1887

Abstract

Upon DNA damage, Sulfolobales exhibit a global gene regulatory response resulting in the expression of DNA transfer and repair proteins and the repression of the cell division machinery. Because the archaeal DNA damage response is still poorly understood, we investigated the promoters of the highly induced operon. Ups pili are involved in cellular aggregation and DNA exchange between cells. With LacS reporter gene assays we identified a conserved, non-palindromic hexanucleotide motif upstream of the core promoter elements to be essential for promoter activity. Substitution of this cis regulatory motif in the promoters resulted in abolishment of cellular aggregation and reduced DNA transfer. By screening the genome we identified a total of 214 genes harbouring the hexanucleotide motif in their respective promoter regions. Many of these genes were previously found to be regulated upon UV light treatment. Given the fact that the identified motif is conserved among and promoters, we speculate that a common regulatory mechanism is present in these two species in response to DNA-damaging conditions.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000455
2017-05-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/163/5/778.html?itemId=/content/journal/micro/10.1099/mic.0.000455&mimeType=html&fmt=ahah

References

  1. Soppa J. Transcription initiation in Archaea: facts, factors and future aspects. Mol Microbiol 1999; 31:1295–1305 [View Article][PubMed]
    [Google Scholar]
  2. Geiduschek EP, Ouhammouch M. Archaeal transcription and its regulators. Mol Microbiol 2005; 56:1397–1407 [View Article][PubMed]
    [Google Scholar]
  3. Grohmann D, Werner F. Recent advances in the understanding of archaeal transcription. Curr Opin Microbiol 2011; 14:328–334 [View Article][PubMed]
    [Google Scholar]
  4. Orell A, Peeters E, Vassen V, Jachlewski S, Schalles S et al. Lrs14 transcriptional regulators influence biofilm formation and cell motility of Crenarchaea. Isme J 2013; 7:1886–1898 [View Article][PubMed]
    [Google Scholar]
  5. Karr EA. Transcription regulation in the third domain. In Advances in Applied Microbiology, 1st ed. vol. 89 Elsevier Inc; 2014 pp. 101–133
    [Google Scholar]
  6. Peeters E, Charlier D. The Lrp family of transcription regulators in archaea. Archaea 2010; 2010:750457 [View Article][PubMed]
    [Google Scholar]
  7. Qureshi SA, Bell SD, Jackson SP. Factor requirements for transcription in the Archaeon Sulfolobus shibatae. Embo J 1997; 16:2927–2936 [View Article][PubMed]
    [Google Scholar]
  8. Bell SD, Jackson SP. The role of transcription factor B in transcription initiation and promoter clearance in the archaeon Sulfolobus acidocaldarius. J Biol Chem 2000; 275:12934–12940 [View Article][PubMed]
    [Google Scholar]
  9. Thomas MC, Chiang CM. The general transcription machinery and general cofactors. Crit Rev Biochem Mol Biol 2006; 41:105–178 [View Article][PubMed]
    [Google Scholar]
  10. Werner F, Weinzierl ROJ. Direct modulation of RNA polymerase core functions by basal transcription factors. Mol Cell Biol 2005; 25:8344–8355 [View Article][PubMed]
    [Google Scholar]
  11. Soppa J. Basal and regulated transcription in Archaea. Adv Appl Microbiol 2001; 50:171–217[PubMed] [CrossRef]
    [Google Scholar]
  12. Grove A. MarR family transcription factors. Curr Biol 2013; 23:R142–R143 [View Article][PubMed]
    [Google Scholar]
  13. Peeters E, Peixeiro N, Sezonov G. Cis-regulatory logic in archaeal transcription. Biochem Soc Trans 2013; 41:326–331 [View Article][PubMed]
    [Google Scholar]
  14. Bell SD, Cairns SS, Robson RL, Jackson SP. Transcriptional regulation of an archaeal operon in vivo and in vitro. Mol Cell 1999; 4:971–982 [View Article][PubMed]
    [Google Scholar]
  15. Dahlke I, Thomm M. A Pyrococcus homolog of the leucine-responsive regulatory protein, LrpA, inhibits transcription by abrogating RNA polymerase recruitment. Nucleic Acids Res 2002; 30:701–710 [View Article][PubMed]
    [Google Scholar]
  16. Lee SJ, Moulakakis C, Koning SM, Hausner W, Thomm M et al. TrmB, a sugar sensing regulator of ABC transporter genes in Pyrococcus furiosus exhibits dual promoter specificity and is controlled by different inducers. Mol Microbiol 2005; 57:1797–1807 [View Article][PubMed]
    [Google Scholar]
  17. Karr EA. The methanogen-specific transcription factor MsvR regulates the fpaA-rlp-rub oxidative stress operon adjacent to msvR in Methanothermobacter thermautotrophicus. J Bacteriol 2010; 192:5914–5922 [View Article][PubMed]
    [Google Scholar]
  18. Keese AM, Schut GJ, Ouhammouch M, Adams MWW, Thomm M. Genome-wide identification of targets for the archaeal heat shock regulator Phr by cell-free transcription of genomic DNA. J Bacteriol 2010; 192:1292–1298 [View Article][PubMed]
    [Google Scholar]
  19. Ouhammouch M, Dewhurst RE, Hausner W, Thomm M, Geiduschek EP. Activation of archaeal transcription by recruitment of the TATA-binding protein. Proc Natl Acad Sci USA 2003; 100:5097–5102 [View Article][PubMed]
    [Google Scholar]
  20. Ochs SM, Thumann S, Richau R, Weirauch MT, Lowe TM et al. Activation of archaeal transcription mediated by recruitment of transcription factor B. J Biol Chem 2012; 287:18863–18871 [View Article][PubMed]
    [Google Scholar]
  21. Kessler A, Sezonov G, Guijarro JI, Desnoues N, Rose T et al. A novel archaeal regulatory protein, Sta1, activates transcription from viral promoters. Nucleic Acids Res 2006; 34:4837–4845 [View Article][PubMed]
    [Google Scholar]
  22. Brouns SJJ, Walther J, Snijders APL, Van De Werken HJG, Willemen HL et al. Identification of the missing links in prokaryotic pentose oxidation pathways: evidence for enzyme recruitment. J Biol Chem 2006; 281:27378–27388 [View Article][PubMed]
    [Google Scholar]
  23. Lassak K, Peeters E, Wróbel S, Albers SV. The one-component system ArnR: a membrane-bound activator of the crenarchaeal archaellum. Mol Microbiol 2013; 88:125–139 [View Article][PubMed]
    [Google Scholar]
  24. Peeters E, Albers SV, Vassart A, Driessen AJM, Charlier D. Ss-LrpB, a transcriptional regulator from Sulfolobus solfataricus, regulates a gene cluster with a pyruvate ferredoxin oxidoreductase-encoding operon and permease genes. Mol Microbiol 2009; 71:972–988 [View Article][PubMed]
    [Google Scholar]
  25. Peng N, Xia Q, Chen Z, Liang YX, She Q. An upstream activation element exerting differential transcriptional activation on an archaeal promoter. Mol Microbiol 2009; 74:928–939 [View Article][PubMed]
    [Google Scholar]
  26. Van De Werken HJ, Verhees CH, Akerboom J, De Vos WM, Van Der Oost J. Identification of a glycolytic regulon in the archaea Pyrococcus and Thermococcus. FEMS Microbiol Lett 2006; 260:69–76 [View Article][PubMed]
    [Google Scholar]
  27. Peng N, Ao X, Liang YX, She Q. Archaeal promoter architecture and mechanism of gene activation. Biochem Soc Trans 2011; 39:99–103 [View Article][PubMed]
    [Google Scholar]
  28. Brock TD, Brock KM, Belly RT, Weiss RL. Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch Mikrobiol 1972; 84:54–68 [View Article][PubMed]
    [Google Scholar]
  29. Fröls S, Gordon PMK, Panlilio MA, Duggin IG, Bell SD et al. Response of the hyperthermophilic archaeon Sulfolobus solfataricus to UV damage. J Bacteriol 2007; 189:8708–8718 [View Article][PubMed]
    [Google Scholar]
  30. Götz D, Paytubi S, Munro S, Lundgren M, Bernander R et al. Responses of hyperthermophilic crenarchaea to UV irradiation. Genome Biol 2007; 8:R220 [View Article][PubMed]
    [Google Scholar]
  31. van Wolferen M, Wagner A, van der Does C, Albers SV. The archaeal Ced system imports DNA. Proc Natl Acad Sci USA 2016; 113:2496–2501 [View Article][PubMed]
    [Google Scholar]
  32. Ajon M, Fröls S, van Wolferen M, Stoecker K, Teichmann D et al. UV-inducible DNA exchange in hyperthermophilic archaea mediated by type IV pili. Mol Microbiol 2011; 82:807–817 [View Article][PubMed]
    [Google Scholar]
  33. Fröls S, Ajon M, Wagner M, Teichmann D, Zolghadr B et al. UV-inducible cellular aggregation of the hyperthermophilic archaeon Sulfolobus solfataricus is mediated by pili formation. Mol Microbiol 2008; 70:938–952 [View Article]
    [Google Scholar]
  34. van Wolferen M, Ajon M, Driessen AJM, Albers SV. Molecular analysis of the UV-inducible pili operon from Sulfolobus acidocaldarius. Microbiologyopen 2013; 2:928–937 [View Article][PubMed]
    [Google Scholar]
  35. Cohen O, Doron S, Wurtzel O, Dar D, Edelheit S et al. Comparative transcriptomics across the prokaryotic tree of life. Nucleic Acids Res 2016; 44:W46–W53 [View Article][PubMed]
    [Google Scholar]
  36. Berkner S, Wlodkowski A, Albers SV, Lipps G, Inducible LG. Inducible and constitutive promoters for genetic systems in Sulfolobus acidocaldarius. Extremophiles 2010; 14:249–259 [View Article][PubMed]
    [Google Scholar]
  37. Wagner M, van Wolferen M, Wagner A, Lassak K, Meyer BH et al. Versatile genetic tool box for the crenarchaeote Sulfolobus acidocaldarius. Front Microbiol 2012; 3:214 [View Article][PubMed]
    [Google Scholar]
  38. Wagner M, Wagner A, Ma X, Kort JC, Ghosh A et al. Investigation of the malE promoter and MalR, a positive regulator of the maltose regulon, for an improved expression system in Sulfolobus acidocaldarius. Appl Environ Microbiol 2014; 80:1072–1081 [View Article][PubMed]
    [Google Scholar]
  39. Lassak K, Neiner T, Ghosh A, Klingl A, Wirth R et al. Molecular analysis of the crenarchaeal flagellum. Mol Microbiol 2012; 83:110–124 [View Article][PubMed]
    [Google Scholar]
  40. Notredame C, Higgins DG, Heringa J. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 2000; 302:205–217 [View Article][PubMed]
    [Google Scholar]
  41. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004; 14:1188–1190 [View Article][PubMed]
    [Google Scholar]
  42. Jonuscheit M, Martusewitsch E, Stedman KM, Schleper C. A reporter gene system for the hyperthermophilic archaeon Sulfolobus solfataricus based on a selectable and integrative shuttle vector. Mol Microbiol 2003; 48:1241–1252 [View Article][PubMed]
    [Google Scholar]
  43. Anjum RS, Bray SM, Blackwood JK, Kilkenny ML, Coelho MA et al. Involvement of a eukaryotic-like ubiquitin-related modifier in the proteasome pathway of the archaeon Sulfolobus acidocaldarius. Nat Commun 2015; 6:8163 [View Article][PubMed]
    [Google Scholar]
  44. Zeng C, Zhao YZ, Cui CZ, Zhang H, Zhu JY et al. Characterization of the Haloarcula hispanica amyH gene promoter, an archaeal promoter that confers promoter activity in Escherichia coli. Gene 2009; 442:1–7 [View Article][PubMed]
    [Google Scholar]
  45. Aravind L, Anantharaman V, Balaji S, Babu MM, Iyer LM. The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol Rev 2005; 29:231–262 [View Article][PubMed]
    [Google Scholar]
  46. Guillière F, Peixeiro N, Kessler A, Raynal B, Desnoues N et al. Structure, function, and targets of the transcriptional regulator SvtR from the hyperthermophilic archaeal virus SIRV1. J Biol Chem 2009; 284:22222–22237 [View Article][PubMed]
    [Google Scholar]
  47. Bell SD, Kosa PL, Sigler PB, Jackson SP. Orientation of the transcription preinitiation complex in archaea. Proc Natl Acad Sci USA 1999; 96:13662–13667 [View Article][PubMed]
    [Google Scholar]
  48. Qureshi SA, Jackson SP. Sequence-specific DNA binding by the S. shibatae TFIIB homolog, TFB, and its effect on promoter strength. Mol Cell 1998; 1:389–400 [View Article][PubMed]
    [Google Scholar]
  49. Paytubi S, White MF. The crenarchaeal DNA damage-inducible transcription factor B paralogue TFB3 is a general activator of transcription. Mol Microbiol 2009; 72:1487–1499 [View Article][PubMed]
    [Google Scholar]
  50. Fröls S, Ajon M, Wagner M, Teichmann D, Zolghadr B et al. UV-inducible cellular aggregation of the hyperthermophilic archaeon Sulfolobus solfataricus is mediated by pili formation. Mol Microbiol 2008; 70:938–952 [View Article][PubMed]
    [Google Scholar]
  51. Rzechorzek NJ, Blackwood JK, Bray SM, Maman JD, Pellegrini L et al. Structure of the hexameric HerA ATPase reveals a mechanism of translocation-coupled DNA-end processing in archaea. Nat Commun 2014; 5:5506 [View Article][PubMed]
    [Google Scholar]
  52. Robinson NP, Dionne I, Lundgren M, Marsh VL, Bernander R et al. Identification of two origins of replication in the single chromosome of the archaeon Sulfolobus solfataricus. Cell 2004; 116:25–38 [View Article]
    [Google Scholar]
  53. Grogan DW, Hansen JE. Molecular characteristics of spontaneous deletions in the hyperthermophilic archaeon Sulfolobus acidocaldarius. J Bacteriol 2003; 185:1266–1272 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000455
Loading
/content/journal/micro/10.1099/mic.0.000455
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error