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Cold temperatures, low water activity, and low nutrient availability are biological stressors for microbes residing in permafrosts. Psychrobacter arcticus 273-4 was isolated after inhabiting Kolyma permafrosts for 10,000-40,000 yr. Using an oligonucleotide microarray with probes for 95% of the P. arcticus genes, we compared its gene expression profiles during exponential growth at 22°C, 17°C, 0°C, and -6°C in defined medium. Thirteen of the 42 transcription factors present in the genome were upregulated in the cold. Previously described cold responsive genes for maintenance of membrane fluidity, translation and transcription were upregulated at low temperature, but those involved with carbon metabolism and DNA binding increased in expression with increasing temperature. Genes of unknown function accounted for 32% of differentially expressed genes, suggesting their potential role in cold acclimation. Several pairs of duplicate genes with homologous functions had inverse expression patterns over temperature. Genetic and bioinformatic studies will determine if this exchange of expression of warm-adapted for cold-adapted alleles is adaptive for cold growth. Genes for oxidative damage repair were strongly upregulated during growth in the cold, a result consistent with increased dissolved oxygen in cold growth medium. The stringent response, a growth-slowing response to carbon starvation, was strongly activated in the cold and, as a result, energy and carbon metabolism genes were downregulated. However, expression of several genes for the biosynthesis of proline, cystine, histidine and tryptophan increased at cold temperatures. Indeed, supplementation of growth medium with those amino acids increased the growth rates of P. arcticus at 0°C while not increasing growth rates at 17°C or 22°C. These results suggest that most of the genes of P. arcticus are evolutionarily adapted to function in a wide range of temperatures, but P. arcticus must still compensate for slow rates at key points in its metabolism by slowing its growth rate, and its consumption of resources.

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