Systems biology of cold adaptation in the polyextremophilic red algaGaldieria sulphuraria

Abstract

12Rapid fluctuation of environmental conditions can impose severe stress upon living organisms. 13 Surviving such episodes of stress requires a rapid acclimation response, e.g., by transcriptional 14 and post-transcriptional mechanisms. Persistent change of the environmental context, however, 15 requires longer-term adaptation at the genetic level. Fast-growing unicellular aquatic 16 eukaryotes enable analysis of adaptive responses at the genetic level in a laboratory setting. In 17 this study, we applied continuous cold stress (28°C) to the thermoacidophile red alga G. 18 sulphuraria, which is 14°C below its optimal growth temperature of 42°C. Cold stress was 19 applied for more than 100 generations to identify components that are critical for conferring 20 thermal adaptation. After cold exposure for more than 100 generations, the cold-adapted 21 samples grew ~30% faster than the starting population. Whole-genome sequencing revealed 22 757 variants located on 429 genes (6.1% of the transcriptome) encoding molecular functions 23 involved in cell cycle regulation, gene regulation, signaling, morphogenesis, microtubule 24 nucleation, and transmembrane transport. CpG islands located in the intergenic region 25 accumulated a significant number of variants, which is likely a sign of epigenetic remodeling. 26We present 20 candidate genes and three putative cis-regulatory elements with various 27 functions most affected by temperature. Our work shows that natural selection towards 28 temperature tolerance is a complex systems biology problem that involves gradual 29 reprogramming of an intricate gene network and deeply nested regulators. 30 31 32