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Viral evasion of a bacterial suicide system by RNA-based molecular mimicry enables infectious altruism.

Blower TR, Evans TJ, Przybilski R, Fineran PC, Salmond GP - PLoS Genet. (2012)

Bottom Line: The ΦTE escape mutants had expanded the number of these "pseudo-ToxI" genetic repeats and, in one case, an escape phage had "hijacked" ToxI from the plasmid-borne toxIN locus, through recombination.This is the first example of a non-coding RNA encoded by a phage that evolves by selective expansion and recombination to enable viral suppression of a defensive bacterial suicide system.Furthermore, the ΦTE escape phages had evolved enhanced capacity to transduce replicons expressing ToxIN, demonstrating virus-mediated horizontal transfer of genetic altruism.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom.

ABSTRACT
Abortive infection, during which an infected bacterial cell commits altruistic suicide to destroy the replicating bacteriophage and protect the clonal population, can be mediated by toxin-antitoxin systems such as the Type III protein-RNA toxin-antitoxin system, ToxIN. A flagellum-dependent bacteriophage of the Myoviridae, ΦTE, evolved rare mutants that "escaped" ToxIN-mediated abortive infection within Pectobacterium atrosepticum. Wild-type ΦTE encoded a short sequence similar to the repetitive nucleotide sequence of the RNA antitoxin, ToxI, from ToxIN. The ΦTE escape mutants had expanded the number of these "pseudo-ToxI" genetic repeats and, in one case, an escape phage had "hijacked" ToxI from the plasmid-borne toxIN locus, through recombination. Expression of the pseudo-ToxI repeats during ΦTE infection allowed the phage to replicate, unaffected by ToxIN, through RNA-based molecular mimicry. This is the first example of a non-coding RNA encoded by a phage that evolves by selective expansion and recombination to enable viral suppression of a defensive bacterial suicide system. Furthermore, the ΦTE escape phages had evolved enhanced capacity to transduce replicons expressing ToxIN, demonstrating virus-mediated horizontal transfer of genetic altruism.

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Related in: MedlinePlus

ΦTE morphology and genome overview.(A–B) Transmission electron micrographs of individual ΦTE virus particles. The tail is fully extended in (A) and contracted in (B). Each scale bar represents 100 nm. (C) Summary of the 142,349 bp circularly-permuted genome of ΦTE, including all ORFs (colour coded to function where possible), two tRNAs and the ncRNA comprising pseudo-ToxI, encoded by the escape locus (Table S2). Selected ΦTE genes are indicated by “TE_x” around the genome, for orientation. GC skew and GC content are shown along with the tBLASTx results against two related phages, coliphage rv5 and Salmonella phage PVP-SE1.
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pgen-1003023-g001: ΦTE morphology and genome overview.(A–B) Transmission electron micrographs of individual ΦTE virus particles. The tail is fully extended in (A) and contracted in (B). Each scale bar represents 100 nm. (C) Summary of the 142,349 bp circularly-permuted genome of ΦTE, including all ORFs (colour coded to function where possible), two tRNAs and the ncRNA comprising pseudo-ToxI, encoded by the escape locus (Table S2). Selected ΦTE genes are indicated by “TE_x” around the genome, for orientation. GC skew and GC content are shown along with the tBLASTx results against two related phages, coliphage rv5 and Salmonella phage PVP-SE1.

Mentions: Mutant Pba strain SCC34 has a mucoid morphology that provides resistance to infection by lipopolysaccharide (LPS)-dependent phages, such as the generalised transducing phage ΦM1 [20], [21]. ΦTE was initially isolated from treated sewage effluent enriched for phages using SCC34 as host, as part of a screen for lipopolysaccharide (LPS)-independent phages. Using transmission electron microscopy, ΦTE was seen to have an isometric, icosahedral, head measuring 98 ±4 nm from flat face to flat face and a tail measuring 124±3 nm when extended (Figure 1A), or 65±7 nm when contracted (Figure 1B). ΦTE was classified as a member of the Myoviridae of the order Caudovirales [22]. A bank of ΦTE-resistant transposon-mutants of Pba was generated in order to identify the host receptor for ΦTE. These mutants of Pba remained sensitive to ΦM1 but were resistant to the flagellum-dependent phage, ΦAT1 [23]. Seven of the transposon insertions conferring ΦTE-resistance disrupted genes involved in flagellum biosynthesis (Table S1), suggesting that the host receptor for ΦTE was the flagellum. Restriction enzyme digestion analysis of the extracted ΦTE genome showed that it was terminally redundant and circularly permuted (Figure S1).


Viral evasion of a bacterial suicide system by RNA-based molecular mimicry enables infectious altruism.

Blower TR, Evans TJ, Przybilski R, Fineran PC, Salmond GP - PLoS Genet. (2012)

ΦTE morphology and genome overview.(A–B) Transmission electron micrographs of individual ΦTE virus particles. The tail is fully extended in (A) and contracted in (B). Each scale bar represents 100 nm. (C) Summary of the 142,349 bp circularly-permuted genome of ΦTE, including all ORFs (colour coded to function where possible), two tRNAs and the ncRNA comprising pseudo-ToxI, encoded by the escape locus (Table S2). Selected ΦTE genes are indicated by “TE_x” around the genome, for orientation. GC skew and GC content are shown along with the tBLASTx results against two related phages, coliphage rv5 and Salmonella phage PVP-SE1.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3475682&req=5

pgen-1003023-g001: ΦTE morphology and genome overview.(A–B) Transmission electron micrographs of individual ΦTE virus particles. The tail is fully extended in (A) and contracted in (B). Each scale bar represents 100 nm. (C) Summary of the 142,349 bp circularly-permuted genome of ΦTE, including all ORFs (colour coded to function where possible), two tRNAs and the ncRNA comprising pseudo-ToxI, encoded by the escape locus (Table S2). Selected ΦTE genes are indicated by “TE_x” around the genome, for orientation. GC skew and GC content are shown along with the tBLASTx results against two related phages, coliphage rv5 and Salmonella phage PVP-SE1.
Mentions: Mutant Pba strain SCC34 has a mucoid morphology that provides resistance to infection by lipopolysaccharide (LPS)-dependent phages, such as the generalised transducing phage ΦM1 [20], [21]. ΦTE was initially isolated from treated sewage effluent enriched for phages using SCC34 as host, as part of a screen for lipopolysaccharide (LPS)-independent phages. Using transmission electron microscopy, ΦTE was seen to have an isometric, icosahedral, head measuring 98 ±4 nm from flat face to flat face and a tail measuring 124±3 nm when extended (Figure 1A), or 65±7 nm when contracted (Figure 1B). ΦTE was classified as a member of the Myoviridae of the order Caudovirales [22]. A bank of ΦTE-resistant transposon-mutants of Pba was generated in order to identify the host receptor for ΦTE. These mutants of Pba remained sensitive to ΦM1 but were resistant to the flagellum-dependent phage, ΦAT1 [23]. Seven of the transposon insertions conferring ΦTE-resistance disrupted genes involved in flagellum biosynthesis (Table S1), suggesting that the host receptor for ΦTE was the flagellum. Restriction enzyme digestion analysis of the extracted ΦTE genome showed that it was terminally redundant and circularly permuted (Figure S1).

Bottom Line: The ΦTE escape mutants had expanded the number of these "pseudo-ToxI" genetic repeats and, in one case, an escape phage had "hijacked" ToxI from the plasmid-borne toxIN locus, through recombination.This is the first example of a non-coding RNA encoded by a phage that evolves by selective expansion and recombination to enable viral suppression of a defensive bacterial suicide system.Furthermore, the ΦTE escape phages had evolved enhanced capacity to transduce replicons expressing ToxIN, demonstrating virus-mediated horizontal transfer of genetic altruism.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom.

ABSTRACT
Abortive infection, during which an infected bacterial cell commits altruistic suicide to destroy the replicating bacteriophage and protect the clonal population, can be mediated by toxin-antitoxin systems such as the Type III protein-RNA toxin-antitoxin system, ToxIN. A flagellum-dependent bacteriophage of the Myoviridae, ΦTE, evolved rare mutants that "escaped" ToxIN-mediated abortive infection within Pectobacterium atrosepticum. Wild-type ΦTE encoded a short sequence similar to the repetitive nucleotide sequence of the RNA antitoxin, ToxI, from ToxIN. The ΦTE escape mutants had expanded the number of these "pseudo-ToxI" genetic repeats and, in one case, an escape phage had "hijacked" ToxI from the plasmid-borne toxIN locus, through recombination. Expression of the pseudo-ToxI repeats during ΦTE infection allowed the phage to replicate, unaffected by ToxIN, through RNA-based molecular mimicry. This is the first example of a non-coding RNA encoded by a phage that evolves by selective expansion and recombination to enable viral suppression of a defensive bacterial suicide system. Furthermore, the ΦTE escape phages had evolved enhanced capacity to transduce replicons expressing ToxIN, demonstrating virus-mediated horizontal transfer of genetic altruism.

Show MeSH
Related in: MedlinePlus