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

Abstract

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 CO 2 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 CO 2 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.

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

“…Our results therefore indicate that CEF around PSI is large but transient under anoxic conditions, whereas in comparison it could be very weak in oxic conditions in both T. pseudonana and E. gracilis . This is in line with our previous studies indicating that CEF around PSI is very low in oxic condition in diatoms ( Bailleul et al., 2015 ) and in E. gracilis ( Gain et al., 2021 ). CEF is also higher in anoxic conditions than in oxic conditions in C. reinhardtii ( Alric, 2010 ), suggesting that the mechanisms behind LEF and CEF partitioning may be broadly shared in photosynthetic eukaryotes.…”

“…In E. gracilis and T. pseudonana , this raises the question of the role of hydrogenase in photosynthetic electron transport under anoxic conditions. In addition, previous studies indicated that CEF around PSI is very low in oxic condition in diatoms ( Bailleul et al., 2015 ) and in E. gracilis ( Gain et al., 2021 ). However, the activity of CEF under anoxic conditions has never been studied.…”

Weak acids produced during anaerobic respiration suppress both photosynthesis and aerobic respiration

“…Nevertheless, in the case of Chlamydomonas , the chlororespiratory enzymes PTOX and NDA2 are probably not electrogenic as they are both monotopic and chloroplast stroma-exposed 54 . Likewise, ATP synthase running in reverse mode could lower the lumen pH thanks to ATP hydrolysis 55 and it has been demonstrated that ATP (of mitochondrial origin) hydrolysis by chloroplastic ATP synthase occurs in dark oxic conditions in several species (Diatoms 13 , Phaemonas 56 , Euglens 14 ), however, in anoxic conditions, this is unlikely to happen because mitochondrial respiration is abolished. As anticipated, using ptox2 , nda2 and FUD50 mutants, we unambiguously demonstrated that the lumen acidification in the presence of weak acids does not originate from chlororespiration nor from ATP hydrolysis.…”

“…Additionally, a tight energetic coupling was found between chloroplasts and mitochondria in Chlamydomonas via a redistribution of reducing power 11 , 12 . In phylogenetically distant microalgae such as diatoms or Euglenas, metabolite exchange between aerobic pathways has also been shown 13 , 14 .…”

Growth parameters and responses of green algae across a gradient of phototrophic, mixotrophic and heterotrophic conditions

“…Other studies suggested maintenance of photosynthesis in mixotrophic growth may depend on species and/or organic substrate ( Kamalanathan et al, 2017 ; Cecchin et al, 2018 ). Organic C supply can even support photosynthesis by reducing photoinhibition or improving CO 2 supply ( Xie et al, 2016 ; Curien et al, 2021 ; Gain et al, 2021 ) and Chlamydomonas cells also show regulation of inorganic carbon acquisition in response to organic C supply, possibly by stimulating respiratory CO 2 production inside cells which can be used for photosynthesis ( Fett & Coleman, 1994 ). However, some species need a light supply to be able to use glucose or to maximize growth benefit of organic C ( Chioccioli, Hankamer & Ross, 2014 ; Curien et al, 2021 ).…”