Dataset Information

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 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.

SUBMITTER: Curien G

PROVIDER: S-EPMC8252106 | biostudies-literature | 2021 Jul

REPOSITORIES: biostudies-literature

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

Curien Gilles G Lyska Dagmar D Guglielmino Erika E Westhoff Phillip P Janetzko Janina J Tardif Marianne M Hallopeau Clément C Brugière Sabine S Dal Bo Davide D Decelle Johan J Gallet Benoit B Falconet Denis D Carone Michele M Remacle Claire C Ferro Myriam M Weber Andreas P M APM Finazzi Giovanni G

The New phytologist 20210501 1

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. ...[more]

PMID: 33764540

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Project description:Purpose: Red algae show two putative phases of massive genome reduction. RNA-splicing represents an important form of post-transcriptional regulation in eukaryotes. This process generates increased transcriptome and proteome diversity via alternative splicing that can maximize the DNA-encoded genetic diversity embedded within genomes. Why would Spliceosomal Machinery genes and a relatively more complex intron-exon structure be preserved in the compact Galdieria genome? The answer may lie in the fact that RNA-splicing represents an important form of post-transcriptional regulation in eukaryotes. It is hypothesized that his process generates increased transcriptome and proteome diversity via alternative splicing that can maximize the DNA-encoded genetic diversity embedded within genomes. Methods: The experimental design followed a temperature shift timeline: after two weeks of cultivation at 42°C, constant illumination (90 μE) and constant shaking (160 rpm) in photoautotrophic conditions the first sampling took place (H-42) and the cultures of G.sulphuraria were swiftly moved to 28°C. After cold treatment at 28°C for 48 hours, a second sampling was performed (C-28.1). The G. sulphuraria was then switched to 46°C for 48 hours, at end of which a third sampling was retrieved (H-46). It again was followed by a cold treatment at 28°C for 48 hours when a fourth sampling was retrieved (C-28.2). Altogether, two 48h timepoints from high temperatures (42°C and 46oC) and two 48h timepoints from cold temperature (28°C) were targeted for sampling. Results: We show that RNA-splicing provides an avenue for generating transcriptome diversity under strong constraints on genome size and gene number. Conclusions: We report the relatively high retention of Spliceosomal Machinery genes and the enrichment of intron-exon structures in G. sulphuraria that might be associated with the exceptional transcriptome and proteome diversity of this species. These results suggest that the losses of genes and functions caused by genome reduction might be mitigated by sequence diversity generated by a robust RNA-splicing system. More generally, the strong constraints imposed by genome reduction appear to be ameliorated by processes that operate on the transcriptomic and proteomic levels.

Dataset Information

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

Publications

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

Similar Datasets

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