Coevolution of DNA-Interacting Proteins and Genome “Dialect”

Abstract

Several species-specific characteristics of genome organization that are superimposed on its coding aspects were proposed earlier, including genome signature (GS), genome accent, and compositional spectrum (CS). These notions could be considered as representatives of genome dialect (GD). We measured within the Proteobacteria some GD representatives, the relative abundance of dinucleotides or GS, the profiles of occurrence of 10 nucleotide words (CS), and the profiles of occurrence of 20 nucleotide words, using a degenerate two-letter alphabet (purine-pyrimidine compositional spectra [PPCS]). Here, we show that the evolutionary distances between DNA repair and recombination orthologous enzymes (especially those of the nucleotide excision repair system) are highly correlated with PPCS and GS distances. Orthologous proteins involved in structural or metabolic processes (control group) have significantly lower correlations of their evolutionary distances with the PPCS and GS distances. We hypothesize that the high correlation of the evolutionary distances of the DNA repair orthologous enzymes with their GD is a result of the coevolution of the DNA repair enzymes' structures and GDs. Species GDs could be substantially influenced by the function of DNA polymerase I (the bacterial major DNA repair polymerase). This might cause the correlation of species GDs differentiation with evolutionary changes of species DNA polymerase I. Simultaneously, the structures of DNA repair-recombination enzymes might be evolutionarily sensitive and responsive to changes in the structure of their substrate-the DNA (including those that are represented by GD differentiation). We further discuss the rationale and mechanisms of the hypothesized coevolution. We suggest that stress might be an important cause of changes in the repair-recombination genes and the GD and the trigger of the aforementioned coevolution process. Other triggers might be massive horizontal gene transfer and ecological selection.