Novel bacteriophages containing a genome of another bacteriophage within their genomes

Maud M Swanson, Brian Reavy, Kira S Makarova, Peter J Cock, David W Hopkins, Lesley Torrance, Eugene V Koonin, Michael Taliansky

Research output: Contribution to journalArticle

32 Citations (Scopus)

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.

Original languageEnglish
Article numbere40683
JournalPLoS ONE
Volume7
Issue number7
DOIs
Publication statusPrint publication - 2012
Externally publishedYes

Fingerprint

Bacteriophages
bacteriophages
Genes
Genome
genome
Bacillus thuringiensis
Prophages
Cereus
Siphoviridae
Bacilli
Bacillus thuringiensis subsp. kurstaki
Horizontal Gene Transfer
genes
Gene Regulatory Networks
Bacillus (bacteria)
DNA replication
Regulator Genes
Multigene Family
Bacillus cereus
DNA Replication

Keywords

  • Bacillus Phages/genetics
  • Bacillus subtilis/virology
  • Bacteriophages/genetics
  • Genes, Viral/genetics
  • Genome, Viral/genetics
  • Host Specificity/genetics
  • Open Reading Frames/genetics
  • Phylogeny
  • Siphoviridae/genetics
  • Sporosarcina/virology
  • Viral Proteins/chemistry
  • Virion/ultrastructure

Cite this

Swanson, M. M., Reavy, B., Makarova, K. S., Cock, P. J., Hopkins, D. W., Torrance, L., ... Taliansky, M. (2012). Novel bacteriophages containing a genome of another bacteriophage within their genomes. PLoS ONE, 7(7), [e40683]. https://doi.org/10.1371/journal.pone.0040683
Swanson, Maud M ; Reavy, Brian ; Makarova, Kira S ; Cock, Peter J ; Hopkins, David W ; Torrance, Lesley ; Koonin, Eugene V ; Taliansky, Michael. / Novel bacteriophages containing a genome of another bacteriophage within their genomes. In: PLoS ONE. 2012 ; Vol. 7, No. 7.
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Swanson, MM, Reavy, B, Makarova, KS, Cock, PJ, Hopkins, DW, Torrance, L, Koonin, EV & Taliansky, M 2012, 'Novel bacteriophages containing a genome of another bacteriophage within their genomes', PLoS ONE, vol. 7, no. 7, e40683. https://doi.org/10.1371/journal.pone.0040683

Novel bacteriophages containing a genome of another bacteriophage within their genomes. / Swanson, Maud M; Reavy, Brian; Makarova, Kira S; Cock, Peter J; Hopkins, David W; Torrance, Lesley; Koonin, Eugene V; Taliansky, Michael.

In: PLoS ONE, Vol. 7, No. 7, e40683, 2012.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Novel bacteriophages containing a genome of another bacteriophage within their genomes

AU - Swanson, Maud M

AU - Reavy, Brian

AU - Makarova, Kira S

AU - Cock, Peter J

AU - Hopkins, David W

AU - Torrance, Lesley

AU - Koonin, Eugene V

AU - Taliansky, Michael

PY - 2012

Y1 - 2012

N2 - 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.

AB - 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.

KW - Bacillus Phages/genetics

KW - Bacillus subtilis/virology

KW - Bacteriophages/genetics

KW - Genes, Viral/genetics

KW - Genome, Viral/genetics

KW - Host Specificity/genetics

KW - Open Reading Frames/genetics

KW - Phylogeny

KW - Siphoviridae/genetics

KW - Sporosarcina/virology

KW - Viral Proteins/chemistry

KW - Virion/ultrastructure

U2 - 10.1371/journal.pone.0040683

DO - 10.1371/journal.pone.0040683

M3 - Article

C2 - 22815791

VL - 7

JO - PLoS ONE

JF - PLoS ONE

SN - 1932-6203

IS - 7

M1 - e40683

ER -