Molecular mechanisms of adaptation emerging from the physics and evolution of nucleic acids and proteins

Abstract

DNA, RNA and proteins are major biological macromolecules that coevolve and adapt to environments as components of one highly interconnected system. We explore here sequence/structure determinants of mechanisms of adaptation of these molecules, links between them, and results of their mutual evolution. We complemented statistical analysis of genomic and proteomic sequences with folding simulations of RNA molecules, unraveling causal relations between compositional and sequence biases reflecting molecular adaptation on DNA, RNA and protein levels. We found many compositional peculiarities related to environmental adaptation and the life style. Specifically, thermal adaptation of protein-coding sequences in Archaea is characterized by a stronger codon bias than in Bacteria. Guanine and cytosine load in the third codon position is important for supporting the aerobic life style, and it is highly pronounced in Bacteria. The third codon position also provides a tradeoff between arginine and lysine, which are favorable for thermal adaptation and aerobicity, respectively. Dinucleotide composition provides stability of nucleic acids via strong base-stacking in ApG dinucleotides. In relation to coevolution of nucleic acids and proteins, thermostability-related demands on the amino acid composition affect the nucleotide content in the second codon position in Archaea.

Phenotypic divergence of thermotolerance: Molecular basis and cold adaptive evolution related to intrinsic DNA flexibility of glacier‐inhabitingCryobacteriumstrains

“…The debate of the nature of the relationship between growth temperature and GC content, especially GC3, has gone on for more than 40 years. Most data and analyses in prokaryotes failed to show a positive correlation between genomic GC content, especially GC3 and T OPT (Galtier and Lobry, ; Hurst and Merchant, ; Basak and Ghosh, ; Goncearenco et al ., ), although the result of Musto et al . () did support this.…”

“…() did support this. This may be explained by the fact that most of these studies examined very distant phylogenetic groups that included eubacteria and archaea (Galtier and Lobry, ; Hurst and Merchant, ; Basak and Ghosh, ; Goncearenco et al ., ), but the work of Musto et al . () examined more phylogenetically closer groups.…”

“…Goncearenco et al . () concluded that increased GC3 content was not a result of thermal adaptation but instead related to an aerobic life style.…”

Massively parallel sampling of lattice proteins reveals foundations of thermal adaptation

“…The noticeable split of the predictions into a hydrophobic and charged arms is reminiscent of the positive and negative design hypotheses, 18 and may be also due to the specific structure of the Miyazawa-Jernigan amino acid interaction matrix, with only two major eigenvalues. 45 To compare the prediction of our theory with biological data, we used a dataset of 191 bacteria and archaea with completely sequenced genomes and known optimum growth temperatures 46 in the range between 7 and 103 • C. We have then performed the linear regression between the frequencies of each of the 20 amino acid types and optimum growth temperature, and plotted the slopes of that regression against the theoretical predictions from Eq. (15).…”

Structural Perspectives on the Evolutionary Expansion of Unique Protein-Protein Binding Sites

“…It is well known that archaeal and bacterial genomes and proteomes differ in their nucleotide and amino acid compositions (54), and that the composition of protein-protein binding sites may also differ among species (55). However, the evolutionary trends in the composition and physicochemical properties of unique protein-binding sites have not been analyzed in detail previously.…”