Tandem Repeats in Bacillus: Unique Features and Taxonomic Distribution

Abstract

Little is known about DNA tandem repeats across prokaryotes. We have recently described an enigmatic group of tandem repeats in bacterial genomes with a constant repeat size but variable sequence. These findings strongly suggest that tandem repeat size in some bacteria is under strong selective constraints. Here, we extend these studies and describe tandem repeats in a large set of Bacillus. Some species have very few repeats, while other species have a large number. Most tandem repeats have repeats with a constant size (either 52 or 20-21 nt), but a variable sequence. We characterize in detail these intriguing tandem repeats. Individual species have several families of tandem repeats with the same repeat length and different sequence. This result is in strong contrast with eukaryotes, where tandem repeats of many sizes are found in any species. We discuss the possibility that they are transcribed as small RNA molecules. They may also be involved in the stabilization of the nucleoid through interaction with proteins. We also show that the distribution of tandem repeats in different species has a taxonomic significance. The data we present for all tandem repeats and their families in these bacterial species will be useful for further genomic studies.

Keywords: Bacillus; Bacillus coagulans; bacteria; bacterial nucleoid; non-coding DNA; satellites; small RNA; tandem repeats.

Figure 1

Number of genomes as a function of the number of tandem repeats in bins of 10 tandem repeats. Genomes with few tandem repeats (0–10) represent 40% of the total genomes analyzed.

Figure 2

The number of tandem repeats with each repeat length is shown. The entirety of all tandem repeats of all Bacillus genomes has been used. The bar at 61 nt includes all lengths over 60 nt. The distribution is clearly non-random, three types of repeat lengths predominate: 20–21, 51–53, and multiples of three nucleotides. A few repeats of size 40–41 nt are also present, which are related to the 20–21 nt tandem repeats.

Figure 3

Alignment of three B. coagulans genomes; NCBI codes: NC_015634.1, NZ_CP026649.1, and NZ_CP025437.1. Tandem repeats are plotted as vertical black lines with a thickness proportional to the tandem repeat length. The whole genomes are presented in the upper frame; there is an extensive overall alignment, but many small gaps are apparent. The lower frame shows a small amplified region (50 Kb). Further examples are given in Figure S2. The correspondence of tandem repeats in different genomes is only approximate.

Figure 4

Models of transcribed RNA tandem repeats: (a) Model of an RNA with nine repeats of 52 nt, prepared with RNA; (b) RNA sponge: Fragment of folded RNA (five repeats) interacting with several proteins; (c) interaction of tandem repeat RNA (black) with messenger RNA (red); (d) interaction of tandem repeat RNA (black) with messenger RNA (red), facilitated by interaction with the Hfq protein hexamer; (e) model of the complex of a partially doubly stranded RNA and the Hfq protein, PDB code 4V2S [29]; (f) direct interaction of an RNA tandem repeat with DNA.