Transcription termination controls prophage maintenance in Escherichia coli genomes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 35, 2013, Pages 14414-14419

  Menouni, Rachid ^a   Champ, Stéphanie ^a   Espinosa, Leon ^a   Boudvillain, Marc ^b,c   Ansaldi, Mireille ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b CENTRE DE BIOPHYSIQUE MOLÉCULAIRE   (France)

^c UNIVERSITÉ D'ORLÉANS   (France)

Author keywords

Bacteriophage; Transcriptional regulation; Transduction

Indexed keywords

BICOZAMYCIN; TRANSCRIPTION TERMINATION FACTOR RHO;

ARTICLE; BACTERIAL GENOME; CONTROLLED STUDY; DNA REPAIR; ESCHERICHIA COLI; GENE EXPRESSION; GENETIC ORGANIZATION; NONHUMAN; PRIORITY JOURNAL; PROKARYOTIC CELL; PROPHAGE; TRANSCRIPTION TERMINATION;

BACTERIOPHAGE; TRANSCRIPTIONAL REGULATION; TRANSDUCTION;

COLIPHAGES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE SILENCING; GENOME, BACTERIAL; LYSOGENY; PROPHAGES; REAL-TIME POLYMERASE CHAIN REACTION; RECOMBINATION, GENETIC; TERMINATOR REGIONS, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84883433978     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1303400110     Document Type: Article

References (49)

1. Brüssow H, Canchaya C, Hardt WD (2004) Phages and the evolution of bacterial pathogens: From genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68(3):560-602.
2. Touchon M, et al. (2009) Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5(1):e1000344.
3. Bobay L-M, Rocha EP, Touchon M(2012) The adaptation of temperate bacteriophages to their host genomes. Mol Biol Evol 30(4):737-751.
4. Bossi L, Fuentes JA, Mora G, Figueroa-Bossi N (2003) Prophage contribution to bacterial population dynamics. J Bacteriol 185(21):6467-6471.
5. Figueroa-Bossi N, Bossi L (1999) Inducible prophages contribute to Salmonella virulence in mice. Mol Microbiol 33(1):167-176.
6. Boyd EF, Almagro-Moreno S, Parent MA (2009) Genomic islands are dynamic, ancient integrative elements in bacterial evolution. Trends Microbiol 17(2):47-53.
7. Boyd EF (2012) Bacteriophage-encoded bacterial virulence factors and phage-pathogenicity island interactions. Adv Virus Res 82:91-118.
8. Roossinck MJ (2011) The good viruses: Viral mutualistic symbioses. Nat Rev Microbiol 9(2):99-108.
9. Edgar R, et al. (2008) Bacteriophage infection is targeted to cellular poles. Mol Microbiol 68(5):1107-1116.
10. McDaniel L, Paul JH (2005) Effect of nutrient addition and environmental factors on prophage induction in natural populations of marine synechococcus species. Appl Environ Microbiol 71(2):842-850.
11. Court DL, Oppenheim AB, Adhya SL (2007) A new look at bacteriophage lambda genetic networks. J Bacteriol 189(2):298-304.
12. Cardinale CJ, et al. (2008) Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli. Science 320(5878):935-938.
13. Baños RC, Aznar S, Madrid C, Juárez A (2011) Differential functional properties of chromosomal- and plasmid-encoded H-NS proteins. Res Microbiol 162(4):382-385.
14. Navarre WW, et al. (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313(5784):236-238.
15. Dorman CJ (2007) H-NS, the genome sentinel. Nat Rev Microbiol 5(2):157-161.
16. Peters JM, et al. (2012) Rho and NusG suppress pervasive antisense transcription in Escherichia coli. Genes Dev 26(23):2621-2633.
17. Lang B, et al. (2007) High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res 35(18): 6330-6337.
18. Fang FC, Rimsky S (2008) New insights into transcriptional regulation by H-NS. Curr Opin Microbiol 11(2):113-120.
19. Sullivan SL, Gottesman ME (1992) Requirement for E. coli NusG protein in factordependent transcription termination. Cell 68(5):989-994.
20. Boudvillain M, Nollmann M, Margeat E (2010) Keeping up to speed with the transcription termination factor Rho motor. Transcription 1(2):70-75.
21. Mooney RA, Schweimer K, Rösch P, Gottesman M, Landick R (2009) Two structurally independent domains of E. coli NusG create regulatory plasticity via distinct interactions with RNA polymerase and regulators. J Mol Biol 391(2):341-358.
22. Nash H (1996) Site-specific recombination: Integration, excision, resolution, and inversion of defined DNA segments. Escherichia coli and Salmonella: Cellular and Molecular Biology (Am Soc Microbiol, Washington), pp 2363-2376.
23. Lewis JA, Hatfull GF (2001) Control of directionality in integrase-mediated recombination: Examination of recombination directionality factors (RDFs) including Xis and Cox proteins. Nucleic Acids Res 29(11):2205-2216.
24. Panis G, et al. (2010) Tight regulation of the intS gene of the KplE1 prophage: A new paradigm for integrase gene regulation. PLoS Genet 6(10):e1001149.
25. Campbell AM (1986) Bacteriophage lambda as a model system. Bioessays 5(6): 277-280.
26. Dhillon TS, Poon AP, Chan D, Clark AJ (1998) General transducing phages like Salmonella phage P22 isolated using a smooth strain of Escherichia coli as host. FEMS Microbiol Lett 161(1):129-133.
27. Clark AJ, Inwood W, Cloutier T, Dhillon TS (2001) Nucleotide sequence of coliphage HK620 and the evolution of lambdoid phages. J Mol Biol 311(4):657-679.
28. Panis G, Méjean V, Ansaldi M (2007) Control and regulation of KplE1 prophage sitespecific recombination: A new recombination module analyzed. J Biol Chem 282(30): 21798-21809.
29. Panis G, Duverger Y, Champ S, Ansaldi M (2010) Protein binding sites involved in the assembly of the KplE1 prophage intasome. Virology 404(1):41-50.
30. Wang X, et al. (2010) Cryptic prophages help bacteria cope with adverse environments. Nat Commun 1:147.
31. Burmann BM, et al. (2010) A NusE:NusG complex links transcription and translation. Science 328(5977):501-504.
32. Hart CM, Roberts JW (1991) Rho-dependent transcription termination. Characterization of the requirement for cytidine in the nascent transcript. J Biol Chem 266(35): 24140-24148.
33. Adhya S, Gottesman M (1982) Promoter occlusion: Transcription through a promoter may inhibit its activity. Cell 29(3):939-944.
34. Das A, Court D, Adhya S (1976) Isolation and characterization of conditional lethal mutants of Escherichia coli defective in transcription termination factor rho. Proc Natl Acad Sci USA 73(6):1959-1963.
35. Elantak L, Ansaldi M, Guerlesquin F, Méjean V, Morelli X (2005) Structural and genetic analyses reveal a key role in prophage excision for the TorI response regulator inhibitor. J Biol Chem 280(44):36802-36808.
36. Friedman DI, Court DL (2006) Regulation of lambda gene expression by transcription termination and antitermination. The Bacteriophages, ed Calendar R (Oxford Univ Press, New York), 2nd Ed, pp 83-103.
37. Roberts JW, et al. (1998) Antitermination by bacteriophage lambda Q protein. Cold Spring Harb Symp Quant Biol 63:319-325.
38. Washburn RS, Gottesman ME (2011) Transcription termination maintains chromosome integrity. Proc Natl Acad Sci USA 108(2):792-797.
39. Norman A, Hestbjerg Hansen L, Sørensen SJ (2005) Construction of a ColD cda promoter-based SOS-green fluorescent protein whole-cell biosensor with higher sensitivity toward genotoxic compounds than constructs based on recA, umuDC, or sulA promoters. Appl Environ Microbiol 71(5):2338-2346.
40. Lemire S, Figueroa-Bossi N, Bossi L (2011) Bacteriophage crosstalk: Coordination of prophage induction by trans-acting antirepressors. PLoS Genet 7(6):e1002149.
41. Lew K, Casjens S (1975) Identification of early proteins coded by bacteriophage P22. Virology 68(2):525-533.
42. Tao L, Wu X, Sun B (2010) Alternative σ factor sigmaH modulates prophage integration and excision in Staphylococcus aureus. PLoS Pathog 6(5):e1000888.
43. Hong SH, Wang X, Wood TK (2010) Controlling biofilm formation, prophage excision and cell death by rewiring global regulator H-NS of Escherichia coli. Microb Biotechnol 3(3):344-356.
44. Champ S, et al. (2011) Chaperone-assisted excisive recombination, a solitary role for DnaJ (Hsp40) chaperone in lysogeny escape. J Biol Chem 286(45):38876-38885.
45. Maamar H, Raj A, Dubnau D (2007) Noise in gene expression determines cell fate in Bacillus subtilis. Science 317(5837):526-529.
46. So L-H, et al. (2011) General properties of transcriptional time series in Escherichia coli. Nat Genet 43(6):554-560.
47. Rabhi M, et al. (2011) The Sm-like RNA chaperone Hfq mediates transcription antitermination at Rho-dependent terminators. EMBO J 30(14):2805-2816.
48. Bossi L, Schwartz A, Guillemardet B, Boudvillain M, Figueroa-Bossi N (2012) A role for Rho-dependent polarity in gene regulation by a noncoding small RNA. Genes Dev 26(16):1864-1873.
49. Feklistov A, et al. (2008) Rifamycins do not function by allosteric modulation of binding of Mg2+ to the RNA polymerase active center. Proc Natl Acad Sci USA 105(39):14820-14825.