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

Gilles Curien,Claire Remacle,Clément Hallopeau,Andreas P.M Weber,Giovanni Finazzi,Johan Decelle,Marianne Tardif,Myriam Ferro,Denis Falconet,Janina Janetzko,Michele Carone,Benoit Gallet,Erika Guglielmino,Dagmar Lyska,Davide Dal Bo,Phillip Westhoff,Sabine Brugière

doi:10.1111/nph.17359

Abstract

Summary 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 CO2 supply through respiration. This synergistic effect is lost when inorganic carbon limitation is artificially overcome by saturating photosynthesis with added external CO2.Proteomic and metabolic profiling corroborates this conclusion suggesting that mixotrophy is an opportunistic mechanism to increase intracellular CO2 concentration under physiological conditions, boosting photosynthesis by enhancing the carboxylation activity of Ribulose‐1,5‐bisphosphate 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.

Highlights

78 79 The unicellular red alga Galdieria sulphuraria belongs to the Cyanidiophyceae, a class that includes five species often flourishing in different extreme environments (Merola et al, 1981; Gross et al, 1998; Gross & Oesterhelt, 1999; Oesterhelt et al., 2007)
Here, we show instead that photosynthesis and carbon metabolism operate simultaneously in Galdieria sulphuraria SAG21.92 under mixotrophic conditions, provided that the temperature conditions are kept close to the ones experienced by this alga in its natural environment
Biomass 389 production could be increased by increasing the light intensity in both phototrophic cells supplemented with 0.5% CO2 (Fig S8c) or in mixotrophic cells (Fig S8d). These findings are fully consistent with the hypothesis that photosynthesis is CO2 limited in air, and that this limitation can be alleviated by endogenous or exogenous CO2. 395 Metabolic acclimation to mixotrophy in G. sulphuraria

Summary

Introduction

78 79 The unicellular red alga Galdieria sulphuraria belongs to the Cyanidiophyceae, a class that includes five species often flourishing in different extreme environments (Merola et al, 1981; Gross et al, 1998; Gross & Oesterhelt, 1999; Oesterhelt et al., 2007). Genome analysis (Barbier et al, 2005; Schonknecht et al, 2013; Rossoni et al, 2019a) has pinpointed a very high metabolic flexibility of this alga, which is confirmed by its ability to grow in photoautotrophy (exclusive use of light as an energy source) and heterotrophy (organic carbon respiration of more than 50 different substrates, (Gross & Schnarrenberger, 1995)) This capacity, along with the peculiar pH optimum for growth, allow G. sulphuraria to be cultivated in open ponds containing organic matter, overcoming other microorganisms, considered as contaminants in this case. Cells were provided with air or CO2-enriched air by active bubbling (see Methods S1)

Methods

Results

Conclusion