Abstract

Microorganisms inhabiting cold environments have evolved strategies to tolerate and thrive in those extreme conditions, mainly the low temperature that slow down reaction rates. Among described molecular and metabolic adaptations to enable functioning in the cold, there is the synthesis of cold-active proteins/enzymes. In bacterial cold-active proteins, reduced proline content and highly flexible and larger catalytic active sites than mesophylls counterparts have been described. However, beyond the low temperature, microorganisms’ physiological requirements may differ according to their growth velocities, influencing their global protein compositions. This hypothesis was tested in this work using eight cold-adapted yeasts isolated from Antarctica, for which their growth parameters were measured and their draft genomes determined and bioinformatically analyzed. The optimal temperature for yeasts’ growth ranged from 10 to 22°C, and yeasts having similar or same optimal temperature for growth displayed significative different growth rates. The sizes of the draft genomes ranged from 10.7 (Tetracladium sp.) to 30.7 Mb (Leucosporidium creatinivorum), and the GC contents from 37 (Candida sake) to 60% (L. creatinivorum). Putative genes related to various kinds of stress were identified and were especially numerous for oxidative and cold stress responses. The putative proteins were classified according to predicted cellular function and subcellular localization. The amino acid composition was compared among yeasts considering their optimal temperature for growth and growth rates. In several groups of predicted proteins, correlations were observed between their contents of flexible amino acids and both the yeasts’ optimal temperatures for growth and their growth rates. In general, the contents of flexible amino acids were higher in yeasts growing more rapidly as their optimal temperature for growth was lower. The contents of flexible amino acids became lower among yeasts with higher optimal temperatures for growth as their growth rates increased.

Highlights

  • Microorganisms are the primary responsible for nutrient recycling and organic matter mineralization in cold environments, which are predominant on our planet and are defined as having constant temperatures below 5◦C (Gerday et al, 2000; Feller and Gerday, 2003a; Somero, 2004; D’Amico et al, 2006a; Gangwar et al, 2009; Margesin and Feller, 2010; Margesin and Miteva, 2011)

  • The number of predicted coding sequences (CDSs) ranged from 23,034 in W. anomalus to 68,860 in L. creatinivorum, and the percentages of CDSs that were annotated ranged from 10% to 28% in M. gelida and Tetracladium sp., respectively

  • In relation to putative tRNA genes, a higher number was predicted in L. creatinivorum (156 tRNAs, 22 clusters), M. gelida (234 tRNAs, 27 clusters) and C. sake (499 tRNAs, 88 clusters), and a smaller number was predicted in P. glacialis (49 tRNAs, 8 clusters) and Tetracladium sp. (52 tRNAs, 9 clusters)

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Summary

Introduction

Microorganisms are the primary responsible for nutrient recycling and organic matter mineralization in cold environments, which are predominant on our planet and are defined as having constant temperatures below 5◦C (Gerday et al, 2000; Feller and Gerday, 2003a; Somero, 2004; D’Amico et al, 2006a; Gangwar et al, 2009; Margesin and Feller, 2010; Margesin and Miteva, 2011). Mechanisms described to counteract low temperatures and freezing include the synthesis of cryoprotectant molecules, cold-active enzymes, membrane fluidity regulation and, in general, molecular and metabolic adaptations to enable functioning in the cold (Margesin et al, 2007; Buzzini and Margesin, 2013; Alcaíno et al, 2015; Baeza et al, 2017). Bacteria are the most heavily studied cold-adapted microorganisms (Demain and Adrio, 2008; Margesin and Feller, 2010), and in the few sequenced bacterial genomes the genes involved in protein synthesis have attracted attention from researchers. The higher number of genes involved in protein synthesis (such as rRNA and tRNA genes) observed in cold-adapted bacterial genomes than in mesophilic bacterial genomes has been suggested to be an adaptation to compensate for the reduced translation rate under low-temperature conditions (Methé et al, 2005; Médigue et al, 2005; Riley et al, 2008)

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