#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Bacteriophage Crosstalk: Coordination of Prophage Induction by Trans-Acting Antirepressors


Many species of bacteria harbor multiple prophages in their genomes. Prophages often carry genes that confer a selective advantage to the bacterium, typically during host colonization. Prophages can convert to infectious viruses through a process known as induction, which is relevant to the spread of bacterial virulence genes. The paradigm of prophage induction, as set by the phage Lambda model, sees the process initiated by the RecA-stimulated self-proteolysis of the phage repressor. Here we show that a large family of lambdoid prophages found in Salmonella genomes employs an alternative induction strategy. The repressors of these phages are not cleaved upon induction; rather, they are inactivated by the binding of small antirepressor proteins. Formation of the complex causes the repressor to dissociate from DNA. The antirepressor genes lie outside the immunity region and are under direct control of the LexA repressor, thus plugging prophage induction directly into the SOS response. GfoA and GfhA, the antirepressors of Salmonella prophages Gifsy-1 and Gifsy-3, each target both of these phages' repressors, GfoR and GfhR, even though the latter proteins recognize different operator sites and the two phages are heteroimmune. In contrast, the Gifsy-2 phage repressor, GtgR, is insensitive to GfoA and GfhA, but is inactivated by an antirepressor from the unrelated Fels-1 prophage (FsoA). This response is all the more surprising as FsoA is under the control of the Fels-1 repressor, not LexA, and plays no apparent role in Fels-1 induction, which occurs via a Lambda CI-like repressor cleavage mechanism. The ability of antirepressors to recognize non-cognate repressors allows coordination of induction of multiple prophages in polylysogenic strains. Identification of non-cleavable gfoR/gtgR homologues in a large variety of bacterial genomes (including most Escherichia coli genomes in the DNA database) suggests that antirepression-mediated induction is far more common than previously recognized.


Vyšlo v časopise: Bacteriophage Crosstalk: Coordination of Prophage Induction by Trans-Acting Antirepressors. PLoS Genet 7(6): e32767. doi:10.1371/journal.pgen.1002149
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002149

Souhrn

Many species of bacteria harbor multiple prophages in their genomes. Prophages often carry genes that confer a selective advantage to the bacterium, typically during host colonization. Prophages can convert to infectious viruses through a process known as induction, which is relevant to the spread of bacterial virulence genes. The paradigm of prophage induction, as set by the phage Lambda model, sees the process initiated by the RecA-stimulated self-proteolysis of the phage repressor. Here we show that a large family of lambdoid prophages found in Salmonella genomes employs an alternative induction strategy. The repressors of these phages are not cleaved upon induction; rather, they are inactivated by the binding of small antirepressor proteins. Formation of the complex causes the repressor to dissociate from DNA. The antirepressor genes lie outside the immunity region and are under direct control of the LexA repressor, thus plugging prophage induction directly into the SOS response. GfoA and GfhA, the antirepressors of Salmonella prophages Gifsy-1 and Gifsy-3, each target both of these phages' repressors, GfoR and GfhR, even though the latter proteins recognize different operator sites and the two phages are heteroimmune. In contrast, the Gifsy-2 phage repressor, GtgR, is insensitive to GfoA and GfhA, but is inactivated by an antirepressor from the unrelated Fels-1 prophage (FsoA). This response is all the more surprising as FsoA is under the control of the Fels-1 repressor, not LexA, and plays no apparent role in Fels-1 induction, which occurs via a Lambda CI-like repressor cleavage mechanism. The ability of antirepressors to recognize non-cognate repressors allows coordination of induction of multiple prophages in polylysogenic strains. Identification of non-cleavable gfoR/gtgR homologues in a large variety of bacterial genomes (including most Escherichia coli genomes in the DNA database) suggests that antirepression-mediated induction is far more common than previously recognized.


Zdroje

1. CookeFJBrownDJFookesMPickardDIvensA 2008 Characterization of the genomes of a diverse collection of Salmonella enterica serovar Typhimurium definitive phage type 104. J Bacteriol 190 8155 8162

2. Figueroa-BossiNUzzauSMaloriolDBossiL 2001 Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella. Mol Microbiol 39 260 271

3. ThomsonNBakerSPickardDFookesMAnjumM 2004 The role of prophage-like elements in the diversity of Salmonella enterica serovars. J Mol Biol 339 279 300

4. WaldorMKFriedmanDI 2005 Phage regulatory circuits and virulence gene expression. Curr Opin Microbiol 8 459 465

5. TylerJSMillsMJFriedmanDI 2004 The operator and early promoter region of the Shiga toxin type 2-encoding bacteriophage 933W and control of toxin expression. J Bacteriol 186 7670 7679

6. WagnerPLLivnyJNeelyMNAchesonDWFriedmanDI 2002 Bacteriophage control of Shiga toxin 1 production and release by Escherichia coli. Mol Microbiol 44 957 970

7. BossiLFigueroa-BossiN 2005 Prophage arsenal of Salmonella enterica serovar Typhimurium. WaldorMFriedmanDAdhyaS Phages: Their Role in Bacterial Pathogenesis and Biotechnology Washington, DC ASM Press 165 186

8. LemireSFigueroa-BossiNBossiL 2008 Prophage Contribution to Salmonella Virulence and Diversity. HenselMSchmidtH Horizontal Gene Transfer in the Evolution of Bacterial Pathogenesis Cambridge, England Cambridge University 159 191

9. Figueroa-BossiNCoissacENetterPBossiL 1997 Unsuspected prophage-like elements in Salmonella typhimurium. Mol Microbiol 25 161 173

10. LemireSFigueroa-BossiNBossiL 2008 A singular case of prophage complementation in mutational activation of recET orthologs in Salmonella enterica serovar Typhimurium. J Bacteriol 190 6857 6866

11. EffantinGFigueroa-BossiNSchoehnGBossiLConwayJF 2010 The tripartite capsid gene of Salmonella phage Gifsy-2 yields a capsid assembly pathway engaging features from HK97 and λ. Virology 402 355 365

12. JarvikTSmillieCGroismanEAOchmanH 2010 Short-term signatures of evolutionary change in the Salmonella enterica serovar Typhimurium 14028 genome. J Bacteriol 192 560 567

13. GalkinVEYuXBielnickiJNdjonkaDBellCE 2009 Cleavage of bacteriophage λ cI repressor involves the RecA C-terminal domain. J Mol Biol 385 779 787

14. NdjonkaDBellCE 2006 Structure of a hyper-cleavable monomeric fragment of phage λ repressor containing the cleavage site region. J Mol Biol 362 479 489

15. PaboCOSauerRTSturtevantJMPtashneM 1979 The λ repressor contains two domains. Proc Natl Acad Sci U S A 76 1608 1612

16. SauerRTRossMJPtashneM 1982 Cleavage of the λ and P22 repressors by recA protein. J Biol Chem 257 4458 4462

17. MardanovAVRavinNV 2007 The antirepressor needed for induction of linear plasmid-prophage N15 belongs to the SOS regulon. J Bacteriol 189 6333 6338

18. ShearwinKEBrumbyAMEganJB 1998 The Tum protein of coliphage 186 is an antirepressor. J Biol Chem 273 5708 5715

19. HoisethSKStockerBA 1981 Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291 238 239

20. UzzauSFigueroa-BossiNRubinoSBossiL 2001 Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci U S A 98 15264 15269

21. McClellandMSandersonKESpiethJCliftonSWLatreilleP 2001 Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413 852 856

22. BunnyKLiuJRothJ 2002 Phenotypes of lexA mutations in Salmonella enterica: evidence for a lethal lexA null phenotype due to the Fels-2 prophage. J Bacteriol 184 6235 6249

23. LittleJWHarperJE 1979 Identification of the lexA gene product of Escherichia coli K-12. Proc Natl Acad Sci U S A 76 6147 6151

24. LamontIBrumbyAMEganJB 1989 UV induction of coliphage 186: prophage induction as an SOS function. Proc Natl Acad Sci U S A 86 5492 5496

25. BurgessRRArthurTMPietzBC 2000 Mapping protein-protein interaction domains using ordered fragment ladder far-western analysis of hexahistidine-tagged fusion proteins. Methods Enzymol 328 141 157

26. FaubladierMBouchéJP 1994 Division inhibition gene dicF of Escherichia coli reveals a widespread group of prophage sequences in bacterial genomes. J Bacteriol 176 1150 1156

27. LusettiSLVoloshinONInmanRBCamerini-OteroRDCoxMM 2004 The DinI protein stabilizes RecA protein filaments. J Biol Chem 279 30037 30046

28. VoloshinONRamirezBEBaxACamerini-OteroRD 2001 A model for the abrogation of the SOS response by an SOS protein: a negatively charged helix in DinI mimics DNA in its interaction with RecA. Genes Dev 15 415 427

29. YasudaTNagataTOhmoriH 1996 Multicopy suppressors of the cold-sensitive phenotype of the pcsA68 (dinD68) mutation in Escherichia coli. J Bacteriol 178 3854 3859

30. KimseyHHWaldorMK 2009 Vibrio cholerae LexA coordinates CTX prophage gene expression. J Bacteriol 191 6788 6795

31. QuinonesMKimseyHHWaldorMK 2005 LexA cleavage is required for CTX prophage induction. Mol Cell 17 291 300

32. NickelsBE 2009 A new twist on a classic paradigm: illumination of a genetic switch in Vibrio cholerae phage CTXφ. J Bacteriol 191 6779 6781

33. DavisBMKimseyHHKaneAVWaldorMK 2002 A satellite phage-encoded antirepressor induces repressor aggregation and cholera toxin gene transfer. EMBO J 21 4240 4249

34. McLeodSMKimseyHHDavisBMWaldorMK 2005 CTXφ and Vibrio cholerae: exploring a newly recognized type of phage-host cell relationship. Mol Microbiol 57 347 356

35. SusskindMMBotsteinD 1975 Mechanism of action of Salmonella phage P22 antirepressor. J Mol Biol 98 413 424

36. SusskindMMBotsteinD 1978 Molecular genetics of bacteriophage P22. Microbiol Rev 42 385 413

37. PrellHH 1978 Ant-mediated transactivation of early genes in Salmonella prophage P22 by superinfecting virulent P22 mutants. Mol Gen Genet 164 331 334

38. BertaniG 2004 Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J Bacteriol 186 595 600

39. SchmiegerH 1972 Phage P22-mutants with increased or decreased transduction abilities. Mol Gen Genet 119 75 88

40. BochnerBR 1984 Curing bacterial cells of lysogenic viruses by using UCB indicator plates. Biotechniques 2 234 240

41. DatsenkoKAWannerBL 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

42. MurphyKCCampelloneKGPoteeteAR 2000 PCR-mediated gene replacement in Escherichia coli. Gene 246 321 330

43. YuDEllisHMLeeECJenkinsNACopelandNG 2000 An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci U S A 97 5978 5983

44. CherepanovPPWackernagelW 1995 Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158 9 14

45. SpiritoFBossiL 1996 Long-distance effect of downstream transcription on activity of the supercoiling-sensitive leu-500 promoter in a topA mutant of Salmonella typhimurium. J Bacteriol 178 7129 7137

46. MillerVLMekalanosJJ 1988 A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170 2575 2583

47. Figueroa-BossiNLemireSMaloriolDBalbontínRCasadesúsJ 2006 Loss of Hfq activates the σE-dependent envelope stress response in Salmonella enterica. Mol Microbiol 62 838 852

48. MillerJH 1992 A Short Course in Bacterial Genetics. A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria Cold Spring Harbor, New York Cold Spring Harbor Laboratory Press

49. LilleengenK 1948 Typing of Salmonella typhimurium by means of bacteriophage. Acta Pathol Microbiol Scand 77 2 125

50. FieldsPISwansonRVHaidarisCGHeffronF 1986 Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci U S A 83 5189 5193

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 6
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#