Abstract
A ~10–11 bp periodicity in dinucleotides imparting DNA bending, with shorter periods found in organisms with positively-supercoiled DNA and longer periods found in organisms with negatively-supercoiled DNA, was previously suggested to assist in DNA compaction. However, when measured with more robust methods, variation in the observed periods between organisms with different growth temperatures is not consistent with that hypothesis. We demonstrate that dinucleotide periodicity does not arise solely by mutational biases but is under selection. We found variation between genomes in both the period and the suite of dinucleotides that are periodic. Whereas organisms with similar growth temperatures have highly variable periods, differences in periods increase with phylogenetic distance between organisms. In addition, while the suites of dinucleotides under selection for periodicity become more dissimilar among more distantly-related organisms, there is a core set of dinucleotides that are strongly periodic among genomes in all domains of life. Notably, this core set of periodic motifs are not involved in DNA bending. These data indicate that dinucleotide periodicity is an ancient genomic architecture which may play a role in shaping the evolution of genes and genomes.
Highlights
A dominant mode of bacterial genome evolution is the acquisition of foreign DNA via lateral gene transfer, or LGT [1, 2]
We examined the spacings between all possible pairs of nucleotides and found that different dinucleotides were strongly periodic in different organisms
The period varied among organisms between 9.7 and 11.8 nucleotides; contrary to long-held assumptions, the period was not related to organismal growth temperature
Summary
A dominant mode of bacterial genome evolution is the acquisition of foreign DNA via lateral gene transfer, or LGT [1, 2]. As foreign DNA may incur a detriment upon insertion into a new recipient genome, the acquisition must have a net positive impact on fitness to be successful [6,7,8,9]. In addition to being a repository of information, a chromosome is a large polymer that must be maneuvered in various ways, such as compaction [10], segregation during cell division [11], or accessibility of genes during transcription [12]. These processes would be facilitated by information embedded within and between genes, termed genomic architecture. An acquisition will be retained only if the benefits outweigh these detriments [6,7,8,9]
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