Protein and DNA Sequence Determinants of Thermophilic Adaptation

Abstract

There have been considerable attempts in the past to relate phenotypic trait—habitat temperature of organisms—to their genotypes, most importantly compositions of their genomes and proteomes. However, despite accumulation of anecdotal evidence, an exact and conclusive relationship between the former and the latter has been elusive. We present an exhaustive study of the relationship between amino acid composition of proteomes, nucleotide composition of DNA, and optimal growth temperature (OGT) of prokaryotes. Based on 204 complete proteomes of archaea and bacteria spanning the temperature range from −10 °C to 110 °C, we performed an exhaustive enumeration of all possible sets of amino acids and found a set of amino acids whose total fraction in a proteome is correlated, to a remarkable extent, with the OGT. The universal set is Ile, Val, Tyr, Trp, Arg, Glu, Leu (IVYWREL), and the correlation coefficient is as high as 0.93. We also found that the G + C content in 204 complete genomes does not exhibit a significant correlation with OGT (R = −0.10). On the other hand, the fraction of A + G in coding DNA is correlated with temperature, to a considerable extent, due to codon patterns of IVYWREL amino acids. Further, we found strong and independent correlation between OGT and the frequency with which pairs of A and G nucleotides appear as nearest neighbors in genome sequences. This adaptation is achieved via codon bias. These findings present a direct link between principles of proteins structure and stability and evolutionary mechanisms of thermophylic adaptation. On the nucleotide level, the analysis provides an example of how nature utilizes codon bias for evolutionary adaptation to extreme conditions. Together these results provide a complete picture of how compositions of proteomes and genomes in prokaryotes adjust to the extreme conditions of the environment.

Evolutionary Dynamics of the Prokaryotic Adaptive Immunity System CRISPR-Cas in an Explicit Ecological Context

“…This observation links the present results to those of our earlier modeling study of CRISPRCas in which we have shown that the immunological memory provided by CRISPR-Cas can be effective only at moderate virus diversities (40). This result has been suggested to explain the ubiquity of CRISPR-Cas in hyperthermophiles as opposed to the substantially lower prevalence in mesophiles given that the rates of mutation fixation are much lower in hyperthermophiles (both hosts and viruses) than in mesophiles (69,70). The present findings offer a complementary and simpler perspective on the difference in the prevalence of CRISPR-Cas between hyperthermophiles and mesophiles: extremely large populations in which CRISPR-Cas becomes useless according to the model results are known only for mesophiles, whereas hyperthermophiles typically exist as smaller populations (71)(72)(73)(74) in which CRISPR-Cas immunity is predicted to be efficient.…”

Sequences downstream of the start codon and their relations to G + C content and optimal growth temperature in prokaryotic genomes

“…The relation of optimal growth temperature, amino acid composition and nucleotide composition has been systematically analyzed by Zeldovich et al (2007). Here optimal growth temperature is another factor found to influence the patterns of ORF 5 0 terminal regions.…”

Helix‐coil energetics for helix formers and breakers reflect context and temperature: Mutants of helically robust, guest‐sensitive homopeptide hosts

“…First, our recent observations suggest that low-temperature melting features of mutants derived from alanine-rich peptides lack generality and may provide poor models for helix-coil equilibria that are studied at physiologically relevant temperatures. Second, recent sequence analyses of genomes from thermophilic organisms show that seven amino acid residues have unusually high frequencies of occurrence in thermophilic proteins, 4,5 but alanine, an exceptionally strong helix former at low temperatures, is not among them. All but two of these residues are helix breakers near 08C.…”