Abstract
Microorganisms have evolved to colonize all biospheres, including extremely cold environments, facing several stressor conditions, mainly low/freezing temperatures. In general, terms, the strategies developed by cold-adapted microorganisms include the synthesis of cryoprotectant and stress-protectant molecules, cold-active proteins, especially enzymes, and membrane fluidity regulation. The strategy could differ among microorganisms and concerns the characteristics of the cold environment of the microorganism, such as seasonal temperature changes. Microorganisms can develop strategies to grow efficiently at low temperatures or tolerate them and grow under favorable conditions. These differences can be found among the same kind of microorganisms and from the same cold habitat. In this work, eight cold-adapted yeasts isolated from King George Island, subAntarctic region, which differ in their growth properties, were studied about their response to low temperatures at the transcriptomic level. Sixteen ORFeomes were assembled and used for gene prediction and functional annotation, determination of gene expression changes, protein flexibilities of translated genes, and codon usage bias. Putative genes related to the response to all main kinds of stress were found. The total number of differentially expressed genes was related to the temperature variation that each yeast faced. The findings from multiple comparative analyses among yeasts based on gene expression changes and protein flexibility by cellular functions and codon usage bias raise significant differences in response to cold among the studied Antarctic yeasts. The way a yeast responds to temperature change appears to be more related to its optimal temperature for growth (OTG) than growth velocity. Yeasts with higher OTG prepare to downregulate their metabolism to enter the dormancy stage. In comparison, yeasts with lower OTG perform minor adjustments to make their metabolism adequate and maintain their growth at lower temperatures.
Highlights
Microorganisms inhabiting cold environments, which are predominant on our planet and are defined as having constant temperatures below 5◦C (Siddiqui et al, 2013; Buzzini and Margesin, 2014; Margesin, 2017), must face several stressor conditions, related mainly to low/freezing temperatures
The differential gene expression was determined for putative genes for each yeast when cultivated at high temperature vs. 4◦C and expressed as log2-fold change, the results shown in Figure 1 (p ≤ 0.05)
In the case of differentially expressed genes (DEGs) identified as ribosomal subunits, higher numbers were found in C. sake, Tetracladium sp., and W. anomalus, only 3 in Cryptococcus sp., and none in V. victoriae and M. gelida (Figure 3B)
Summary
Microorganisms inhabiting cold environments, which are predominant on our planet and are defined as having constant temperatures below 5◦C (Siddiqui et al, 2013; Buzzini and Margesin, 2014; Margesin, 2017), must face several stressor conditions, related mainly to low/freezing temperatures. The higher number of rRNA and tRNA genes observed in cold-adapted than mesophilic bacterial genomes was suggested as a compensation for the reduced translation rate at low temperature (Methé et al, 2005; Médigue et al, 2005; Riley et al, 2008), a process crucial for rapid metabolism and response to environmental changes. Putative genes were predicted from their ORFeomes and functionally classified; their expression level and codon usage bias were determined and characterized according to the estimated flexibility of encoding proteins. Both up- and downregulated genes were found, including those canonically associated with the response to all main kinds of stress, whose number was directly related to the temperature variation that each yeast faced. Yeasts isolated from the same Antarctic region could be stated to have developed different strategies to respond to cold
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