Silencing of DNase Colicin E8 Gene Expression by a Complex Nucleoprotein Assembly Ensures Timely Colicin Induction

English version České info

Colicins are considered model proteins for studying bacterial toxins. These narrow spectrum antibiotics can kill by a variety of mechanisms, e.g. by forming pores in the membranes of susceptible cells or by degrading their nucleic acids. Colicin genes are plasmid-encoded and repressed by the master regulator of the DNA damage response, LexA. Induction of several pore-forming colicin genes is also repressed by IscR, which ensures that colicin genes are switched on as a last resort in DNA damaged cells, when nutrients are depleted. Here we show that nuclease colicin genes are not controlled by IscR but that the AsnC protein, in concert with LexA, is directly responsible for uncoupling the immediate expression of the DNase colicin E8 from the main induction of the SOS response. AsnC wraps the DNA of the colicin E8 promoter into a complex nucleoprotein assembly and the architecture of this complex is altered by the presence of the amino acid L-asparagine. Thus, repression by metabolite-responsive and DNA-damage responsive regulators operates at the regulatory regions of different colicins. Hence, the response to several environmental signals have been integrated to ensure that, following DNA damage, colicin synthesis is tightly repressed and induced only in terminally damaged cells.

Vyšlo v časopise: Silencing of DNase Colicin E8 Gene Expression by a Complex Nucleoprotein Assembly Ensures Timely Colicin Induction. PLoS Genet 11(6): e32767. doi:10.1371/journal.pgen.1005354
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005354

Souhrn

Zdroje

1. Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, Postle K, et al. Colicin biology. Microbiol Mol Biol Rev. 2007;71: 158–229. 17347522

2. Mader A, von Bronk B, Ewald B, Kesel S, Schnetz K, Frey E, et al. Amount of Colicin Release in Escherichia coli Is Regulated by Lysis Gene Expression of the Colicin E2 Operon. PLoS One. 2015;10: e0119124. doi: 10.1371/journal.pone.0119124 25751274

3. Lloubes R, Bernadac A, Houot L, Pommier S. Non classical secretion systems. Res Microbiol. 2013;164: 655–663. doi: 10.1016/j.resmic.2013.03.015 23542424

4. Walker D, Rolfe M, Thompson A, Moore GR, James R, Hinton JCD, et al. Transcriptional profiling of colicin-induced cell death of Escherichia coli MG1655 identifies potential mechanisms by which bacteriocins promote bacterial diversity. J Bacteriol. 2004;186: 866–869. 14729715

5. Czaran TL, Hoekstra RF, Pagie L. Chemical warfare between microbes promotes biodiversity. Proc Natl Acad Sci U S A. 2003;99: 786–790.

6. Majeed H, Gillor O, Kerr B, Riley MA. Competitive interactions in Escherichia coli populations: the role of bacteriocins. ISME J. 2011;5: 71–81. doi: 10.1038/ismej.2010.90 20664553

7. Kirkup BC, Riley MA. Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo. Nature. 2004;428: 412–414. 15042087

8. Cornforth DM, Foster KR. Competition sensing: the social side of bacterial stress responses. Nat Rev Microbiol. 2013;11: 285–293. doi: 10.1038/nrmicro2977 23456045

9. Butala M, Žgur-Bertok D, Busby SJ. The bacterial LexA transcriptional repressor. Cell Mol Life Sci. 2009;66: 82–93. doi: 10.1007/s00018-008-8378-6 18726173

10. Salles B, Weisemann JM, Weinstock GM. Temporal control of colicin E1 induction. J Bacteriol. 1987;169: 5028–5034. 3117771

11. Butala M, Sonjak S, Kamenšek S, Hodošček M, Browning DF, Žgur-Bertok D, et al. Double locking of an Escherichia coli promoter by two repressors prevents premature colicin expression and cell lysis. Mol Microbiol. 2012;86: 129–139. doi: 10.1111/j.1365-2958.2012.08179.x 22812562

12. Perez-Rueda E, Collado-Vides J. Common history at the origin of the position-function correlation in transcriptional regulators in archaea and bacteria. J Mol Evol. 2001;53: 172–179. 11523004

13. Thaw P, Sedelnikova SE, Muranova T, Wiese S, Ayora S, Alonso JC, et al. Structural insight into gene transcriptional regulation and effector binding by the Lrp/AsnC family. Nucleic Acids Res. 2006;34: 1439–1449. 16528101

14. Kolling R, Lother H. AsnC: an autogenously regulated activator of asparagine synthetase A transcription in Escherichia coli. J Bacteriol. 1985;164: 310–315. 2864330

15. Poggio S, Domeinzain C, Osorio A, Camarena L. The nitrogen assimilation control (Nac) protein represses asnC and asnA transcription in Escherichia coli. FEMS Microbiol Lett. 2002;206: 151–156. 11814655

16. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol. 2006;2: 2006 0008.

17. Lim CJ, Whang YR, Kenney LJ, Yan J. Gene silencing H-NS paralogue StpA forms a rigid protein filament along DNA that blocks DNA accessibility. Nucleic Acids Res. 2012;40: 3316–3328. doi: 10.1093/nar/gkr1247 22187157

18. Mayer O, Rajkowitsch L, Lorenz C, Konrat R, Schroeder R. RNA chaperone activity and RNA-binding properties of the E. coli protein StpA. Nucleic Acids Res. 2007;35: 1257–1269. 17267410

19. Shiraishi K, Ogata Y, Hanada K, Kano Y, Ikeda H. Roles of the DNA binding proteins H-NS and StpA in homologous recombination and repair of bleomycin-induced damage in Escherichia coli. Genes Genet Syst. 2007;82: 433–439. 17991999

20. Wolf T, Janzen W, Blum C, Schnetz K. Differential dependence of StpA on H-NS in autoregulation of stpA and in regulation of bgl. J Bacteriol. 2006;188: 6728–6738. 16980475

21. Craig ML, Suh WC, Record MT Jr. HO. and DNase I probing of E sigma 70 RNA polymerase—lambda PR promoter open complexes: Mg2+ binding and its structural consequences at the transcription start site. Biochemistry. 1995;34: 15624–15632. 7495790

22. Lee DJ, Minchin SD, Busby SJ. Activating transcription in bacteria. Annu Rev Microbiol. 2012;66: 125–152. doi: 10.1146/annurev-micro-092611-150012 22726217

23. Brinkman AB, Ettema TJ, de Vos WM, van der Oost J. The Lrp family of transcriptional regulators. Mol Microbiol. 2003;48: 287–294. 12675791

24. Ren J, Sainsbury S, Combs SE, Capper RG, Jordan PW, Berrow NS, et al. The structure and transcriptional analysis of a global regulator from Neisseria meningitidis. J Biol Chem. 2007;282: 14655–14664. 17374605

25. Hol FJ, Voges MJ, Dekker C, Keymer JE. Nutrient-responsive regulation determines biodiversity in a colicin-mediated bacterial community. BMC Biol. 2014;12: 68. doi: 10.1186/s12915-014-0068-2 25159553

26. Schwartz CJ, Giel JL, Patschkowski T, Luther C, Ruzicka FJ, Beinert H, et al. IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins. Proc Natl Acad Sci U S A. 2001;98: 14895–14900. 11742080

27. Wu Y, Outten FW. IscR controls iron-dependent biofilm formation in Escherichia coli by regulating type I fimbria expression. J Bacteriol. 2009;191: 1248–1257. doi: 10.1128/JB.01086-08 19074392

28. Pugsley AP. The ins and outs of colicins. Part I: Production, and translocation across membranes. Microbiol Sci. 1984;1: 168–175. 6444117

29. Butala M, Klose D, Hodnik V, Rems A, Podlesek Z, Klare JP, et al. Interconversion between bound and free conformations of LexA orchestrates the bacterial SOS response. Nucleic Acids Res. 2011;39: 6546–6557. doi: 10.1093/nar/gkr265 21576225

30. Lodge J, Fear J, Busby S, Gunasekaran P, Kamini NR. Broad host range plasmids carrying the Escherichia coli lactose and galactose operons. FEMS Microbiol Lett. 1992;74: 271–276. 1526459

31. Butala M, Busby SJ, Lee DJ. DNA sampling: a method for probing protein binding at specific loci on bacterial chromosomes. Nucleic Acids Res. 2009;37: e37. doi: 10.1093/nar/gkp043 19181705

32. Miller JH. Experiments in molecular genetics. 2nd ed. New York: Cold Spring Harbor Laboratory Press; 1972.

33. Sambrook J, Fritsch EF, Maniatis M.Molecular cloning: a laboratory manual. 2nd ed. New York: Cold Spring Harbor Laboratory Press; 1987.

34. Browning DF, Cole JA, Busby SJ. Regulation by nucleoid-associated proteins at the Escherichia coli nir operon promoter. J Bacteriol. 2008;190: 7258–7267. doi: 10.1128/JB.01015-08 18757534

35. Squire DJ, Xu M, Cole JA, Busby SJ, Browning DF. Competition between NarL-dependent activation and Fis-dependent repression controls expression from the Escherichia coli yeaR and ogt promoters. Biochem J. 2009;420: 249–257. doi: 10.1042/BJ20090183 19245365