Living in trinity of extremes: Genomic and proteomic signatures of halophilic, thermophilic, and pH adaptation

Since nucleic acids and proteins of unicellular prokaryotes are directly exposed to extreme environmental conditions, it is possible to explore the genomic-proteomic compositional determinants of molecular mechanisms of adaptation developed by them in response to harsh environmental conditions. Using a wealth of currently available complete genomes/proteomes we were able to explore signatures of adaptation to three environmental factors, pH, salinity, and temperature, observing major trends in compositions of their nucleic acids and proteins. We derived predictors of thermostability, halophilic, and pH adaptations and complemented them by the principal components analysis. We observed a clear difference between thermophilic and salinity/pH adaptations, whereas latter invoke seemingly overlapping mechanisms. The genome-proteome compositional trade-off reveals an intricate balance between the work of base paring and base stacking in stabilization of coding DNA and r/tRNAs, and, at the same time, universal requirements for the stability and foldability of proteins regardless of the nucleotide biases. Nevertheless, we still found hidden fingerprints of ancient evolutionary connections between the nucleotide and amino acid compositions indicating their emergence, mutual evolution, and adjustment. The evolutionary perspective on the adaptation mechanisms is further studied here by means of the comparative analysis of genomic/proteomic traits of archaeal and bacterial species. The overall picture of genomic/proteomic signals of adaptation obtained here provides a foundation for future engineering and design of functional biomolecules resistant to harsh environments.