Viral Evasion of a Bacterial Suicide System by RNA–Based Molecular Mimicry Enables Infectious Altruism

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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.

Vyšlo v časopise: Viral Evasion of a Bacterial Suicide System by RNA–Based Molecular Mimicry Enables Infectious Altruism. PLoS Genet 8(10): e32767. doi:10.1371/journal.pgen.1003023
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003023

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Zdroje

1. FozoEM, MakarovaKS, ShabalinaSA, YutinN, KooninEV, et al. (2010) Abundance of type I toxin-antitoxin systems in bacteria: searches for new candidates and discovery of novel families. Nucl Acids Res 38: 3743–3759.

2. LeplaeR, GeeraertsD, HallezR, GuglielminiJ, DrezeP, et al. (2011) Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucl Acids Res 39: 5513–5525.

3. BlowerTR, ShortFL, RaoF, MizuguchiK, PeiXY, et al. (2012) Identification and classification of bacterial Type III toxin-antitoxin systems encoded in chromosomal and plasmid genomes. Nucl Acids Res doi:10.1093/nar/gks231

4. BlowerTR, SalmondGP, LuisiBF (2011) Balancing at survival's edge: the structure and adaptive benefits of prokaryotic toxin-antitoxin partners. Curr Opin Struc Biol 21: 109–118.

5. OguraT, HiragaS (1983) Mini-F plasmid genes that couple host cell division to plasmid proliferation. Proc Natl Acad Sci U S A 80: 4784–4788.

6. GerdesK, ChristensenSK, Lobner-OlesenA (2005) Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 3: 371–382.

7. MaisonneuveE, ShakespeareLJ, JorgensenMG, GerdesK (2011) Bacterial persistence by RNA endonucleases. Proc Natl Acad Sci U S A 108: 13206–13211.

8. MagnusonRD (2007) Hypothetical functions of toxin-antitoxin systems. J Bacteriol 189: 6089–6092.

9. PecotaDC, WoodTK (1996) Exclusion of T4 phage by the hok/sok killer locus from plasmid R1. J Bacteriol 178: 2044–2050.

10. HazanR, Engelberg-KulkaH (2004) Escherichia coli mazEF-mediated cell death as a defense mechanism that inhibits the spread of phage P1. Mol Genet Genomics 272: 227–234.

11. FineranPC, BlowerTR, FouldsIJ, HumphreysDP, LilleyKS, et al. (2009) The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc Natl Acad Sci U S A 106: 894–899.

12. BlowerTR, FineranPC, JohnsonMJ, TothIK, HumphreysDP, et al. (2009) Mutagenesis and functional characterisation of the RNA and protein components of the toxIN abortive infection and toxin-antitoxin locus of Erwinia. J Bacteriol 191: 6029–6039.

13. BlowerTR, PeiXY, ShortFL, FineranPC, HumphreysDP, et al. (2011) A processed non-coding RNA regulates an altruistic bacterial antiviral system. Nat Struc Mol Biol 18: 185–190.

14. EmondE, HollerBJ, BoucherI, VandenberghPA, VedamuthuER, et al. (1998) AbiQ, an abortive infection mechanism from Lactococcus lactis. Appl Environ Microbiol 64: 4748–4756.

15. LabrieSJ, SamsonJE, MoineauS (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8: 317–327.

16. ChopinMC, ChopinA, BidnenkoE (2005) Phage abortive infection in lactococci: variations on a theme. Curr Opin Microbiol 8: 473–479.

17. BouchardJD, MoineauS (2004) Lactococcal phage genes involved in sensitivity to AbiK and their relation to single-strand annealing proteins. J Bacteriol 186: 3649–3652.

18. HaaberJ, RousseauGM, HammerK, MoineauS (2009) Identification and characterization of the phage gene sav, involved in sensitivity to the lactococcal abortive infection mechanism AbiV. Appl Environ Microbiol 75: 2484–2494.

19. BellKS, SebaihiaM, PritchardL, HoldenMT, HymanLJ, et al. (2004) Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci U S A 101: 11105–11110.

20. TothIK, MulhollandV, CooperV, BentleyS, ShihY-L, et al. (1997) Generalized transduction in the potato blackleg pathogen Erwinia carotovora subsp. atroseptica by bacteriophage ΦM1. Microbiology 143: 2433–2438.

21. Evans TJ (2009) Investigation of bacteriophages and their use in the analysis of enterobacterial virulence. Ph.D Thesis, Department of Biochemistry, University of Cambridge, UK.

22. AckermannHW, DuBowMS, GershmanM, Karska-WysockiB, KasatiyaSS, et al. (1997) Taxonomic changes in tailed phages of enterobacteria. Arch Virol 142: 1381–1390.

23. EvansTJ, TraunerA, KomitopoulouE, SalmondGP (2010) Exploitation of a new flagellatropic phage of Erwinia for positive selection of bacterial mutants attenuated in plant virulence: towards phage therapy. J Appl Microbiol 108: 676–685.

24. SantosSB, KropinskiAM, CeyssensPJ, AckermannHW, VillegasA, et al. (2011) Genomic and Proteomic Characterization of the Broad-Host-Range Salmonella Phage PVP-SE1: Creation of a New Phage Genus. J Virol 85: 11265–11273.

25. GuzmanLM, BelinD, CarsonMJ, BeckwithJ (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121–4130.

26. ChangAC, CohenSN (1978) Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134: 1141–1156.

27. LiuH, CoulthurstSJ, PritchardL, HedleyPE, RavensdaleM, et al. (2008) Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog 4: e1000093 doi:10.1371/journal.ppat.1000093

28. DatsenkoKA, WannerBL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640–6645.

29. LabrieSJ, MoineauS (2007) Abortive infection mechanisms and prophage sequences significantly influence the genetic makeup of emerging lytic lactococcal phages. J Bacteriol 189: 1482–1487.

30. HillC, MillerLA, KlaenhammerTR (1991) In vivo genetic exchange of a functional domain from a type II A methylase between lactococcal plasmid pTR2030 and a virulent bacteriophage. J Bacteriol 173: 4363–4370.

31. WeinbergZ, PerreaultJ, MeyerMM, BreakerRR (2009) Exceptional structured noncoding RNAs revealed by bacterial metagenome analysis. Nature 462: 656–659.

32. RobertsF, AllisonGE, VermaNK (2007) Transcription-termination-mediated immunity and its prevention in bacteriophage SfV of Shigella flexneri. J Gen Virol 88: 3187–3197.

33. PettyNK, ToribioAL, GouldingD, FouldsI, ThomsonN, DouganG, SalmondGPC (2007) A generalized transducing phage for the murine pathogen Citrobacter rodentium. Microbiology 153: 2984–2988.

34. MonsonR, FouldsI, FowerakerJ, WelchM, SalmondGPC (2011) The Pseudomonas aeruginosa generalized transducing phage phiPA3 is a new member of the phiKZ-like group of ‘jumbo’ phages, and infects model laboratory strains and clinical isolates from cystic fibrosis patients. Microbiology 157: 859–867.

35. HaaberJ, MoineauS, HammerK (2009) Activation and transfer of the chromosomal phage resistance mechanism AbiV in Lactococcus lactis. Appl Environ Microbiol 75: 3358–3361.

36. KlaenhammerTR, SanozkyRB (1985) Conjugal transfer from Streptococcus lactis ME2 of plasmids encoding phage resistance, nisin resistance and lactose-fermenting ability: evidence for a high-frequency conjugative plasmid responsible for abortive infection of virulent bacteriophage. J Gen Microbiol 131: 1531–1541.

37. PettyNK, FouldsIJ, PradelE, EwbankJJ, SalmondGP (2006) A generalized transducing phage (ΦIF3) for the genomically sequenced Serratia marcescens strain Db11: a tool for functional genomics of an opportunistic human pathogen. Microbiology 152: 1701–1708.

38. DelcherAL, BratkeKA, PowersEC, SalzbergSL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23: 673–679.

39. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.

40. LoweTM, EddySR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucl Acids Res 25: 955–964.

41. SuzekBE, ErmolaevaMD, SchreiberM, SalzbergSL (2001) A probabilistic method for identifying start codons in bacterial genomes. Bioinformatics 17: 1123–1130.

42. RutherfordK, ParkhillJ, CrookJ, HorsnellT, RiceP, et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944–945.

43. GrantJR, StothardP (2008) The CGView Server: a comparative genomics tool for circular genomes. Nucl Acids Res 36: W181–184.

44. FineranPC, EversonL, SlaterH, SalmondGP (2005) A GntR family transcriptional regulator (PigT) controls gluconate-mediated repression and defines a new, independent pathway for regulation of the tripyrrole antibiotic, prodigiosin, in Serratia. Microbiology 151: 3833–3845.

45. PrzybilskiR, GrafS, LescouteA, NellenW, WesthofE, et al. (2005) Functional hammerhead ribozymes naturally encoded in the genome of Arabidopsis thaliana. Plant Cell 17: 1877–1885.

46. PrzybilskiR, RichterC, GristwoodT, ClulowJS, VercoeRB, et al. (2011) Csy4 is responsible for CRISPR RNA processing in Pectobacterium atrosepticum. RNA Biol 8: 517–528.