Mixotrophic growth of the extremophile Galdieria sulphuraria reveals the flexibility of its carbon assimilation metabolism

Abstract

Galdieria sulphuraria is a cosmopolitan microalga found in volcanic hot springs and calderas. It grows at low pH in photoautotrophic (use of light as a source of energy) or heterotrophic (respiration as a source of energy) conditions, using an unusually broad range of organic carbon sources. Previous data suggested that G. sulphuraria cannot grow mixotrophically (simultaneously exploiting light and organic carbon as energy sources), its photosynthetic machinery being repressed by organic carbon.Here, we show that G. sulphuraria SAG21.92 thrives in photoautotrophy, heterotrophy and mixotrophy. By comparing growth, biomass production, photosynthetic and respiratory performances in these three trophic modes, we show that addition of organic carbon to cultures (mixotrophy) relieves inorganic carbon limitation of photosynthesis thanks to increased CO 2 supply through respiration. This synergistic effect is lost when inorganic carbon limitation is artificially overcome by saturating photosynthesis with added external CO 2 .Proteomic and metabolic profiling corroborates this conclusion suggesting that mixotrophy is an opportunistic mechanism to increase intracellular CO 2 concentration under physiological conditions, boosting photosynthesis by enhancing the carboxylation activity of Ribulose-1,5bisphosphate carboxylase-oxygenase (Rubisco) and decreasing photorespiration.We discuss possible implications of these findings for the ecological success of Galdieria in extreme environments and for biotechnological applications.

Growth under Different Trophic Regimes and Synchronization of the Red Microalga Galdieria sulphuraria

“…This confirms the ability of G. sulphuraria to cope with stress caused by high light using metabolic modulation [78]. In the case of mixotrophic growth, it could also be caused by the increase in intracellular CO 2 in Galdieria [79]. Interestingly, the DMs achieved were comparable under both trophic regimes at 40 • C and 750 µmol photons m −2 s −1 (Table 1), suggesting the need for further studies, particularly of photosynthetic performance.…”

“…Evaluation of photosynthetic parameters of G. sulphuraria affected by different trophic regimes and growth conditions, especially in the context of photo-inhibition under high light intensities, would be a relevant future research direction. For example, photosynthesis of mixotrophic G. sulphuraria was boosted by enhancing carboxylation activity of Rubisco and decreasing photorespiration [79]. Similarly, Rubisco was affected by different trophic regimes in G. phlegrea [84].…”

Consequences of Mixotrophy on Cell Energetic Metabolism in Microchloropsis gaditana Revealed by Genetic Engineering and Metabolic Approaches

“…This is, e.g., the case of some Chlorella species (e.g., Chlorella sorokininana ; Cecchin et al, 2018 , see, however, Zhang et al, 2017 for a different conclusion in Chlorella zoofingensis ) and of the diatom Phaeodactylum tricornutum ( Liu et al, 2009 ; Villanova et al, 2017 ). In the green oleaginous alga Ettlia oleoabundans and the red extremophyle alga Galdieria sulphuraria , mixotrophy stimulates both photosynthesis and respiration ( Ferroni et al, 2018 ; Curien et al, 2021 ). Overall, these findings indicate that while respiration is always increased by the addition of organic carbon, the photosynthetic responses change according to the nature of the microalga considered.…”

“…Increasing respiration could be sufficient to fulfill the cell energy requirement for growth, via, e.g., enhanced consumption of cell reserves, under conditions where contribution by photosynthesis is relatively low. Conversely enhanced respiration could boost photosynthesis by providing extra CO 2 for carbon assimilation, provided that the photosynthetic apparatus is not dismantled by the addition of exogenous carbon sources ( Ferroni et al, 2018 ; Curien et al, 2021 ). Finally, respiratory consumption of organic compounds may be incomplete, allowing a (partial) direct utilization of their carbon scaffolds for anabolic processes.…”

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 ).…”