Origin and fate of repeats in bacteria

Abstract

We investigated 53 complete bacterial chromosomes for intrachromosomal repeats. In previous studies on eukaryote chromosomes, we proposed a model for the dynamics of repeats based on the continuous genesis of tandem repeats, followed by an active process of high deletion rate, counteracted by rearrangement events that may prevent the repeats from being deleted. The present study of long repeats in the genomes of Bacteria and Archaea suggests that our model of interspersed repeats dynamics may apply to them. Thus the duplication process might be a consequence of very ancient mechanisms shared by all three domains. Moreover, we show that there is a strong negative correlation between nucleotide composition bias and the repeat density of genomes. We hypothesise that in highly biased genomes, non-duplicated small repeats arise more frequently by random effects and are used as primers for duplication mechanisms, leading to a higher density of large repeats.

Figure 1

A model of interspersed repeats dynamics. In this model, interspersed repeats originate mainly from tandem repeats, which can be separated by further chromosomal rearrangements. In newly created repeats with a small spacer (i) the conversion rate is high, keeping the two copies identical and (ii) the deletion rate is also high, so that over a longer time scale only small repeats are retained. However, if one or more rearrangements (e.g. insertion, translocation and/or inversion) occur separating the two copies, both deletion and conversion rates decrease markedly. Both copies are then free to evolve.

Figure 2

Repeat density as a function of chromosome size. Plot of D_N as a function of chromosome size. This figure illustrates the positive correlation between D_N and chromosome size.

Figure 3

Densities of inverted repeats versus direct repeats. For each of the 53 chromosomes, we plotted the densities in number (D_N2 = two-copy number/size in Mb) of inverted repeats as a function of D_N2 of direct repeats. Because of the large difference in densities between genomes, two scales have been used. Abbreviations of species used in this figure correspond to those described in Table 1. The density of direct repeats is generally greater than the density of inverted repeats, but both are of the same order of magnitude.

Figure 4

Complexity of chromosomes as a function of repeat density. Entropy (a measure of nucleotide complexity) of each of the 53 chromosomes as a function of their global repeat density. Entropy measures the nucleotide complexity of a sequence: if each nucleotide frequency is 0.25, then entropy is maximum (1), else it is lower. This figure illustrates that entropy is negatively correlated with repeat density.