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Systems Biology of Cold Adaptation in the Polyextremophilic Red Alga Galdieria sulphuraria.

ABSTRACT: Rapid fluctuation of environmental conditions can impose severe stress upon living organisms. Surviving such episodes of stress requires a rapid acclimation response, e.g., by transcriptional and post-transcriptional mechanisms. Persistent change of the environmental context, however, requires longer-term adaptation at the genetic level. Fast-growing unicellular aquatic eukaryotes enable analysis of adaptive responses at the genetic level in a laboratory setting. In this study, we applied continuous cold stress (28°C) to the thermoacidophile red alga G. sulphuraria, which is 14°C below its optimal growth temperature of 42°C. Cold stress was applied for more than 100 generations to identify components that are critical for conferring thermal adaptation. After cold exposure for more than 100 generations, the cold-adapted samples grew ?30% faster than the starting population. Whole-genome sequencing revealed 757 variants located on 429 genes (6.1% of the transcriptome) encoding molecular functions involved in cell cycle regulation, gene regulation, signaling, morphogenesis, microtubule nucleation, and transmembrane transport. CpG islands located in the intergenic region accumulated a significant number of variants, which is likely a sign of epigenetic remodeling. We present 20 candidate genes and three putative cis-regulatory elements with various functions most affected by temperature. Our work shows that natural selection toward temperature tolerance is a complex systems biology problem that involves gradual reprogramming of an intricate gene network and deeply nested regulators.

SUBMITTER: Rossoni AW

PROVIDER: S-EPMC6504705 | 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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Systems Biology of Cold Adaptation in the Polyextremophilic Red Alga Galdieria sulphuraria.

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