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Exploring the evolution of the Bacillus cereus group repeat element bcr1 by comparative genome analysis of closely related strains

Department of Pharmaceutical Biosciences (Microbiology), University of Oslo, PO Box 1068 Blindern, 0316 Oslo, Norway

Correspondence
Ole Andreas Økstad
o.a.l.okstad{at}biotek.uio.no

bcr1 is a chromosomal 155 bp repeated element found uniquely and ubiquitously in the Bacillus cereus group of Gram-positive bacteria; it exhibits several features characteristic of mobile elements, including a variable distribution pattern between strains. Here, highly similar bcr1 elements in non-conserved genomic loci are identified in a set of closely related B. cereus and Bacillus thuringiensis strains near the Bacillus anthracis phylogenetic cluster. It is also shown that bcr1 may be present on small RNA transcripts in the 100–400 bp size range. In silico folding of bcr1 at the RNA level indicated that transcripts may form a double-hairpin-like structure predicted to have high structural stability. A functional role of bcr1 at the RNA level is supported by multiple cases of G–U base-pairing, and compensatory mutations maintaining structural stability of the RNA fold. In silico folding at the DNA level produced similar predicted structures, with the potential to form a cruciform structure at open DNA complexes. The predicted structural stability was greater for bcr1 elements showing high sequence identities to bcr1 elements in non-conserved chromosomal loci in other strains, relative to other bcr1 copies. bcr1 mobility could thus be dependent on the formation of a stable DNA or RNA intermediate. Furthermore, bcr1 elements potentially encoding structurally stable and less stable transcripts were phylogenetically intermixed, indicating that loss of bcr1 mobility may have occurred multiple times during evolution. Repeated elements with similar features in other bacteria have been shown to provide functions such as mRNA stabilization, transcription termination and/or promoter function. Similarly, bcr1 may constitute a mobile element which occasionally gains a function when it enters an appropriate chromosomal locus.

The multiple-sequence alignment results for the full-length repeats examined in this study have been deposited into the EMBL-ALIGN database with the accession number ALIGN_001090.

Two supplementary figures showing the multiple sequence alignment and the predicted RNA folding of the full-length bcr1 repeats and two supplementary tables listing the chromosomal coordinates of full-length and partial bcr1 sequences in the strains studied are available with the online version of this paper.