Transposable Prophage Mu Is Organized as a Stable Chromosomal Domain of

English version České info

The E.
coli chromosome is compacted by segregation into 400–500 supercoiled domains by both active and passive mechanisms, for example, transcription and DNA-protein association. We find that prophage Mu is organized as a stable domain bounded by the proximal location of Mu termini L and R, which are 37 kbp apart on the Mu genome. Formation/maintenance of the Mu ‘domain’ configuration, reported by Cre-loxP recombination and 3C (chromosome conformation capture), is dependent on a strong gyrase site (SGS) at the center of Mu, the Mu L end and MuB protein, and the E. coli nucleoid proteins IHF, Fis and HU. The Mu domain was observed at two different chromosomal locations tested. By contrast, prophage λ does not form an independent domain. The establishment/maintenance of the Mu domain was promoted by low-level transcription from two phage promoters, one of which was domain dependent. We propose that the domain confers transposition readiness to Mu by fostering topological requirements of the reaction and the proximity of Mu ends. The potential benefits to the host cell from a subset of proteins expressed by the prophage may in turn help its long-term stability.

Vyšlo v časopise: Transposable Prophage Mu Is Organized as a Stable Chromosomal Domain of. PLoS Genet 9(11): e32767. doi:10.1371/journal.pgen.1003902
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003902

Souhrn

Zdroje

1. TraversA, MuskhelishviliG (2005) Bacterial chromatin. Curr Opin Genet Dev 15: 507–514.

2. SindenRR, PettijohnDE (1981) Chromosomes in living Escherichia coli cells are segregated into domains of supercoiling. Proc Natl Acad Sci U S A 78: 224–228.

3. PostowL, HardyCD, ArsuagaJ, CozzarelliNR (2004) Topological domain structure of the Escherichia coli chromosome. Genes Dev 18: 1766–1779.

4. DillonSC, DormanCJ (2010) Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 8: 185–195.

5. MacvaninM, AdhyaS (2012) Architectural organization in E. coli nucleoid. Biochim Biophys Acta 1819: 830–835.

6. ValensM, PenaudS, RossignolM, CornetF, BoccardF (2004) Macrodomain organization of the Escherichia coli chromosome. EMBO J 23: 4330–4341.

7. BoccardF, EsnaultE, ValensM (2005) Spatial arrangement and macrodomain organization of bacterial chromosomes. Mol Microbiol 57: 9–16.

8. WorcelA, BurgiE (1972) On the structure of the folded chromosome of Escherichia coli. J Mol Biol 71: 127–147.

9. HardyCD, CozzarelliNR (2005) A genetic selection for supercoiling mutants of Escherichia coli reveals proteins implicated in chromosome structure. Mol Microbiol 57: 1636–1652.

10. LuijsterburgMS, NoomMC, WuiteGJ, DameRT (2006) The architectural role of nucleoid-associated proteins in the organization of bacterial chromatin: a molecular perspective. J Struct Biol 156: 262–272.

11. WitzG, StasiakA (2010) DNA supercoiling and its role in DNA decatenation and unknotting. Nucleic Acids Res 38: 2119–2133.

12. CrozatE, WinkworthC, GaffeJ, HallinPF, RileyMA, et al. (2010) Parallel genetic and phenotypic evolution of DNA superhelicity in experimental populations of Escherichia coli. Mol Biol Evol 27: 2113–2128.

13. Chaconas G, Harshey RM (2002) Transposition of phage Mu DNA; Craig NL, Craigie R, Gellert M, Lambowitz AM, editors. Washington DC: ASM Press. 384–402 p.

14. MannaD, BreierAM, HigginsNP (2004) Microarray analysis of transposition targets in Escherichia coli: the impact of transcription. Proc Natl Acad Sci U S A 101: 9780–9785.

15. GeJ, LouZ, CuiH, ShangL, HarsheyRM (2011) Analysis of phage Mu DNA transposition by whole-genome Escherichia coli tiling arrays reveals a complex relationship to distribution of target selection protein B, transcription and chromosome architectural elements. J Biosci 36: 587–601.

16. HarsheyRM, JayaramM (2006) The Mu transpososome through a topological lens. Crit Rev Biochem Mol Biol 41: 387–405.

17. SokolskyTD, BakerTA (2003) DNA gyrase requirements distinguish the alternate pathways of Mu transposition. Mol Microbiol 47: 397–409.

18. PatoML (1994) Central location of the Mu strong gyrase binding site is obligatory for optimal rates of replicative transposition. Proc Natl Acad Sci U S A 91: 7056–7060.

19. OramM, PatoML (2004) Mu-like prophage strong gyrase site sequences: analysis of properties required for promoting efficient Mu DNA replication. J Bacteriol 186: 4575–4584.

20. PatoML, BanerjeeM (1996) The Mu strong gyrase-binding site promotes efficient synapsis of the prophage termini. Mol Microbiol 22: 283–292.

21. PathaniaS, JayaramM, HarsheyRM (2002) Path of DNA within the Mu transpososome. Transposase interactions bridging two Mu ends and the enhancer trap five DNA supercoils. Cell 109: 425–436.

22. DekkerJ, RippeK, DekkerM, KlecknerN (2002) Capturing chromosome conformation. Science 295: 1306–1311.

23. WangW, LiGW, ChenC, XieXS, ZhuangX (2011) Chromosome organization by a nucleoid-associated protein in live bacteria. Science 333: 1445–1449.

24. HoessR, AbremskiK, SternbergN (1984) The nature of the interaction of the P1 recombinase Cre with the recombining site loxP. Cold Spring Harb Symp Quant Biol 49: 761–768.

25. Van Duyne GD (2002) A structural view of tyrosine recombinase site-specific recombination; Craig NL, Craigie R, Gellert M, Lambowitz AM, editors. Washington DC: ASM Press. 93–117 p.

26. AbremskiK, HoessR, SternbergN (1983) Studies on the properties of P1 site-specific recombination: evidence for topologically unlinked products following recombination. Cell 32: 1301–1311.

27. SteinRA, DengS, HigginsNP (2005) Measuring chromosome dynamics on different time scales using resolvases with varying half-lives. Mol Microbiol 56: 1049–1061.

28. PatoML, KarlokM, WallC, HigginsNP (1995) Characterization of Mu prophage lacking the central strong gyrase binding site: localization of the block in replication. J Bacteriol 177: 5937–5942.

29. PatoML (2004) Replication of Mu prophages lacking the central strong gyrase site. Res Microbiol 155: 553–558.

30. RovinskiyN, AgblekeAA, ChesnokovaO, PangZ, HigginsNP (2012) Rates of gyrase supercoiling and transcription elongation control supercoil density in a bacterial chromosome. PLoS Genet 8: e1002845.

31. de WitE, de LaatW (2012) A decade of 3C technologies: insights into nuclear organization. Genes Dev 26: 11–24.

32. UmbargerMA, ToroE, WrightMA, PorrecaGJ, BauD, et al. (2011) The three-dimensional architecture of a bacterial genome and its alteration by genetic perturbation. Mol Cell 44: 252–264.

33. Goosen N, van de Putte P (1987) Regulation of transcription. In: Symonds N, Toussaint A, Van de Putte P, Howe MM, editors. Phage Mu. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory. pp. 41–52.

34. GreeneEC, MizuuchiK (2002) Dynamics of a protein polymer: the assembly and disassembly pathways of the MuB transposition target complex. EMBO J 21: 1477–1486.

35. GoosenN, van HeuvelM, MoolenaarGF, van de PutteP (1984) Regulation of Mu transposition. II. The Escherichia coli HimD protein positively controls two repressor promoters and the early promoter of bacteriophage Mu. Gene 32: 419–426.

36. KrauseHM, HigginsNP (1986) Positive and negative regulation of the Mu operator by Mu repressor and Escherichia coli integration host factor. J Biol Chem 261: 3744–3752.

37. van RijnPA, GoosenN, van de PutteP (1988) Integration host factor of Escherichia coli regulates early- and repressor transcription of bacteriophage Mu by two different mechanisms. Nucleic Acids Res 16: 4595–4605.

38. HigginsNP, CollierDA, KilpatrickMW, KrauseHM (1989) Supercoiling and integration host factor change the DNA conformation and alter the flow of convergent transcription in phage Mu. J Biol Chem 264: 3035–3042.

39. KarambelkarS, SwapnaG, NagarajaV (2012) Silencing of toxic gene expression by Fis. Nucleic Acids Res 40: 4358–4367.

40. Azaro MA, Landy A, editors (2002) λ integrase and the λ Int family. Washington, D.C.: American Society for Microbiology. 118–148 p.

41. EspeliO, BoccardF (2006) Organization of the Escherichia coli chromosome into macrodomains and its possible functional implications. J Struct Biol 156: 304–310.

42. Reyes-LamotheR, WangX, SherrattD (2008) Escherichia coli and its chromosome. Trends Microbiol 16: 238–245.

43. HigginsNP, YangX, FuQ, RothJR (1996) Surveying a supercoil domain by using the gamma delta resolution system in Salmonella typhimurium. J Bacteriol 178: 2825–2835.

44. Garcia-RussellN, HarmonTG, LeTQ, AmaladasNH, MathewsonRD, et al. (2004) Unequal access of chromosomal regions to each other in Salmonella: probing chromosome structure with phage lambda integrase-mediated long-range rearrangements. Mol Microbiol 52: 329–344.

45. WatsonMA, BoocockMR, StarkWM (1996) Rate and selectively of synapsis of res recombination sites by Tn3 resolvase. J Mol Biol 257: 317–329.

46. NashHA, PollockTJ (1983) Site-specific recombination of bacteriophage lambda. The change in topological linking number associated with exchange of DNA strands. J Mol Biol 170: 19–38.

47. GeJ, LouZ, HarsheyRM (2010) Immunity of replicating Mu to self-integration: a novel mechanism employing MuB protein. Mobile DNA 1: 8.

48. CraigieR, MizuuchiM, MizuuchiK (1984) Site-specific recognition of the bacteriophage Mu ends by the Mu A protein. Cell 39: 387–394.

49. MorganGJ, HatfullGF, CasjensS, HendrixRW (2002) Bacteriophage Mu genome sequence: analysis and comparison with Mu-like prophages in Haemophilus, Neisseria and Deinococcus. J Mol Biol 317: 337–359.

50. TolstorukovMY, VirnikKM, AdhyaS, ZhurkinVB (2005) A-tract clusters may facilitate DNA packaging in bacterial nucleoid. Nucleic Acids Res 33: 3907–3918.

51. HarsheyRM, GetzoffED, BaldwinDL, MillerJL, ChaconasG (1985) Primary structure of phage Mu transposase: homology to Mu repressor. Proc Natl Acad Sci U S A 82: 7676–7680.

52. MizuuchiM, WeisbergRA, MizuuchiK (1986) DNA sequence of the control region of phage D108: the N-terminal amino acid sequences of repressor and transposase are similar both in phage D108 and in its relative, phage Mu. Nucleic Acids Res 14: 3813–3825.

53. GreeneEC, MizuuchiK (2004) Visualizing the assembly and disassembly mechanisms of the MuB transposition targeting complex. J Biol Chem 279: 16736–16743.

54. GeJ, HarsheyRM (2008) Congruence of in vivo and in vitro insertion patterns in hot E. coli gene targets of transposable element Mu: opposing roles of MuB in target capture and integration. J Mol Biol 380: 598–607.

55. ScheirerKE, HigginsNP (2001) Transcription induces a supercoil domain barrier in bacteriophage Mu. Biochimie 83: 155–159.

56. ChampionK, HigginsNP (2007) Growth rate toxicity phenotypes and homeostatic supercoil control differentiate Escherichia coli from Salmonella enterica serovar Typhimurium. J Bacteriol 189: 5839–5849.

57. Ali AzamT, IwataA, NishimuraA, UedaS, IshihamaA (1999) Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181: 6361–6370.

58. van DrunenCM, van ZuylenC, MientjesEJ, GoosenN, van de PutteP (1993) Inhibition of bacteriophage Mu transposition by Mu repressor and Fis. Mol Microbiol 10: 293–298.

59. BetermierM, PoquetI, AlazardR, ChandlerM (1993) Involvement of Escherichia coli FIS protein in maintenance of bacteriophage Mu lysogeny by the repressor: control of early transcription and inhibition of transposition. J Bacteriol 175: 3798–3811.

60. CraigieR, Arndt-JovinDJ, MizuuchiK (1985) A defined system for the DNA strand-transfer reaction at the initiation of bacteriophage Mu transposition: protein and DNA substrate requirements. Proc Natl Acad Sci U S A 82: 7570–7574.

61. LavoieBD, ChaconasG (1993) Site-specific HU binding in the Mu transpososome: conversion of a sequence-independent DNA-binding protein into a chemical nuclease. Genes Dev 7: 2510–2519.

62. HiranoT (2006) At the heart of the chromosome: SMC proteins in action. Nat Rev Mol Cell Biol 7: 311–322.

63. PathaniaS, JayaramM, HarsheyRM (2003) A unique right end-enhancer complex precedes synapsis of Mu ends: the enhancer is sequestered within the transpososome throughout transposition. EMBO J 22: 3725–3736.

64. CraigieR, MizuuchiK (1986) Role of DNA topology in Mu transposition: mechanism of sensing the relative orientation of two DNA segments. Cell 45: 793–800.

65. CasjensS (2003) Prophages and bacterial genomics: what have we learned so far? Mol Microbiol 49: 277–300.

66. CanchayaC, FournousG, BrussowH (2004) The impact of prophages on bacterial chromosomes. Mol Microbiol 53: 9–18.

67. DaviesMR, BroadbentSE, HarrisSR, ThomsonNR, van der WoudeMW (2013) Horizontally acquired glycosyltransferase operons drive Salmonellae lipopolysaccharide diversity. PLoS Genet 9: e1003568.

68. FrostLS, LeplaeR, SummersAO, ToussaintA (2005) Mobile genetic elements: the agents of open source evolution. Nature reviews Microbiology 3: 722–732.

69. LinL, BitnerR, EdlinG (1977) Increased reproductive fitness of Escherichia coli lambda lysogens. J Virol 21: 554–559.

70. BarondessJJ, BeckwithJ (1990) A bacterial virulence determinant encoded by lysogenic coliphage lambda. Nature 346: 871–874.

71. PaolozziL, GhelardiniP (1992) A case of lysogenic conversion: modification of cell phenotype by constitutive expression of the Mu gem operon. Res Microbiol 143: 237–243.

72. d'Adda di FagagnaF, WellerGR, DohertyAJ, JacksonSP (2003) The Gam protein of bacteriophage Mu is an orthologue of eukaryotic Ku. EMBO Rep 4: 47–52.

73. EdlinG, LinL, BitnerR (1977) Reproductive fitness of P1, P2, and Mu lysogens of Escherichia coli. J Virol 21: 560–564.

74. 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.

75. SawitzkeJA, ThomasonLC, CostantinoN, BubunenkoM, DattaS, et al. (2007) Recombineering: in vivo genetic engineering in E. coli, S. enterica, and beyond. Materials and Methods Enzymol 421: 171–199.

76. DattaS, CostantinoN, ZhouX, CourtDL (2008) Identification and analysis of recombineering functions from Gram-negative and Gram-positive bacteria and their phages. Proc Natl Acad Sci U S A 105: 1626–1631.

77. KolmseeT, HenggeR (2011) Rare codons play a positive role in the expression of the stationary phase sigma factor RpoS (sigma(S)) in Escherichia coli. RNA Biol 8: 913–921.

78. FilutowiczM, JonczykP (1983) The gyrB gene product functions in both initiation and chain polymerization of Escherichia coli chromosome replication: suppression of the initiation deficiency in gyrB-ts mutants by a class of rpoB mutations. Mol Gen Genet 191: 282–287.

79. LaineB, KmiecikD, SautiereP, BiserteG, Cohen-SolalM (1980) Complete amino-acid sequences of DNA-binding proteins HU-1 and HU-2 from Escherichia coli. Eur J Biochem 103: 447–461.

80. FriedmanDI (1988) Integration host factor: a protein for all reasons. Cell 55: 545–554.

81. GiacaloneMJ, GentileAM, LovittBT, BerkleyNL, GundersonCW, et al. (2006) Toxic protein expression in Escherichia coli using a rhamnose-based tightly regulated and tunable promoter system. Biotechniques 40: 355–364.

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

83. HagegeH, KlousP, BraemC, SplinterE, DekkerJ, et al. (2007) Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nature protocols 2: 1722–1733.

84. GondorA, RougierC, OhlssonR (2008) High-resolution circular chromosome conformation capture assay. Nature protocols 3: 303–313.

85. MaCH, KachrooAH, MacieszakA, ChenTY, GugaP, et al. (2009) Reactions of Cre with methylphosphonate DNA: similarities and contrasts with Flp and vaccinia topoisomerase. PloS one 4: e7248.

86. Symonds N, Toussaint A, Van de Putte P, Howe MM (1987) Phage Mu. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.

87. KrauseHM, RothwellMR, HigginsNP (1983) The early promoter of bacteriophage Mu: definition of the site of transcript initiation. Nucleic Acids Res 11: 5483–5495.