equal ability to process captured photons and deliver them to PSII reaction centers. However, CS506 grew faster than CS509. This was consistent with its higher light requirement for saturation of photosynthesis (Ik ). Greater shade tolerance of CS509 was indicated by its higher ability to harvest light (α), lower photosynthetic light compensation point (Ic ), and higher chlorophyll a to biovolume ratio. Strain-specific differences were found in relation to non-photochemical quenching, effective absorption cross-sectional area of PSIIα-centers (σPSIIα), and the antenna connectivity parameter of PSIIα (Jcon PSIIα). These findings highlighted differences in the transfer of excitation from phycobilisome/PSII to PSI, on the dependence on different pigments for light harvesting and on the functioning of the PSII reaction centers between the two strains. The results of this study showed that both performance and composition of the photosynthetic apparatus are different between these strains, though with only two strains examined we cannot attribute the performance of strain 506 to its ability to produce cylindrospermopsins. The emphasis on a strain-specific light adaptation/acclimation is crucial to our understanding of how different light conditions (both quantity and quality) can trigger the occurrence of different C. raciborskii strains and control their competition and/or dominance in natural ecosystems.

Elevated CO2 causes changes in the photosynthetic apparatus of a toxic cyanobacterium, Cylindrospermopsis raciborskii.

We studied the physiological acclimation of growth, photosynthesis and CO2-concentrating mechanism (CCM) in Cylindrospermopsis raciborskii exposed to low (present day; L-CO2) and high (1300ppm; H-CO2) pCO2. Results showed that under H-CO2 the cell specific division rate (µc) was higher and the CO2- and light-saturated photosynthetic rates (Vmax and Pmax) doubled. The cells' photosynthetic affinity for CO2 (K0.5CO2) was halved compared to L-CO2 cultures. However, no significant differences were found in dark respiration rates (Rd), pigment composition and light harvesting efficiency (α). In H-CO2 cells, non-photochemical quenching (NPQ), associated with state transitions of the electron transport chain (ETC), was negligible. Simultaneously, a reorganisation of PSII features including antenna connectivity (JconPSIIα), heterogeneity (PSIIα/ß) and effective absorption cross sectional area (σPSIIα/ß) was observed. In relation to different activities of the CCM, our findings suggest that for cells grown under H-CO2: (1) there is down-regulation of CCM activity; (2) the ability of cells to use the harvested light energy is altered; (3) the occurrence of state transitions is likely to be associated with changes of electron flow (cyclic vs linear) through the ETC; (4) changes in PSII characteristics are important in regulating state transitions.