Adaptation to Aquatic and Terrestrial Environments in Chlorella vulgaris (Chlorophyta)

The globally distributed green microalga Chlorella vulgaris (Chlorophyta) colonizes aquatic and terrestrial habitats, but the molecular mechanisms underpinning survival in these two contrasting environments are far from understood. Here, we compared the authentic strain of C. vulgaris from an aquatic habitat with a strain from a terrestrial high alpine habitat previously determined as Chlorella mirabilis. Molecular phylogeny of SSU rDNA (823 bp) showed that the two strains differed by one nucleotide only. Sequencing of the ITS2 region confirmed that both strains belong to the same species, but to distinct ribotypes. Therefore, the terrestrial strain was re-assessed as C. vulgaris. To study the response to environmental conditions experienced on land, we assessed the effects of irradiance and temperature on growth, of temperature on photosynthesis and respiration, and of desiccation and rehydration on photosynthetic performance. In contrast to the aquatic strain, the terrestrial strain tolerated higher temperatures and light conditions, had a higher photosynthesis-to-respiration ratio at 25°C, still grew at 30°C and was able to fully recover photosynthetic performance after desiccation at 84% relative humidity. The two strains differed most in their response to the dehydration/rehydration treatment, which was further investigated by untargeted GC-MS-based metabolite profiling to gain insights into metabolic traits differentiating the two strains. The two strains differed in their allocation of carbon and nitrogen into their primary metabolites. Overall, the terrestrial strain had higher contents of readily available nitrogen-based metabolites, especially amino acids and the polyamine putrescine. Dehydration and rehydration led to differential regulation of the amino acid metabolism, the tricarboxylic acid cycle and sucrose metabolism. The data are discussed with a view to differences in phenotypic plasticity of the two strains, and we suggest that the two genetically almost identical C. vulgaris strains are attractive models to study mechanisms that protect from abiotic stress factors, which are more frequent in terrestrial than aquatic habitats, such as desiccation and irradiation.