The genome sequence of Psychrobacter arcticus 273-4, a psychroactive Siberian permafrost bacterium, reveals mechanisms for adaptation to low-temperature growth

Abstract

Psychrobacter arcticus strain 273-4, which grows at temperatures as low as -10 degrees C, is the first cold-adapted bacterium from a terrestrial environment whose genome was sequenced. Analysis of the 2.65-Mb genome suggested that some of the strategies employed by P. arcticus 273-4 for survival under cold and stress conditions are changes in membrane composition, synthesis of cold shock proteins, and the use of acetate as an energy source. Comparative genome analysis indicated that in a significant portion of the P. arcticus proteome there is reduced use of the acidic amino acids and proline and arginine, which is consistent with increased protein flexibility at low temperatures. Differential amino acid usage occurred in all gene categories, but it was more common in gene categories essential for cell growth and reproduction, suggesting that P. arcticus evolved to grow at low temperatures. Amino acid adaptations and the gene content likely evolved in response to the long-term freezing temperatures (-10 degrees C to -12 degrees C) of the Kolyma (Siberia) permafrost soil from which this strain was isolated. Intracellular water likely does not freeze at these in situ temperatures, which allows P. arcticus to live at subzero temperatures.

FIG. 1.

Diagram of the P. arcticus 273-4 genome. The outermost two circles (circles 1 and 2) show the genes in the forward and reverse strands, respectively; different colors indicate different function categories. The next two circles (circles 3 and 4) show the class 1 repeat elements in the forward and reverse strands, respectively. Circles 5 and 6 show transposons and IS elements (green) and prophage (red) in the forward and reverse strands, respectively; circle 7 shows the GC content; and circle 8 shows the GC skew.

FIG. 2.

Cold adaptation. The upper graph shows cold adaptation ratios that were calculated by using all of the genes whose data were statistically significantly different from data in the Swiss-Prot database in favor (cold adapted) or against (hot adapted). A ratio of 1 indicates that the proportions of genes in the two categories are equal. The lower graph shows the total numbers of genes used to generate the ratios.

FIG. 3.

Distribution of cold adaptation qualities across COG categories. The statistical significance of differences between the number of genes with cold qualities and the number of genes with hot qualities in each COG category was determined using the chi-square test. The results were ranked using a scale from 0 to 3, where a P value of <0.001 was 3, a P value of <0.05 was 2, a P value of <0.10 was 1, and a P value of >0.10 was 0. Enrichment of cold-adapted qualities was indicated by a plus sign, and enrichment of hot-adapted qualities was indicated by a minus sign. Rankings were used for cluster analysis of the COG categories.