Novel bacteriophages containing a genome of another bacteriophage within their genomes - PubMed (original) (raw)

Novel bacteriophages containing a genome of another bacteriophage within their genomes

Maud M Swanson et al. PLoS One. 2012.

Abstract

A novel bacteriophage infecting Staphylococus pasteuri was isolated during a screen for phages in Antarctic soils. The phage named SpaA1 is morphologically similar to phages of the family Siphoviridae. The 42,784 bp genome of SpaA1 is a linear, double-stranded DNA molecule with 3' protruding cohesive ends. The SpaA1 genome encompasses 63 predicted protein-coding genes which cluster within three regions of the genome, each of apparently different origin, in a mosaic pattern. In two of these regions, the gene sets resemble those in prophages of Bacillus thuringiensis kurstaki str. T03a001 (genes involved in DNA replication/transcription, cell entry and exit) and B. cereus AH676 (additional regulatory and recombination genes), respectively. The third region represents an almost complete genome (except for the short terminal segments) of a distinct bacteriophage, MZTP02. Nearly the same gene module was identified in prophages of B. thuringiensis serovar monterrey BGSC 4AJ1 and B. cereus Rock4-2. These findings suggest that MZTP02 can be shuttled between genomes of other bacteriophages and prophages, leading to the formation of chimeric genomes. The presence of a complete phage genome in the genome of other phages apparently has not been described previously and might represent a 'fast track' route of virus evolution and horizontal gene transfer. Another phage (BceA1) nearly identical in sequence to SpaA1, and also including the almost complete MZTP02 genome within its own genome, was isolated from a bacterium of the B. cereus/B. thuringiensis group. Remarkably, both SpaA1 and BceA1 phages can infect B. cereus and B. thuringiensis, but only one of them, SpaA1, can infect S. pasteuri. This finding is best compatible with a scenario in which MZTP02 was originally contained in BceA1 infecting Bacillus spp, the common hosts for these two phages, followed by emergence of SpaA1 infecting S. pasteuri.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. Transmission electron micrographs of phage virions showing their isometric heads and long non-contractile tails.

Panel A shows multiple SpaA1 virions and panel B shows a single Bce A1 (B) virions. All scale bars represent 100 nm.

Figure 2. Architectures of SpaA1, BceA1 and MZTP02 genomes: comparison with BLAST protein matches to phage proteins in four Bacillus genomes.

The horizontal bars represent DNA sequences (all to scale) with annotated CDS on the forward (upper) or reverse (lower) strand shown as pointed boxes, generally in alternating blue and purple. The red, green and yellow shading indicates the three functional modules of phages SpaA1 and BceA1 (center) which are 100% identical except for the area around ORF47 (bright red), and the 99% nucleotide identical matching region in module I with phage MZTP02 (second row from top). Rather than the original annotation for MZTP02, annotation based on SpaA1/BceA1 genome analysis (Table 1) is shown, with grey colouring for partial sequences (1 and 19), and genes with frame shifts (12, 13, 17, 18). The bottom three bars represent complete contigs from three separate Bacillus genomes, with red/yellow highlighting top BLAST matches from SpaA1/BceA1 module I and III proteins, showing synteny visually. The top row of bars represents seven contigs from another Bacillus draft genome with green highlighting for BLAST protein matches from SpaA1/BceA1 module II proteins. Three of these contigs have been truncated for display. For clarity, additional BLAST matches to other contigs from these bacterial genomes are not shown (e.g. SpaA1/BceA1 ORF37 matches another contig in B. thuringiensis var. monterrey BGSC A4J1). This figure was drawn using GenomeDiagram and Biopython .

Figure 3. Phylogenetic analysis of selected SpaA1 genes.

A. Bacterial and phage genomes sorted by the number of ORFs matching the SpaA1/MZTP02 region (based on the up to 200 best hits in NR database). On the left, the actual number of hits is indicated. Color code: three bacterial genomes with the 17-15 ORFs matching the SpaA1/MZTP02 region:purple; three bacterial genomes with the 13-12 matching ORFs: light blue; the phage with the largest number of hits matching the SpaA1/MZTP02 region:orange. B, C, D. Unrooted maximum likelihood trees for three ORFs the SpaA1/MZTP02 region. Each terminal tree node is labelled with GenBank Identifier (GI) number and full systematic name of an organism. Color code is the same as in the Figure 3A. The SpaA1 phage sequences are shown in red. Bootstrap support (percentage) are indicated for selected internal branches.

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Novel bacteriophages containing a genome of another bacteriophage within their genomes - PubMed (original) (raw)