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Acclimation of photosynthetic apparatus in the mesophilic red alga Dixoniella giordanoi.

ABSTRACT: Eukaryotic algae are photosynthetic organisms capable of exploiting sunlight to fix carbon dioxide into biomass with highly variable genetic and metabolic features. Information on algae metabolism from different species is inhomogeneous and, while green algae are, in general, more characterized, information on red algae is relatively scarce despite their relevant position in eukaryotic algae diversity. Within red algae, the best-known species are extremophiles or multicellular, while information on mesophilic unicellular organisms is still lacunose. Here, we investigate the photosynthetic properties of a recently isolated seawater unicellular mesophilic red alga, Dixoniella giordanoi. Upon exposure to different illuminations, D. giordanoi shows the ability to acclimate, modulate chlorophyll content, and re-organize thylakoid membranes. Phycobilisome content is also largely regulated, leading to almost complete disassembly of this antenna system in cells grown under intense illumination. Despite the absence of a light-induced xanthophyll cycle, cells accumulate zeaxanthin upon prolonged exposure to strong light, likely contributing to photoprotection. D. giordanoi cells show the ability to perform cyclic electron transport that is enhanced under strong illumination, likely contributing to the protection of Photosystem I from over-reduction and enabling cells to survive PSII photoinhibition without negative impact on growth.

SUBMITTER: Fattore N

PROVIDER: S-EPMC8596783 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Purpose: We aimed at i) obtaining insight into how a thermophile organism reacts to cold stress, and ii) evaluating the impact of HGT candidates on the acclimation process to temperature decrease. 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 (Hot_T48_1) and the cultures of G.sulphuraria were swiftly moved to 28°C ( = cold temperature). "Cold" samples were taken after 3h (Cold_T3_2), 12h (Cold_T12_3) and 48h (Cold_T48_4). After cold treatment at 28°C for 48 hours, the G. sulphuraria was then switched to 46°C for 48 hours (="Hot"). Again, samples were taken after 3h (Hot_T3_5), 12h (Hot_T12_6) and 48h (Hot_T48_7). Altogether, a 48h temperature timeshift at 28°C and successive recovery at 46°C were targeted for sampling. Results: Galdieria sulphuraria is a unicellular red alga that lives in hot, acidic, toxic metal-rich, volcanic environments, where few other organisms survive. Its genome harbours up to 5% of genes most likely acquired through horizontal gene transfer. These genes probably contributed to G. sulphuraria’s adaptation to its extreme habitats, resulting in today’s polyextremophilic traits. Here, we applied RNA-sequencing to obtain insights into the acclimation of a thermophilic organism towards temperatures below its growth optimum and to study how horizontally acquired genes contribute to cold acclimation. A decrease in growth temperature from 42 °C/46 °C to 28 °C resulted in an upregulation of ribosome biosynthesis, while excreted proteins, probably components of the cell wall, were downregulated. Photosynthesis was suppressed at cold temperatures, and transcript abundances indicated that C-metabolism switched from gluconeogenesis to glycogen degradation. Folate cycle and S-adenosylmethionine cycle (one-carbon metabolism) were transcriptionally upregulated, probably to drive the biosynthesis of betaine. All these cold-induced changes in gene expression were reversible upon temperature increase. Numerous genes acquired by horizontal gene transfer displayed pronounced temperature-dependent expression changes, corroborating the view that these genes contributed to adaptive evolution in G. sulphuraria.

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Acclimation of photosynthetic apparatus in the mesophilic red alga Dixoniella giordanoi.

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