Expression of a Novel P22 ORFan Gene Reveals the Phage Carrier State in Typhimurium
We discovered a novel interaction between phage P22 and its host Salmonella Typhimurium LT2 that is characterized by a phage mediated and targeted derepression of the host dgo operon. Upon further investigation, this interaction was found to be instigated by an ORFan gene (designated pid for phage P22 encoded instigator of dgo expression) located on a previously unannotated moron locus in the late region of the P22 genome, and encoding an 86 amino acid protein of 9.3 kDa. Surprisingly, the Pid/dgo interaction was not observed during strict lytic or lysogenic proliferation of P22, and expression of pid was instead found to arise in cells that upon infection stably maintained an unintegrated phage chromosome that segregated asymmetrically upon subsequent cell divisions. Interestingly, among the emerging siblings, the feature of pid expression remained tightly linked to the cell inheriting this phage carrier state and became quenched in the other. As such, this study is the first to reveal molecular and genetic markers authenticating pseudolysogenic development, thereby exposing a novel mechanism, timing, and populational distribution in the realm of phage–host interactions.
Vyšlo v časopise:
Expression of a Novel P22 ORFan Gene Reveals the Phage Carrier State in Typhimurium. PLoS Genet 9(2): e32767. doi:10.1371/journal.pgen.1003269
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003269
Souhrn
We discovered a novel interaction between phage P22 and its host Salmonella Typhimurium LT2 that is characterized by a phage mediated and targeted derepression of the host dgo operon. Upon further investigation, this interaction was found to be instigated by an ORFan gene (designated pid for phage P22 encoded instigator of dgo expression) located on a previously unannotated moron locus in the late region of the P22 genome, and encoding an 86 amino acid protein of 9.3 kDa. Surprisingly, the Pid/dgo interaction was not observed during strict lytic or lysogenic proliferation of P22, and expression of pid was instead found to arise in cells that upon infection stably maintained an unintegrated phage chromosome that segregated asymmetrically upon subsequent cell divisions. Interestingly, among the emerging siblings, the feature of pid expression remained tightly linked to the cell inheriting this phage carrier state and became quenched in the other. As such, this study is the first to reveal molecular and genetic markers authenticating pseudolysogenic development, thereby exposing a novel mechanism, timing, and populational distribution in the realm of phage–host interactions.
Zdroje
1. RohwerF (2003) Global phage diversity. Cell 113: 141.
2. BreitbartM, RohwerF (2005) Here a virus, there a virus, everywhere the same virus? Trends Microbiol 13: 278–284.
3. PalC, MaciáMD, OliverA, SchacharI, BucklingA (2007) Coevolution with viruses drives the evolution of bacterial mutation rates. Nature 450: 1079–1081.
4. BreitbartM (2012) Marine Viruses: Truth or Dare. Annu Rev Marine Sci 4: 425–448.
5. SuttleCA (2007) Marine viruses — major players in the global ecosystem. Nat Rev Microbiol 5: 801–812.
6. BrüssowH, CanchayaC, HardtW-D (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68: 560–602.
7. Ptashne M (2004) A genetic switch. Gann A, Inglis J, Dickerson M, Frey M, Schaefer S, editors. New York: Cold Spring Harbor Laboratory Press. 154p.
8. SternbergN, HoessR (1983) The molecular genetics of bacteriophage P1. Annu Rev Genet 17: 123–154.
9. SusskindMM, BotsteinD (1978) Molecular genetics of bacteriophage P22. Microbiol Rev 42: 385–413.
10. SuttleCA (2005) Viruses in the sea. Nature 437: 356–361.
11. ŁosM, WegrzynG (2012) Pseudolysogeny. Adv Virus Res 82: 339–349.
12. RippS, MillerRV (1997) The role of pseudolysogeny in bacteriophage-host interactions in a natural freshwater environment. Microbiology 143: 2065–2070.
13. RippS, MillerRV (1998) Dynamics of the pseudolysogenic response in slowly growing cells of Pseudomonas aeruginosa. Microbiology 144: 2225–2232.
14. ClokieMR, MillardAD, LetarovAV, HeaphyS (2011) Phages in nature. Bacteriophage 1: 31–45.
15. RigaliS, DerouauxA, GiannottaF, DusartJ (2002) Subdivision of the helix-turn-helix GntR family of bacterial regulators in the FadR, HutC, MocR, and YtrA subfamilies. J Biol Chem 277: 12507–12515.
16. Vander BylC, KropinskiAM (2000) Sequence of the genome of Salmonella bacteriophage P22. J Bacteriol 182: 6472–6481.
17. PedullaML, FordME, KarthikeyanT, HoutzJM, HendrixRW, et al. (2003) Corrected sequence of the bacteriophage P22 genome. J Bacteriol 185: 1475–1477.
18. HayesWS, BorodovskyM (1998) Deriving ribosomal binding site (RBS) statistical models from unannotated DNA sequences and the use of the RBS model for N-terminal prediction. Pac Symp Biocomput 279–290.
19. LiY, AustinS (2002) The P1 plasmid in action: time-lapse photomicroscopy reveals some unexpected aspects of plasmid partition. Plasmid 48: 174–178.
20. LehnherrH, MaguinE, JafriS, YarmolinskyMB (1993) Plasmid addiction genes of bacteriophage P1: doc, which causes cell death on curing of prophage, and phd, which prevents host death when prophage is retained. J Mol Biol 233: 414–428.
21. ZinderN (1958) Lysogenization and superinfection immunity in Salmonella. Virology 5: 291–326.
22. RoucourtB, LavigneR (2009) The role of interactions between phage and bacterial proteins within the infected cell: a diverse and puzzling interactome. Environmental Microbiology 11: 2789–2805.
23. Figueroa-BossiN, BossiL (1999) Inducible prophages contribute to Salmonella virulence in mice. Mol Microbiol 33: 167–176.
24. ChenY, GoldingI, SawaiS, GuoL, CoxEC (2005) Population fitness and the regulation of Escherichia coli genes by bacterial viruses. PLoS Biol 3: e229 doi:10.1371/journal.pbio.0030229.
25. ErikssonS, LucchiniS, ThompsonA, RhenM, HintonJCD (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47: 103–118.
26. KuYW, McDonoughSP, PalaniappanRUM, ChangCF, ChangYF (2005) Novel attenuated Salmonella enterica serovar Choleraesuis strains as live vaccine candidates generated by signature-tagged mutagenesis. Infect Immun 73: 8194–8203.
27. Sambrook J, Russel DW (2001) Molecular cloning (a laboratory manual). New York: Cold Spring Harbor Laboratory press. 2344p.
28. Davis R, Botstein D, Roth J (1980) Advanced bacterial genetics. New York: Cold Spring Harbor Laboratory Press. 254p.
29. SchmiegerH (1972) Phage P22-mutants with increased or decreased transduction abilities. Mol Genet Genomics 119: 75–88.
30. Miller JH (1992) A short course in bacterial genetics. New York: Cold Spring Harbor Laboratory Press. 876p.
31. AertsenA, Tesfazgi MebrhatuM, MichielsCW (2008) Activation of the Salmonella Typhimurium Mrr protein. Biochem Biophys Res Commun 367: 435–439.
32. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.
33. DarlingAE, MauB, PernaNT (2010) progressiveMauve: Multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5: e11147 doi:10.1371/journal.pone.0011147.
34. HughesKT, RothJR (1988) Transitory cis complementation: a method for providing transposition functions to defective transposons. Genetics 119: 9–12.
35. DatsenkoKA, WannerBL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640–6645.
36. CherepanovPP, WackernagelW (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.
37. LindnerAB, MaddenR, DemarezA, StewartEJ, TaddeiF (2008) Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proceedings of the National Academy of Sciences 105: 3076–3081.
38. EspeliO, MercierR, BoccardF (2008) DNA dynamics vary according to macrodomain topography in the E. coli chromosome. Mol Microbiol 68: 1418–1427.
39. SawitzkeJA, CostantinoN, LiX-T, ThomasonLC, BubunenkoM, et al. (2011) Probing cellular processes with oligo-mediated recombination and using the knowledge gained to optimize recombineering. J Mol Biol 407: 45–59.
40. ValdiviaRH, FalkowS (1996) Bacterial genetics by flow cytometry: rapid isolation of Salmonella Typhimurium acid-inducible promoters by differential fluorescence induction. Mol Microbiol 22: 367–378.
41. AustinS, LiY (2002) The P1 plasmid is segregated to daughter cells by a “capture and ejection” mechanism coordinated with Escherichia coli cell division. Mol Microbiol 46: 63–74.
42. NielsenHJ, LiY, YoungrenB, HansenFG, AustinS (2006) Progressive segregation of the Escherichia coli chromosome. Mol Microbiol 61: 383–393.
43. HeukeshovenJ, DernickR (1988) Improved silver staining procedure for fast staining in PhastSystem Development Unit. I. Staining of sodium dodecyl sulfate gels. Electrophoresis 9: 28–32.
44. ShevchenkoA, WilmM, VormO, MannM (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850–858.
45. StewartEJ, MaddenR, PaulG, TaddeiF (2005) Aging and death in an organism that reproduces by morphologically symmetric division. PLoS Biol 3: e45 doi:10.1371/journal.pbio.0030045.
46. McClellandM, SandersonKE, SpiethJ, CliftonSW, LatreilleP, et al. (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852–856.
47. CasjensSR (2005) Comparative genomics and evolution of the tailed-bacteriophages. Curr Opin Microbiol 8: 451–458.
48. ValdiviaRH, FalkowS (1997) Fluorescence-based isolation of bacterial genes expressed within host cells. Science 277: 2007–2011.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2013 Číslo 2
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Complex Inheritance of Melanoma and Pigmentation of Coat and Skin in Grey Horses
- Coordination of Chromatid Separation and Spindle Elongation by Antagonistic Activities of Mitotic and S-Phase CDKs
- Autophagy Induction Is a Tor- and Tp53-Independent Cell Survival Response in a Zebrafish Model of Disrupted Ribosome Biogenesis
- Assembly of the Auditory Circuitry by a Genetic Network in the Mouse Brainstem