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The interplay between nucleoid organization and transcription in archaeal genomes

Nature Reviews Microbiology volume 13, pages 333341 (2015) | Download Citation

Abstract

The archaeal genome is organized by either eukaryotic-like histone proteins or bacterial-like nucleoid-associated proteins. Recent studies have revealed novel insights into chromatin dynamics and their effect on gene expression in archaeal model organisms. In this Progress article, we discuss the interplay between chromatin proteins, such as histones and Alba, and components of the basal transcription machinery, as well as between chromatin structure and gene-specific transcription factors in archaea. Such an interplay suggests that chromatin might have a role in regulating gene expression on both a global and a gene-specific level. Moreover, several archaeal transcription factors combine a global gene regulatory role with an architectural role, thus contributing to chromatin organization and compaction, as well as gene expression. We describe the emerging principles underlying how these factors cooperate in nucleoid structuring and gene regulation.

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References

  1. 1.

    , , , & Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251–260 (1997).

  2. 2.

    & Transcription factories: genome organization and gene regulation. Chem. Rev. 113, 8683–8705 (2013).

  3. 3.

    , , & Genomic looping: a key principle of chromatin organization J. Mol. Microbiol. Biotechnol. 24, 344–359 (2014).

  4. 4.

    & CTCF and cohesin: linking gene regulatory elements with their targets. Cell 152, 1285–1297 (2013).

  5. 5.

    & Genome architecture: domain organization of interphase chromosomes. Cell 152, 1270–1284 (2013).

  6. 6.

    The role of co-transcriptional translation and protein translocation (transertion) in bacterial chromosome segregation. Mol. Microbiol. 45, 17–29 (2002).

  7. 7.

    & Regulation of chromatin by histone modifications. Cell Res. 21, 381–395 (2011).

  8. 8.

    , , & ATP-dependent chromatin-remodeling complexes. Mol. Cell. Biol. 20, 1899–1910 (2000).

  9. 9.

    , & Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154, 490–503 (2013).

  10. 10.

    , , , & Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol. 181, 6361–6370 (1999).

  11. 11.

    The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin. Mol. Microbiol. 56, 858–870 (2005).

  12. 12.

    & Nucleoid-associated proteins in Crenarchaea. Biochem. Soc. Trans. 39, 116–121 (2011).

  13. 13.

    & Recent advances in the understanding of archaeal transcription. Curr. Opin. Microbiol. 14, 328–334 (2011).

  14. 14.

    & DNA-binding proteins and evolution of transcription regulation in the archaea. Nucleic Acids Res. 27, 4658–4670 (1999).

  15. 15.

    , , , & The interaction of Alba, a conserved archaeal chromatin protein, with Sir2 and its regulation by acetylation. Science 296, 148–151 (2002).

  16. 16.

    , & The two faces of Alba: the evolutionary connection between proteins participating in chromatin structure and RNA metabolism. Genome Biol. 4, R64 (2003).

  17. 17.

    , & Sir2 and the acetyltransferase, Pat, regulate the archaeal chromatin protein, Alba. J. Biol. Chem. 280, 21122–21128 (2005).

  18. 18.

    , & Ssh10b, a conserved thermophilic archaeal protein, binds RNA in vivo. Mol. Microbiol. 50, 1605–1615 (2003).

  19. 19.

    et al. The Sac10b homolog in Methanococcus maripaludis binds DNA at specific sites. J. Bacteriol. 191, 2315–2329 (2009).

  20. 20.

    , , , & An abundant DNA binding protein from the hyperthermophilic archaeon Sulfolobus shibatae affects DNA supercoiling in a temperature-dependent fashion. J. Bacteriol. 182, 3929–3933 (2000).

  21. 21.

    , , , & Electron microscopic study of DNA complexes with proteins from the Archaebacterium Sulfolobus acidocaldarius. EMBO J. 5, 3715–3721 (1986).

  22. 22.

    et al. Obligate heterodimerization of the archaeal Alba2 protein with Alba1 provides a mechanism for control of DNA packaging. Structure 13, 963–971 (2005).

  23. 23.

    et al. Alba shapes the archaeal genome using a delicate balance of bridging and stiffening the DNA. Nature Commun. 3, 1328 (2012).

  24. 24.

    , & Crystal structure of archaeal chromatin protein Alba2-double-stranded DNA complex from Aeropyrum pernix K1. J. Biol. Chem. 287, 10394–10402 (2012).

  25. 25.

    & Archaeal histones and the origin of the histone fold. Curr. Opin. Microbiol. 9, 520–525 (2006).

  26. 26.

    , , & Archaeal nucleosomes. Proc. Natl Acad. Sci. USA 94, 12633–12637 (1997).

  27. 27.

    et al. Archaeal histones: structures, stability and DNA binding. Biochem. Soc. Trans. 32, 227–230 (2004).

  28. 28.

    et al. Archaeal nucleosome positioning in vivo and in vitro is directed by primary sequence motifs. BMC Genomics 14, 391 (2013).

  29. 29.

    et al. An alternative beads-on-a-string chromatin architecture in Thermococcus kodakarensis. EMBO Rep. 14, 711–717 (2013).

  30. 30.

    et al. Histone and TK0471/TrmBL2 form a novel heterogeneous genome architecture in the hyperthermophilic archaeon Thermococcus kodakarensis. Mol. Biol. Cell 22, 386–398 (2011).

  31. 31.

    , & Negative constrained DNA supercoiling in archaeal nucleosomes. Mol. Microbiol. 35, 341–349 (2000).

  32. 32.

    , , , & Identification, cloning and characterization of a new DNA-binding protein from the hyperthermophilic methanogen Methanopyrus kandleri. Nucleic Acids Res. 30, 685–694 (2002).

  33. 33.

    , , & The archaeal histone-fold protein HMf organizes DNA into bona fide chromatin fibers. Structure 9, 1201–1211 (2001).

  34. 34.

    et al. Chromatin is an ancient innovation conserved between Archaea and Eukarya. eLife 1, e00078 (2012).

  35. 35.

    & Transcription by an archaeal RNA polymerase is slowed but not blocked by an archaeal nucleosome. J. Bacteriol. 186, 3492–3498 (2004).

  36. 36.

    , , , & HMf, a DNA-binding protein isolated from the hyperthermophilic archaeon Methanothermus fervidus, is most closely related to histones. Proc. Natl Acad. Sci. USA 87, 5788–5791 (1990).

  37. 37.

    et al. A genomic code for nucleosome positioning. Nature 442, 772–778 (2006).

  38. 38.

    et al. A single-base resolution map of an archaeal transcriptome. Genome Res. 20, 133–141 (2010).

  39. 39.

    et al. Biochemical and structural characterization of Cren7, a novel chromatin protein conserved among Crenarchaea. Nucleic Acids Res. 36, 1129–1137 (2008).

  40. 40.

    , , & Small abundant DNA binding proteins from the thermoacidophilic archaeon Sulfolobus shibatae constrain negative DNA supercoils. J. Bacteriol. 180, 2560–2563 (1998).

  41. 41.

    et al. The hyperthermophile protein Sso10a is a dimer of winged helix DNA-binding domains linked by an antiparallel coiled coil rod. J. Mol. Biol. 341, 73–91 (2004).

  42. 42.

    & The DNA-recognition fold of Sso7c4 suggests a new member of SpoVT–AbrB superfamily from archaea. Nucleic Acids Res. 39, 6764–6774 (2011).

  43. 43.

    & Biochemical characterization of DNA-binding proteins from Pyrobaculum aerophilum and Aeropyrum pernix. Extremophiles 12, 235–246 (2008).

  44. 44.

    et al. CC1, a novel crenarchaeal DNA binding protein. J. Bacteriol. 189, 403–409 (2007).

  45. 45.

    , & Transcriptional activation in the context of repression mediated by archaeal histones. Proc. Natl Acad. Sci. USA 107, 6777–6781 (2010).

  46. 46.

    et al. The initiation factor TFE and the elongation factor Spt4/5 compete for the RNAP clamp during transcription initiation and elongation. Mol. Cell 43, 263–274 (2011).

  47. 47.

    & Transcriptional fidelity and proofreading in Archaea and implications for the mechanism of TFS-induced RNA cleavage. Mol. Microbiol. 52, 1133–1143 (2004).

  48. 48.

    , & Transcription factor S, a cleavage induction factor of the archaeal RNA polymerase. J. Biol. Chem. 275, 12393–12399 (2000).

  49. 49.

    et al. Spt4/5 stimulates transcription elongation through the RNA polymerase clamp coiled-coil motif. Nucleic Acids Res. 38, 4040–4051 (2010).

  50. 50.

    , , & Architecture of the RNA polymerase-Spt4/5 complex and basis of universal transcription processivity. EMBO J. 30, 1302–1310 (2011).

  51. 51.

    A nexus for gene expression-molecular mechanisms of Spt5 and NusG in the three domains of life. J. Mol. Biol. 417, 13–27 (2012).

  52. 52.

    , , & Mutational analysis of genes encoding chromatin proteins in the archaeon Methanococcus voltae indicates their involvement in the regulation of gene expression. Mol. Genet. Genom. 272, 76–87 (2004).

  53. 53.

    et al. An archaeal histone is required for transformation of Thermococcus kodakarensis. J. Bacteriol. 194, 6864–6874 (2012).

  54. 54.

    , , & Archaeal histone tetramerization determines DNA affinity and the direction of DNA supercoiling. J. Biol. Chem. 277, 30879–30886 (2002).

  55. 55.

    , & Growth phase-dependent expression and degradation of histones in the thermophilic archaeon Thermococcus zilligii. Mol. Microbiol. 36, 876–885 (2000).

  56. 56.

    , , , & Growth-phase-dependent synthesis of histones in the archaeon Methanothermus fervidus. Proc. Natl Acad. Sci. USA 91, 12624–12628 (1994).

  57. 57.

    & Chromatin disruption and modification. Nucleic Acids Res. 27, 711–720 (1999).

  58. 58.

    Histone acetylation in chromatin structure and transcription. Nature 389, 349–352 (1997).

  59. 59.

    et al. Targeted analysis and discovery of posttranslational modifications in proteins from methanogenic archaea by top-down MS. Proc. Natl Acad. Sci. USA 101, 2678–2683 (2004).

  60. 60.

    & Nuclear functions of prefoldin. Open Biol. 4, 140085 (2014).

  61. 61.

    et al. The prefoldin complex regulates chromatin dynamics during transcription elongation. PLoS Genet. 9, e1003776 (2013).

  62. 62.

    et al. The yeast prefoldin-like URI-orthologue Bud27 associates with the RSC nucleosome remodeler and modulates transcription. Nucleic Acids Res. 42, 9666–9676 (2014).

  63. 63.

    & The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73, 417–435 (2004).

  64. 64.

    , & Structure of a Sir2 substrate, Alba, reveals a mechanism for deacetylation-induced enhancement of DNA binding. J. Biol. Chem. 278, 26071–26077 (2003).

  65. 65.

    , , & Nucleosome organization in the vicinity of transcription factor binding sites in the human genome. BMC Genomics 15, 493 (2014).

  66. 66.

    & Nucleosome free regions in yeast promoters result from competitive binding of transcription factors that interact with chromatin modifiers. PLoS Comput. Biol. 9, e1003181 (2013).

  67. 67.

    , , , & Activation of archaeal transcription by recruitment of the TATA-binding protein. Proc. Natl Acad. Sci. USA 100, 5097–5102 (2003).

  68. 68.

    & A thermostable platform for transcriptional regulation: the DNA-binding properties of two Lrp homologs from the hyperthermophilic archaeon Methanococcus jannaschii. EMBO J. 20, 146–156 (2001).

  69. 69.

    & The Lrp family of transcription regulators in archaea. Archaea 2010, 750457 (2010).

  70. 70.

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

  71. 71.

    & Leucine-responsive regulatory protein: a global regulator of gene expression in E. coli. Annu. Rev. Microbiol. 49, 747–775 (1995).

  72. 72.

    , , , & Ss-LrpB, a transcriptional regulator from Sulfolobus solfataricus, regulates a gene cluster with a pyruvate ferredoxin oxidoreductase-encoding operon and permease genes. Mol. Microbiol. 71, 972–988 (2009).

  73. 73.

    et al. Transcriptional control by two leucine-responsive regulatory proteins in Halobacterium salinarum R1. BMC Mol. Biol. 11, 40 (2010).

  74. 74.

    et al. Feast/famine regulation by transcription factor FL11 for the survival of the hyperthermophilic archaeon Pyrococcus OT3. Structure 15, 1542–1554 (2007).

  75. 75.

    et al. Sa-Lrp from Sulfolobus acidocaldarius is a versatile, glutamine-responsive, and architectural transcriptional regulator. Microbiologyopen 2, 75–93 (2013).

  76. 76.

    , , , & A novel member of the bacterial-archaeal regulator family is a nonspecific DNA-binding protein and induces positive supercoiling. J. Biol. Chem. 276, 10745–10752 (2001).

  77. 77.

    , , & Transcriptional regulation of the gene encoding an alcohol dehydrogenase in the archaeon Sulfolobus solfataricus involves multiple factors and control elements. J. Bacteriol. 185, 3926–3934 (2003).

  78. 78.

    et al. A novel archaeal regulatory protein, Sta1, activates transcription from viral promoters. Nucleic Acids Res. 34, 4837–4845 (2006).

  79. 79.

    et al. Lrs14 transcriptional regulators influence biofilm formation and cell motility of Crenarchaea. ISME J. 7, 1886–1898 (2013).

  80. 80.

    , , , & The role of TrmB and TrmB-like transcriptional regulators for sugar transport and metabolism in the hyperthermophilic archaeon Pyrococcus furiosus. Arch. Microbiol. 190, 247–256 (2008).

  81. 81.

    , , & Lysine methylation mapping of crenarchaeal DNA-directed RNA polymerases by collision-induced and electron-transfer dissociation mass spectrometry. J. Proteome Res. 13, 2637–2648 (2014).

  82. 82.

    , , & Extensive lysine methylation in hyperthermophilic crenarchaea: potential implications for protein stability and recombinant enzymes. Archaea 2010, 106341 (2010).

  83. 83.

    et al. A prototypic lysine methyltransferase 4 from archaea with degenerate sequence specificity methylates chromatin proteins Sul7d and Cren7 in different patterns. J. Biol. Chem. 288, 13728–13740 (2013).

  84. 84.

    et al. Archaeal signal transduction: impact of protein phosphatase deletions on cell size, motility, and energy metabolism in Sulfolobus acidocaldarius. Mol. Cell. Proteomics 12, 3908–3923 (2013).

  85. 85.

    et al. Regulation of archaella expression by the FHA and von Willebrand domain-containing proteins ArnA and ArnB in Sulfolobus acidocaldarius. Mol. Microbiol. 86, 24–36 (2012).

  86. 86.

    & Evolution of multisubunit RNA polymerases in the three domains of life. Nature Rev. Microbiol. 9, 85–98 (2011).

  87. 87.

    Structure and function of archaeal RNA polymerases. Mol. Microbiol. 65, 1395–1404 (2007).

  88. 88.

    & Direct modulation of RNA polymerase core functions by basal transcription factors. Mol. Cell. Biol. 25, 8344–8355 (2005).

  89. 89.

    , & Topography of the euryarchaeal transcription initiation complex. J. Biol. Chem. 279, 5894–5903 (2004).

  90. 90.

    , , & Transcription factor E is a part of transcription elongation complexes. J. Biol. Chem. 282, 35482–35490 (2007).

  91. 91.

    et al. The Sulfolobus initiator element is an important contributor to promoter strength. J. Bacteriol. 195, 5216–5222 (2013).

  92. 92.

    & Identification and genomic analysis of transcription factors in archaeal genomes exemplifies their functional architecture and evolutionary origin. Mol. Biol. Evol. 27, 1449–1459 (2010).

  93. 93.

    , & Genomic repertoires of DNA-binding transcription factors across the tree of life. Nucleic Acids Res. 38, 7364–7377 (2010).

  94. 94.

    , & Cis-regulatory logic in archaeal transcription. Biochem. Soc. Trans. 41, 326–331 (2013).

  95. 95.

    & Archaeal transcription and its regulators. Mol. Microbiol. 56, 1397–1407 (2005).

  96. 96.

    et al. Activation of archaeal transcription mediated by recruitment of transcription factor B. J. Biol. Chem. 287, 18863–18871 (2012).

  97. 97.

    & Pyrococcus homolog of the leucine-responsive regulatory protein, LrpA, inhibits transcription by abrogating RNA polymerase recruitment. Nucleic Acids Res. 30, 701–710 (2002).

  98. 98.

    et al. A global transcriptional regulator in Thermococcus kodakaraensis controls the expression levels of both glycolytic and gluconeogenic enzyme-encoding genes. J. Biol. Chem. 282, 33659–33670 (2007).

  99. 99.

    et al. SurR: a transcriptional activator and repressor controlling hydrogen and elemental sulphur metabolism in Pyrococcus furiosus. Mol. Microbiol. 71, 332–349 (2009).

  100. 100.

    , , , & Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

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Acknowledgements

Research in the laboratory of R.T.D. is supported by grants from the Netherlands Organization for Scientific Research (864.08.001), High Tech Systems & Materials NanoNextNL program 8B, the FOM Foundation for Fundamental Research on Matter program 'Crowd management: the physics of genome processing in complex environments' and the Human Frontier Science Program (RGP0014/2014). E.P. is supported by the Research Foundation Flanders (FWO-Vlaanderen) and by the Research Council of Vrije Universiteit Brussel.

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    • Eveline Peeters
    •  & Rosalie P. C. Driessen

    E.P. and R.P.C.D. contributed equally to this work.

Affiliations

  1. Research Group of Microbiology, Department of Bio-engineering Sciences, Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussels, Belgium.

    • Eveline Peeters
  2. Leiden Institute of Chemistry, Leiden University, Einsteinweg 55, 2333 CC Leiden, The Netherlands.

    • Rosalie P. C. Driessen
    •  & Remus T. Dame
  3. Institute for Structural and Molecular Biology, Division of Biosciences, University College London, Darwin Building, Gower Street, London WC1E 6BT, UK.

    • Finn Werner

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The authors declare no competing financial interests.

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Correspondence to Remus T. Dame.

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https://doi.org/10.1038/nrmicro3467

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