1932

Abstract

The H-NS (heat-stable nucleoid structuring) protein affects both nucleoid compaction and global gene regulation. H-NS appears to act primarily as a silencer of AT-rich genetic material acquired by horizontal gene transfer. As such, it is key in the regulation of most genes involved in virulence and in adaptation to new environmental niches. Here we review recent progress in understanding the biochemistry of H-NS and how xenogeneic silencing affects bacterial evolution. We highlight the strengths and weaknesses of some of the models proposed in H-NS-mediated nucleoprotein complex formation. Based on recent single-molecule studies, we also propose a novel mode of DNA compaction by H-NS termed intrabridging to explain over two decades of observations of the H-NS molecule.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-102215-095301
2016-09-08
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/70/1/annurev-micro-102215-095301.html?itemId=/content/journals/10.1146/annurev-micro-102215-095301&mimeType=html&fmt=ahah

Literature Cited

  1. Ali SS, Soo J, Rao C, Leung AS, Ngai DH-M. 1.  et al. 2014. Silencing by H-NS potentiated the evolution of Salmonella. PLOS Pathog. 10:e1004500 [Google Scholar]
  2. Ali SS, Whitney JC, Stevenson J, Robinson H, Howell PL, Navarre WW. 2.  2013. Structural insights into the regulation of foreign genes in Salmonella by the Hha/H-NS complex. J. Biol. Chem. 288:13356–69 [Google Scholar]
  3. Ali SS, Xia B, Liu J, Navarre WW. 3.  2012. Silencing of foreign DNA in bacteria. Curr. Opin. Microbiol. 15:175–81 [Google Scholar]
  4. Amit R, Oppenheim AB, Stavans J. 4.  2003. Increased bending rigidity of single DNA molecules by H-NS, a temperature and osmolarity sensor. Biophys. J. 84:2467–73 [Google Scholar]
  5. Arold ST, Leonard PG, Parkinson GN, Ladbury JE. 5.  2010. H-NS forms a superhelical protein scaffold for DNA condensation. PNAS 107:15728–32 [Google Scholar]
  6. Aznar S, Paytubi S, Juárez A. 6.  2013. The Hha protein facilitates incorporation of horizontally acquired DNA in enteric bacteria. Microbiology 159:545–54 [Google Scholar]
  7. Baños RC, Pons JI, Madrid C, Juárez A. 7.  2008. A global modulatory role for the Yersinia enterocolitica H-NS protein. Microbiology 154:1281–89 [Google Scholar]
  8. Baños RC, Vivero A, Aznar S, García J, Pons M. 8.  et al. 2009. Differential regulation of horizontally acquired and core genome genes by the bacterial modulator H-NS. PLOS Genet. 5:e1000513 [Google Scholar]
  9. Battesti A, Tsegaye YM, Packer DG, Majdalani N, Gottesman S. 9.  2012. H-NS regulation of IraD and IraM antiadaptors for control of RpoS degradation. J. Bacteriol. 194:2470–78 [Google Scholar]
  10. Baumann CG, Smith SB, Bloomfield VA, Bustamante C. 10.  1997. Ionic effects on the elasticity of single DNA molecules. PNAS 94:6185–90 [Google Scholar]
  11. Berger MF, Philippakis AA, Qureshi AM, He FS, Estep PW 3rd, Bulyk ML. 11.  2006. Compact, universal DNA microarrays to comprehensively determine transcription-factor binding site specificities. Nat. Biotechnol. 24:1429–35 [Google Scholar]
  12. Bickle TA. 12.  2004. Restricting restriction. Mol. Microbiol. 51:3–5 [Google Scholar]
  13. Bloch V, Yang Y, Margeat E, Chavanieu A, Auge MT. 13.  et al. 2003. The H-NS dimerization domain defines a new fold contributing to DNA recognition. Nat. Struct. Mol. Biol. 10:212–18 [Google Scholar]
  14. Boto L. 14.  2010. Horizontal gene transfer in evolution: facts and challenges. Proc. R. Soc. Lond. B 277:819–27 [Google Scholar]
  15. Bouffartigues E, Buckle M, Badaut C, Travers A, Rimsky S. 15.  2007. H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing. Nat. Struct. Mol. Biol. 14:441–48 [Google Scholar]
  16. Castang S, Dove SL. 16.  2010. High-order oligomerization is required for the function of the H-NS family member MvaT in Pseudomonas aeruginosa. Mol. Microbiol. 78:916–31 [Google Scholar]
  17. Castang S, Dove SL. 17.  2012. Basis for the essentiality of H-NS family members in Pseudomonas aeruginosa. J. Bacteriol. 194:5101–9 [Google Scholar]
  18. Castang S, McManus HR, Turner KH, Dove SL. 18.  2008. H-NS family members function coordinately in an opportunistic pathogen. PNAS 105:18947–52 [Google Scholar]
  19. Cathelyn JS, Ellison DW, Hinchliffe SJ, Wren BW, Miller VL. 19.  2007. The RovA regulons of Yersinia enterocolitica and Yersinia pestis are distinct: evidence that many RovA-regulated genes were acquired more recently than the core genome. Mol. Microbiol. 66:189–205 [Google Scholar]
  20. Chen JM, Ren H, Shaw JE, Wang YJ, Li M. 20.  et al. 2008. Lsr2 of Mycobacterium tuberculosis is a DNA-bridging protein. Nucleic Acids Res. 36:2123–35 [Google Scholar]
  21. Cohan FM, Koeppel AF. 21.  2008. The origins of ecological diversity in prokaryotes. Curr. Biol. 18:R1024–34 [Google Scholar]
  22. Coombes BK. 22.  2013. Regulatory evolution at the host-pathogen interface. Can. J. Microbiol. 59:365–67 [Google Scholar]
  23. Cordeiro TN, García J, Bernadó P, Millet O, Pons M. 23.  2015. A three-protein charge zipper stabilizes a complex modulating bacterial gene silencing. J. Biol. Chem. 290:21200–12 [Google Scholar]
  24. Cordeiro TN, Schmidt H, Madrid C, Juárez A, Bernadó P. 24.  et al. 2011. Indirect DNA readout by an H-NS related protein: structure of the DNA complex of the C-terminal domain of Ler. PLOS Pathog. 7:e1002380 [Google Scholar]
  25. Cui T, Leng F. 25.  2007. Specific recognition of AT-rich DNA sequences by the mammalian high mobility group protein AT-hook 2: a SELEX study. Biochemistry 46:13059–66 [Google Scholar]
  26. Dame RT, Luijsterburg MS, Krin E, Bertin PN, Wagner R, Wuite GJ. 26.  2005. DNA bridging: a property shared among H-NS-like proteins. J. Bacteriol. 187:1845–48 [Google Scholar]
  27. Dame RT, Wyman C, Goosen N. 27.  2000. H-NS mediated compaction of DNA visualised by atomic force microscopy. Nucleic Acids Res. 28:3504–10 [Google Scholar]
  28. Desai PT, Porwollik S, Long F, Cheng P, Wollam A. 28.  et al. 2013. Evolutionary genomics of Salmonella enterica subspecies. mBio 4:e00579–12 Erratum. 2013. mBio 4:e00198–13 [Google Scholar]
  29. Ding P, McFarland KA, Jin S, Tong G, Duan B. 29.  et al. 2015. A novel AT-rich DNA recognition mechanism for bacterial xenogeneic silencer MvaT. PLOS Pathog. 11:e1004967 [Google Scholar]
  30. Dorman CJ. 30.  2007. H-NS, the genome sentinel. Nat. Rev. Microbiol. 5:157–61 [Google Scholar]
  31. Dorman CJ. 31.  2014. H-NS-like nucleoid-associated proteins, mobile genetic elements and horizontal gene transfer in bacteria. Plasmid 75:1–11 [Google Scholar]
  32. Doyle M, Fookes M, Ivens A, Mangan MW, Wain J, Dorman CJ. 32.  2007. An H-NS-like stealth protein aids horizontal DNA transmission in bacteria. Science 315:251–52 [Google Scholar]
  33. Fani R, Fondi M. 33.  2009. Origin and evolution of metabolic pathways. Phys. Life Rev. 6:23–52 [Google Scholar]
  34. Farrell MJ, Finkel SE. 34.  2003. The growth advantage in stationary-phase phenotype conferred by rpoS mutations is dependent on the pH and nutrient environment. J. Bacteriol. 185:7044–52 [Google Scholar]
  35. Ferenci T. 35.  2003. What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli?. Trends Microbiol. 11:457–61 [Google Scholar]
  36. García J, Cordeiro TN, Nieto JM, Pons I, Juárez A, Pons M. 36.  2005. Interaction between the bacterial nucleoid associated proteins Hha and H-NS involves a conformational change of Hha. Biochem. J. 388:755–62 [Google Scholar]
  37. García J, Cordeiro TN, Prieto MJ, Pons M. 37.  2012. Oligomerization and DNA binding of Ler, a master regulator of pathogenicity of enterohemorrhagic and enteropathogenic Escherichia coli. Nucleic Acids Res. 40:10254–62 [Google Scholar]
  38. García J, Madrid C, Cendra M, Juárez A, Pons M. 38.  2009. N9L and L9N mutations toggle Hha binding and hemolysin regulation by Escherichia coli and Vibrio cholerae H-NS. FEBS Lett. 583:2911–16 [Google Scholar]
  39. Gordon BR, Imperial R, Wang L, Navarre WW, Liu J. 39.  2008. Lsr2 of Mycobacterium represents a novel class of H-NS-like proteins. J. Bacteriol. 190:7052–59 [Google Scholar]
  40. Gordon BR, Li Y, Cote A, Weirauch MT, Ding P. 40.  et al. 2011. Structural basis for recognition of AT-rich DNA by unrelated xenogeneic silencing proteins. PNAS 108:10690–95 [Google Scholar]
  41. Gordon BR, Li Y, Wang L, Sintsova A, van Bakel H. 41.  et al. 2010. Lsr2 is a nucleoid-associated protein that targets AT-rich sequences and virulence genes in Mycobacterium tuberculosis. PNAS 107:5154–59 [Google Scholar]
  42. Grainger DC, Hurd D, Goldberg MD, Busby SJW. 42.  2006. Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res. 34:4642–52 [Google Scholar]
  43. Haran TE, Mohanty U. 43.  2009. The unique structure of A-tracts and intrinsic DNA bending. Q. Rev. Biophys. 42:41–81 [Google Scholar]
  44. Hengge-Aronis R. 44.  1996. Back to log phase: σS as a global regulator in the osmotic control of gene expression in Escherichia coli. Mol. Microbiol. 21:887–93 [Google Scholar]
  45. Heroven AK, Dersch P. 45.  2006. RovM, a novel LysR-type regulator of the virulence activator gene rovA, controls cell invasion, virulence and motility of Yersinia pseudotuberculosis. Mol. Microbiol. 62:1469–83 [Google Scholar]
  46. Johansson J, Uhlin BE. 46.  1999. Differential protease-mediated turnover of H-NS and StpA revealed by a mutation altering protein stability and stationary-phase survival of Escherichia coli. PNAS 96:10776–81 [Google Scholar]
  47. Landick R, Wade JT, Grainger DC. 47.  2015. H-NS and RNA polymerase: a love-hate relationship?. Curr. Opin. Microbiol. 24:53–59 [Google Scholar]
  48. Langridge GC, Fookes M, Connor TR, Feltwell T, Feasey N. 48.  et al. 2015. Patterns of genome evolution that have accompanied host adaptation in Salmonella. PNAS 112:863–68 [Google Scholar]
  49. Lawson CL, Berman HM. 49.  2008. Indirect readout of DNA sequence by proteins. Protein-Nucleic Acid Interactions: Structural Biology PL Rice, CC Correll 66–90 Cambridge, UK: RSC [Google Scholar]
  50. Lercher MJ, Pál C. 50.  2008. Integration of horizontally transferred genes into regulatory interaction networks takes many million years. Mol. Biol. Evol. 25:559–67 [Google Scholar]
  51. Levine JA, Hansen AM, Michalski JM, Hazen TH, Rasko DA, Kaper JB. 51.  2014. H-NST induces LEE expression and the formation of attaching and effacing lesions in enterohemorrhagic Escherichia coli. PLOS ONE 9:e86618 [Google Scholar]
  52. Lim CJ, Kenney LJ, Yan J. 52.  2014. Single-molecule studies on the mechanical interplay between DNA supercoiling and H-NS DNA architectural properties. Nucleic Acids Res. 42:8369–78 [Google Scholar]
  53. Liu Y, Chen H, Kenney LJ, Yan J. 53.  2010. A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modes. Genes Dev. 24:339–44 [Google Scholar]
  54. Lucchini S, Rowley G, Goldberg MD, Hurd D, Harrison M, Hinton JCD. 54.  2006. H-NS mediates the silencing of laterally acquired genes in bacteria. PLOS Pathog. 2:e81 [Google Scholar]
  55. Ma J, Bai L, Wang MD. 55.  2013. Transcription under torsion. Science 340:1580–83 [Google Scholar]
  56. Madrid C, Balsalobre C, García J, Juárez A. 56.  2007. The novel Hha/YmoA family of nucleoid-associated proteins: use of structural mimicry to modulate the activity of the H-NS family of proteins. Mol. Microbiol. 63:7–14 [Google Scholar]
  57. Marraffini LA, Sontheimer EJ. 57.  2010. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat. Rev. Genet. 11:181–90 [Google Scholar]
  58. Navarre WW, McClelland M, Libby SJ, Fang FC. 58.  2007. Silencing of xenogeneic DNA by H-NS—facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA. Genes Dev. 21:1456–71 [Google Scholar]
  59. Navarre WW, Porwollik S, Wang Y, McClelland M, Rosen H. 59.  et al. 2006. Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313:236–38 [Google Scholar]
  60. Nuccio SP, Bäumler AJ. 60.  2014. Comparative analysis of Salmonella genomes identifies a metabolic network for escalating growth in the inflamed gut. mBio 5:e00929–14 [Google Scholar]
  61. Oshima T, Ishikawa S, Kurokawa K, Aiba H, Ogasawara N. 61.  2006. Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res. 13:141–53 [Google Scholar]
  62. Paytubi S, Madrid C, Forns N, Nieto JM, Balsalobre C. 62.  et al. 2004. YdgT, the Hha paralogue in Escherichia coli, forms heteromeric complexes with H-NS and StpA. Mol. Microbiol. 54:251–63 [Google Scholar]
  63. Polz MF, Alm EJ, Hanage WP. 63.  2013. Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet. 29:170–75 [Google Scholar]
  64. Qu Y, Lim CJ, Whang YR, Liu J, Yan J. 64.  2013. Mechanism of DNA organization by Mycobacterium tuberculosis protein Lsr2. Nucleic Acids Res. 41:5263–72 [Google Scholar]
  65. Renault M, García J, Cordeiro TN, Baldus M, Pons M. 65.  2013. Protein oligomers studied by solid-state NMR—the case of the full-length nucleoid-associated protein histone-like nucleoid structuring protein. FEBS J. 280:2916–28 [Google Scholar]
  66. Rivera-Chávez F, Bäumler AJ. 66.  2015. The pyromaniac inside you: Salmonella metabolism in the host gut. Annu. Rev. Microbiol. 69:31–48 [Google Scholar]
  67. Rojas-López M, Arenas-Hernández MM, Medrano-López A, Martínez de la Pena CF, Puente JL. 67.  et al. 2011. Regulatory control of the Escherichia coli O157:H7 lpf1 operon by H-NS and Ler. J. Bacteriol. 193:1622–32 [Google Scholar]
  68. Shintani M, Suzuki-Minakuchi C, Nojiri H. 68.  2015. Nucleoid-associated proteins encoded on plasmids: occurrence and mode of function. Plasmid 80:32–44 [Google Scholar]
  69. Sorek R, Kunin V, Hugenholtz P. 69.  2008. CRISPR—a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat. Rev. Microbiol. 6:181–86 [Google Scholar]
  70. Sorek R, Zhu Y, Creevey CJ, Francino MP, Bork P, Rubin EM. 70.  2007. Genome-wide experimental determination of barriers to horizontal gene transfer. Science 318:1449–52 [Google Scholar]
  71. Spurio R, Falconi M, Brandi A, Pon CL, Gualerzi CO. 71.  1997. The oligomeric structure of nucleoid protein H-NS is necessary for recognition of intrinsically curved DNA and for DNA bending. EMBO J. 16:1795–805 [Google Scholar]
  72. Srinivasan R, Scolari VF, Lagomarsino MC, Seshasayee ASN. 72.  2015. The genome-scale interplay amongst xenogene silencing, stress response and chromosome architecture in Escherichia coli. Nucleic Acids Res. 43:295–308 [Google Scholar]
  73. Stoebel DM, Free A, Dorman CJ. 73.  2008. Anti-silencing: overcoming H-NS-mediated repression of transcription in gram-negative enteric bacteria. Microbiology 154:2533–45 [Google Scholar]
  74. Summers EL, Meindl K, Uson I, Mitra AK, Radjainia M. 74.  et al. 2012. The structure of the oligomerization domain of Lsr2 from Mycobacterium tuberculosis reveals a mechanism for chromosome organization and protection. PLOS ONE 7:e38542 [Google Scholar]
  75. Tendeng C, Soutourina OA, Danchin A, Bertin PN. 75.  2003. MvaT proteins in Pseudomonas spp.: a novel class of H-NS-like proteins. Microbiology 149:3047–50 [Google Scholar]
  76. Ueda T, Takahashi H, Uyar E, Ishikawa S, Ogasawara N, Oshima T. 76.  2013. Functions of the Hha and YdgT proteins in transcriptional silencing by the nucleoid proteins, H-NS and StpA, in Escherichia coli. DNA Res. 20:263–71 [Google Scholar]
  77. Ueguchi C, Suzuki T, Yoshida T, Tanaka K, Mizuno T. 77.  1996. Systematic mutational analysis revealing the functional domain organization of Escherichia coli nucleoid protein H-NS. J. Mol. Biol. 263:149–62 [Google Scholar]
  78. Ulissi U, Fabbretti A, Sette M, Giuliodori AM, Spurio R. 78.  2014. Time-resolved assembly of a nucleoprotein complex between Shigella flexneri virF promoter and its transcriptional repressor H-NS. Nucleic Acids Res. 42:13039–50 [Google Scholar]
  79. Vasu K, Nagaraja V. 79.  2013. Diverse functions of restriction-modification systems in addition to cellular defense. Microbiol. Molec. Biol. Rev. 77:53–72 [Google Scholar]
  80. Walthers D, Li Y, Liu Y, Anand G, Yan J, Kenney LJ. 80.  2011. Salmonella enterica response regulator SsrB relieves H-NS silencing by displacing H-NS bound in polymerization mode and directly activates transcription. J. Biol. Chem. 286:1895–902 [Google Scholar]
  81. Wang H, Yehoshua S, Ali SS, Navarre WW, Milstein JN. 81.  2014. A biomechanical mechanism for initiating DNA packaging. Nucleic Acids Res 42:11921–27 [Google Scholar]
  82. Will WR, Navarre WW, Fang FC. 82.  2015. Integrated circuits: how transcriptional silencing and counter-silencing facilitate bacterial evolution. Curr. Opin. Microbiol. 23:8–13 [Google Scholar]
  83. Williams LD, Maher LJ 3rd. 83.  2000. Electrostatic mechanisms of DNA deformation. Annu. Rev. Biophys. Biomol. Struct. 29:497–521 [Google Scholar]
  84. Winardhi RS, Fu W, Castang S, Li Y, Dove SL, Yan J. 84.  2012. Higher order oligomerization is required for H-NS family member MvaT to form gene-silencing nucleoprotein filament. Nucleic Acids Res. 40:8942–52 [Google Scholar]
  85. Winardhi RS, Gulvady R, Mellies JL, Yan J. 85.  2014. Locus of enterocyte effacement-encoded regulator (Ler) of pathogenic Escherichia coli competes off histone-like nucleoid-structuring protein (H-NS) through noncooperative DNA binding. J. Biol. Chem. 289:13739–50 [Google Scholar]
  86. Winardhi RS, Yan J, Kenney LJ. 86.  2015. H-NS regulates gene expression and compacts the nucleoid: insights from single-molecule experiments. Biophys. J. 109:1321–29 [Google Scholar]
  87. Zhang C, Guttula D, Liu F, Malar PP, Ng SY. 87.  et al. 2013. Effect of H-NS on the elongation and compaction of single DNA molecules in a nanospace. Soft Matter 9:9593–601 [Google Scholar]
  88. Zhou T, Yang L, Lu Y, Dror I, Dantas Machado AC. 88.  et al. 2013. DNAshape: a method for the high-throughput prediction of DNA structural features on a genomic scale. Nucleic Acids Res. 41:W56–62 [Google Scholar]
  89. Zhou Y, Gottesman S. 89.  2006. Modes of regulation of RpoS by H-NS. J. Bacteriol. 188:7022–25 [Google Scholar]
  90. Zwir I, Yeo WS, Shin D, Latifi T, Huang H, Groisman EA. 90.  2014. Bacterial nucleoid-associated protein uncouples transcription levels from transcription timing. mBio 5:e01485–14 [Google Scholar]
/content/journals/10.1146/annurev-micro-102215-095301
Loading
/content/journals/10.1146/annurev-micro-102215-095301
Loading

Data & Media loading...

  • Article Type: Review Article
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