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PLoS One. 2012; 7(7): e40683.
Published online Jul 17, 2012. doi:  10.1371/journal.pone.0040683
PMCID: PMC3398947
Novel Bacteriophages Containing a Genome of Another Bacteriophage within Their Genomes
Maud M. Swanson,#1 Brian Reavy,#1* Kira S. Makarova,2 Peter J. Cock,1 David W. Hopkins,1¤ Lesley Torrance,1 Eugene V. Koonin,2 and Michael Taliansky1
1The James Hutton Institute, Invergowrie, Dundee, United Kingdom
2National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, United States of America
Ramy K. Aziz, Editor
Cairo University, Egypt
#Contributed equally.
* E-mail: Brian.Reavy/at/hutton.ac.uk
Conceived and designed the experiments: MMS BR DWH LT EVK MT. Performed the experiments: MMS BR. Analyzed the data: MMS BE KSM PJC EVK. Wrote the paper: MMS BR KSM PJC DWH LT EVK MT.
¤Current address: School of Life Sciences, Heriot-Watt University, Edinburgh, United Kingdom
Received March 1, 2012; Accepted June 14, 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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