Induction of photosynthesis under anoxic condition in Thalassiosira pseudonana and Euglena gracilis: interactions between fermentation and photosynthesis.

peer reviewed[en] INTRODUCTION: In their natural environment, microalgae can be transiently exposed to hypoxic or anoxic environments. Whereas fermentative pathways and their interactions with photosynthesis are relatively well characterized in the green alga model Chlamydomonas reinhardtii, little information is available in other groups of photosynthetic micro-eukaryotes. In C. reinhardtii cyclic electron flow (CEF) around photosystem (PS) I, and light-dependent oxygen-sensitive hydrogenase activity both contribute to restoring photosynthetic linear electron flow (LEF) in anoxic conditions. METHODS: Here we analyzed photosynthetic electron transfer after incubation in dark anoxic conditions (up to 24 h) in two secondary microalgae: the marine diatom Thalassiosira pseudonana and the excavate Euglena gracilis. RESULTS: Both species showed sustained abilities to prevent over-reduction of photosynthetic electron carriers and to restore LEF. A high and transient CEF around PSI was also observed specifically in anoxic conditions at light onset in both species. In contrast, at variance with C. reinhardtii, no sustained hydrogenase activity was detected in anoxic conditions in both species. DISCUSSION: Altogether our results suggest that another fermentative pathway might contribute, along with CEF around PSI, to restore photosynthetic activity in anoxic conditions in E. gracilis and T. pseudonana. We discuss the possible implication of the dissimilatory nitrate reduction to ammonium (DNRA) in T. pseudonana and the wax ester fermentation in E. gracilis

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

Fermentation pathways and their interactions with photosynthesis in the marine diatom T. pseudonana: proteomic and biophysics approaches

The glycolysis associated with mitochondrial oxidative phosphorylation is the process by which the vast majority of eukaryotes produces ATP from sugar. Under hypoxic or anoxic conditions, fermentation pathways allow to maintain glycolytic activity by reducing alternative electron acceptors (other than O2) while generating various fermentation by-products. Anaerobic fermentation and photosynthesis coexist when organisms experience hypoxia or anoxia in their natural environment (e.g. marine sediments, eutrophic waters). In photosynthetic microeukaryotes, the detailed study of anaerobic metabolic pathways is limited to few freshwater model organisms such as Chlamydomonas reinhardtii (1). Based a previous genomic survey, Thalassiosira pseudonana, a centric marine diatom would contain a large variety of fermentation pathways (2). In our work, we studied the fermentation pathways and their interactions with photosynthesis in T. pseudonana. We first show that there are different waves of protein expression during the first 24 hours in anoxia in the dark. Several fermentative metabolites are also detected (H2, succinate), and our data suggest the existence of a bacterial fermentative pathway leading to butyrate production. The availability in photosynthetic electron acceptors is reduced but not null after 24h in anoxia. This suggests that at least one fermentative pathway is able to reoxidize photosynthetic electron acceptors, as it was previously shown for hydrogenase activity in C. reinhardtii (3). Finally, by comparing PSI and PSII activity, we evidence that a high and transient cyclic electron flow (CEF) around PSI is key to resume PSII electron transfer in anoxic condition. Overall, our results reveal regulatory mechanisms (CEF and fermentation pathways) that may help T. pseudonana cope with hypoxic or anoxic environments. References: (1) Muller, M. et al. (2012). Microbiol Mol Biol Rev, 76, 444-495 (2) Atteia et al. (2013). Biochim Biophys Acta - Bioenerg 1827: 210–223 (3) Godaux et al. (2013). Int. J. Hydrog. Energy, 38: 1826-183