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.

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

“…This conclusion was based on experiments carried out at 25°C, i.e. a temperature that is far from the physiological optimum of this alga (above 40°C), and therefore decreases photosynthetic performances (Doemel & Brock, 1971;Ford, 1979;Rossoni & Weber, 2019;Rossoni et al, 2019b). Thus, we decided to reinvestigate the possible occurrence of mixotrophy under conditions that resemble natural growth conditions (42°C, pH 2.0) in which G. sulphuraria displays maximum photosynthetic capacity.…”

DNA Methylation in Algae and Its Impact on Abiotic Stress Responses

“…In the thermoacidophile red alga G. sulphuraria , after continuous cold stress (14 °C below its optimal growth temperature) for more than 100 generations, CpG islands located in the intergenic region accumulated a significant number of variants, which is likely a sign of epigenetic remodelling [ 127 ]. Moreover, the cold-adapted samples grew ∼30% faster than the starting population.…”

“…Moreover, the cold-adapted samples grew ∼30% faster than the starting population. The significant growth enhancement of G. sulphuraria grown at low temperatures is driven mainly by mutations in genes involved in the cell cycle, gene regulation and signal transfer, as well as mutations that occurred in the intergenic regions, possibly changing the epigenetic methylation pattern and altering the binding specificity to cis -regulatory elements [ 127 ].…”

Grand Challenges in Microalgae Domestication

“…Eventually, a last challenge concerns random mutagenesis and in vivo directed evolution approaches (Crook et al, 2016 ) as a way to domesticate microalgae (Pourmir and Johannes, 2012 ; Rossoni and Weber, 2019 ). Such strategies require excellent screening methods for selection of improved lines.…”