Abstract
Cold environments, such as glaciers and alpine regions, constitute unique habitats for organisms living on Earth. In these harsh ecosystems, snow algae survive, florish, and even become primary producers for microbial communities. How the snow algae maintain physiological activity during violent ambient temperature changes remains unsolved. To explore the cold adaptation mechanisms of the unicellular snow alga Chlamydomonas nivalis, we compared its physiological responses to a model organism from the same genus, Chlamydomonas reinhardtii. When both cell types were exposed to a shift from 22°C to 4°C, C. nivalis exhibited an apparent advantage in cold tolerance over C. reinhardtii, as C. nivalis had both a higher growth rate and photosynthetic efficiency. To determine the cold tolerance mechanisms of C. nivalis, RNA sequencing was used to compare transcriptomes of both species after 1 h of cold treatment, mimicking temperature fluctuations in the polar region. Differential expression analysis showed that C. nivalis had fewer transcriptomic changes and was more stable during rapid temperature decrease relative to C. reinhardtii, especially for the expression of photosynthesis related genes. Additionally, we found that transcription in C. nivalis was precisely regulated by the cold response network, consisting of at least 12 transcription factors and 3 RNA-binding proteins. Moreover, genes participating in nitrogen metabolism, the pentose phosphate pathway, and polysaccharide biosynthesis were upregulated, indicating that increasing resource assimilation and remodeling of metabolisms were critical for cold adaptation in C. nivalis. Furthermore, we identified horizontally transferred genes differentially expressed in C. nivalis, which are critical for cold adaptation in other psychrophiles. Our results reveal that C. nivalis adapts rapid temperature decrease by efficiently regulating transcription of specific genes to optimize resource assimilation and metabolic pathways, providing critical insights into how snow algae survive and propagate in cold environments.
Highlights
Cold environments, where the temperature remains persistently below or close to the freezing point of 0◦C, occupy more than 80% of the biosphere on Earth, comprising both terrestrial ecosystems and aquatic regions, such as deep oceans and subglacial lakes (Feller and Gerday, 2003; Morgan-Kiss et al, 2006)
Chlamydomonas nivalis UTEX 2824 was obtained from the Culture Collection of Algae at the University of Texas at Austin, and grown in liquid or solid (1.5% agar) Bold 1NV (B1NV) medium
To compare the cold tolerance of C. nivalis UTEX 2824 with the mesophilic species C. reinhardtii CC-124, both algal cells were first grown at 22◦C with an initial concentration of 104 cells mL−1
Summary
Cold environments, where the temperature remains persistently below or close to the freezing point of 0◦C, occupy more than 80% of the biosphere on Earth, comprising both terrestrial ecosystems and aquatic regions, such as deep oceans and subglacial lakes (Feller and Gerday, 2003; Morgan-Kiss et al, 2006). Psychrophiles can include bacteria, algae, fungi, and protozoa, Snow algae, organisms known for producing colorful patches on snowfields, act as the primary producer by providing energy and nutrients for whole psychrophilic biomes These photoautotrophic species can decrease the albedo of the snow in alpine, Antarctic, and Arctic areas, leading to an increase in the melting rate of snow and ice, and accelerating the retreat of glaciers (Lutz et al, 2016; Davey et al, 2019). To survive at low temperatures, C. nivalis may possess unique cold adaptation mechanisms, as reflected in different transcriptional changes of regulatory and functional genes during cold exposure compared with C. reinhardtii. Our study reveals that C. nivalis adjusts to temperature fluctuations through specific transcription factors and RNA-binding proteins that optimizes resource assimilation and metabolic pathways
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