Skip to main content
Log in

Considerations on bacterial nucleoids

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The classic genome organization of the bacterial chromosome is normally envisaged with all its genetic markers linked, thus forming a closed genetic circle of duplex stranded DNA (dsDNA) and several proteins in what it is called as “the bacterial nucleoid.” This structure may be more or less corrugated depending on the physiological state of the bacterium (i.e., resting state or active growth) and is not surrounded by a double membrane as in eukayotic cells. The universality of the closed circle model in bacteria is however slowly changing, as new data emerge in different bacterial groups such as in Planctomycetes and related microorganisms, species of Borrelia, Streptomyces, Agrobacterium, or Phytoplasma. In these and possibly other microorganisms, the existence of complex formations of intracellular membranes or linear chromosomes is typical; all of these situations contributing to weakening the current cellular organization paradigm, i.e., prokaryotic vs eukaryotic cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arold ST, Leonard PG, Parkinson GN, Ladbury JE (2010) H-NS forms a superhelical protein scaffold for DNA condensation. Proc Natl Acad Sci U S A 107:15728–15732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atlung T, Sund S, Olesen K, Brøndsted L (1996) The histone-like protein H-NS acts as a transcriptional repressor for expression of the anaerobic and growth phase activator AppY of Escherichia coli. J Bacteriol 178:3418–3425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azam TA, Hiraga S, Ishihama A (2000) Two types of localization of the DNA-binding proteins within the Escherichia coli nucleoid. Genes Cells 5:613–626

    Article  CAS  PubMed  Google Scholar 

  • Badrinarayanan A, Le TB, Laub MT (2015) Bacterial chromosome organization and segregation. Annu Rev Cell Dev Biol 31:171–199. doi:10.1146/annurev-cellbio-100814-125211

  • Baril C, Richaud C, Baranton G, Saint Girons IS (1989) Linear chromosome of Borrelia burgdorferi. Res Microbiol 140:507–516

    Article  CAS  PubMed  Google Scholar 

  • Bensaid A, Uzan M, Jacq A, Hibner U, Brody E, Rouvière-Yaniv J (1994) Some properties of HU are modified after the infection of Escherichia coli by bacteriophage T4. J Bacteriol 176:1578–1585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Browning DF, Grainger DC, Busby SJ (2010) Effects of nucleoid-associated proteins on bacterial chromosome structure and gene expression. Curr Opin Microbiol 13:773–780

    Article  CAS  PubMed  Google Scholar 

  • Cagliero C, Zhou YN, Jin DJ (2014) Spatial organization of transcription machinery and its segregation from the replisome in fast-growing bacterial cells. Nucleic Acids Res 42:13696–13705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casjens S (1999) Evolution of the linear DNA replicons of the Borrelia spirochetes. Curr Opin Microbiol 2:529–534

    Article  CAS  PubMed  Google Scholar 

  • Casjens SR, Mongodin EF, Qiu W-G, Luft BJ, Schutzer SE, Gilcrease EB, Huang WM, Vujadinovic M, Aron JK, Vargas LC, Freeman S, Radune D, Weidman JF, Dimitrov GI, Khouri HM, Sosa JE, Halpin RA, Dunn JJ, Fraser CM (2012) Genome stability of Lyme disease spirochetes: comparative genomics of Borrelia burgdorferi plasmids. PLoS One 7:e33280. doi:10.1371/journal.pone.0033280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cayrou C, Raoult D, Drancourt M (2010) Broad-spectrum antibiotic resistance of Planctomycetes organisms determined by Etest. J Antimicrob Chemother 65:2119–2122

    Article  CAS  PubMed  Google Scholar 

  • Chaconas G, Kobryn K (2010) Structure, function, and evolution of linear replicons in Borrelia. Annu Rev Microbiol 64:185–202

    Article  CAS  PubMed  Google Scholar 

  • Chapman GB (1959) Electron microscopy of ultrathin sections of bacteria. III. Cell wall, cytoplasmic membrane, and nuclear material. J Bacteriol 78:96–104

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen W, He F, Zhang X, Chen Z, Wen Y, Li J (2010) Chromosomal instability in Streptomyces avermitilis: major deletion in the central region and stable circularized chromosome. BMC Microbiol 10:198

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chumsakul O, Nakamura K, Kurata T, Sakamoto T, Hobman JL, Ogasawara N, Oshima T, Ishikawa S (2013) High-resolution mapping of in vivo genomic transcription factor binding sites using in situ DNase I footprinting and ChIP-seq. DNA Res 20:325–338. doi:10.1093/dnares/dst013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coker C, Bakare OO, Mobley HL (2000) H-NS is a repressor of the Proteus mirabilis urease transcriptional activator gene ureR. J Bacteriol 182:2649–2653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui T, Moro-oka N, Ohsumi K, Kodama K, Ohshima T, Ogasawara N, Mori H, Wanner B, Niki H, Horiuchi T (2007) Escherichia coli with a linear genome. EMBO Rep 8:181–187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dalai B, Zhou R, Wan Y, Kang M, Li L, Li T, Zhang S, Chen H (2009) Histone-like protein H-NS regulates biofilm formation and virulence of Actinobacillus pleuropneumoniae. Microb Pathog 46:128–134

    Article  CAS  PubMed  Google Scholar 

  • Dame RT, Dame T (2016) Bacterial chromatin: converging views at different scales. Curr Opin Cell Biol 40:60–65. doi:10.1016/j.ceb.2016.02.015

    Article  CAS  PubMed  Google Scholar 

  • Dame RT, Wyman C, Wurm R, Wagner R, Goosen N (2002) Structural basis for H-NS-mediated trapping of RNA polymerase in the open initiation complex at the rrnB P1. J Biol Chem 277:2146–2450

  • Dersch P, Kneip S, Bremer E (1994) The nucleoid-associated DNA-binding protein H-NS is required for the efficient adaptation of Escherichia coli K-12 to a cold environment. Mol Gen Genet 245:255–259

    Article  CAS  PubMed  Google Scholar 

  • Desmond E, Gribaldo S (2009) Phylogenomics of sterol synthesis: insights into the origin, evolution, and diversity of a key eukaryotic feature. Genome Biol Evol 1:364–381

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Devos DP (2014) PVC bacteria: variation of, but not exception to, the Gram-negative cell plan. Trends Microbiol 22:14–20

    Article  CAS  PubMed  Google Scholar 

  • Donato GM, Kawula TH (1998) Enhanced binding of altered H-NS protein to flagellar rotor protein FliG causes increased flagellar rotational speed and hypermotility in Escherichia coli. J Biol Chem 273:24030–24036

    Article  CAS  PubMed  Google Scholar 

  • Donato GM, Lelivelt MJ, Kawula TH (1997) Promoter-specific repression of fimB expression by the Escherichia coli nucleoid-associated protein H-NS. J Bacteriol 179:6618–6625

  • Dorman CJ (2014) Function of nucleoid-associated proteins in chromosome structuring and transcriptional regulation. J Mol Microbiol Biotechnol 24:316–331. doi:10.1159/000368850

    Article  CAS  PubMed  Google Scholar 

  • Eijkelkamp BA, Stroeher UH, Hassan KA, Elbourne LD, Paulsen IT, Brown MH (2013) H-NS plays a role in expression of Acinetobacter baumannii virulence features. Infect Immun 81:2574–2583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elbir H, Gimenez G, Robert C, Bergström S, Cutler S, Raoult D, Drancourt M (2012) Complete genome sequence of Borrelia crocidurae. J Bacteriol 194:3723–3724

    Article  PubMed  PubMed Central  Google Scholar 

  • Falconi M, Prosseda G, Giangrossi M, Beghetto E, Colonna B (2001) Involvement of FIS in the H-NS-mediated regulation of virF gene of Shigella and enteroinvasive Escherichia coli. Mol Microbiol 42:439–452

  • Feng JX, Song ZZ, Duan CJ, Zhao S, Wu YQ, Wang C, Dow JM, Tang JL (2009) The xrvA gene of Xanthomonas oryzae pv. oryzae, encoding an H-NS-like protein, regulates virulence in rice. Microbiology 155:3033–3044

    Article  CAS  PubMed  Google Scholar 

  • Ferdows MS, Barbour AG (1989) Megabase-sized linear DNA in the bacterium Borrelia burgdorferi, the Lyme disease agent. Proc Natl Acad Sci U S A 86:5969–5973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forterre P (2002) A hot story from comparative genomics: reverse gyrase is the only hyperthermophile-specific protein. Trends Genet 18:236–237

    Article  CAS  PubMed  Google Scholar 

  • Forterre P (2011) A new fusion hypothesis for the origin of Eukarya better than previous ones, but probably also wrong. Res Microbiol 162:77–91

    Article  CAS  PubMed  Google Scholar 

  • Franzmann PD, Skerman VB (1984) Gemmata obscuriglobus, a new genus and species of the budding bacteria. Antonie Van Leeuwenhoek 50:261–268

    Article  CAS  PubMed  Google Scholar 

  • Franzon JH, Santos DS (2004) A role for histone-like protein H1 (H-NS) in the regulation of hemolysin expression by Serratia marcescens. Braz J Med Biol Res 37:1763–1769

    Article  CAS  PubMed  Google Scholar 

  • Fuerst JA (2005) Intracellular compartmentation in Planctomycetes. Annu Rev Microbiol 59:299–328

    Article  CAS  PubMed  Google Scholar 

  • Fuerst JA, Sagulenko E (2010) Protein uptake by bacteria: an endocytosis-like process in the planctomycete Gemmata obscuriglobus. Commun Integr Biol 3:572–575

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fuerst JA, Sagulenko E (2011) Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat Rev Microbiol 9:403–413

    Article  CAS  PubMed  Google Scholar 

  • Fuerst JA, Sagulenko E (2013) Nested bacterial boxes: nuclear and other intracellular compartments in Planctomycetes. J Mol Microbiol Biotechnol 23:95–103. doi:10.1159/000346544

    Article  CAS  PubMed  Google Scholar 

  • Gérard F, Dri AM, Moreau PL (1999) Role of Escherichia coli RpoS, LexA and H-NS global regulators in metabolism and survival under aerobic, phosphate-starvation conditions. Microbiology 145:1547–1562

    Article  PubMed  Google Scholar 

  • Glöckner FO, Kube M, Bauer M, Teeling H, Lombardot T, Ludwig W, Gade D, Beck A, Borzym K, Heitmann K, Rabus R, Schlesner H, Amann R, Reinhardt R (2003) Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci U S A 100:8298–8303

    Article  PubMed  PubMed Central  Google Scholar 

  • Gottshall EY, Seebart C, Gatlin JC, Ward NL (2014) Spatially segregated transcription and translation in cells of the endomembrane-containing bacterium Gemmata obscuriglobus. Proc Natl Acad Sci U S A 111:11067–11072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grainger DC, Goldberg MD, Lee DJ, Busby SJ (2008) Selective repression by Fis and H-NS at the Escherichia coli dps promoter. Mol Microbiol 68:1366–1377

    Article  CAS  PubMed  Google Scholar 

  • Guo M, Zhou Q, Zhou Y, Yang L, Liu T, Yang J, Chen Y, Su L, Xu J, Chen J, Liu F, Chen J, Dai W, Ni P, Fang C, Yang R (2014) Genomic evolution of 11 type strains within family Planctomycetaceae. PLoS One 9:e86752

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hammar M, Arnqvist A, Bian Z, Olsén A, Normark S (1995) Expression of two csg operons is required for production of fibronectin- and congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol 18:661–670

    Article  CAS  PubMed  Google Scholar 

  • Heroven AK, Nagel G, Tran HJ, Parr S, Dersch P (2004) RovA is autoregulated and antagonizes H-NS-mediated silencing of invasin and rovA expression in Yersinia pseudotuberculosis. Mol Microbiol 53:871–888

    Article  CAS  PubMed  Google Scholar 

  • Hinnebusch BJ, Bendich AJ (1997) The bacterial nucleoid visualized by fluorescence microscopy of cells lysed within agarose: comparison of Escherichia coli and spirochetes of the genus Borrelia. J Bacteriol 179:2228–2237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hommais F, Krin E, Laurent-Winter C, Soutourina O, Malpertuy A, Le Caer JP, Danchin A, Bertin P (2001) Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol Microbiol 40:20–36

    Article  CAS  PubMed  Google Scholar 

  • Huang SH, Kobryn K2 (2016) The Borrelia burgdorferi telomere resolvase, ResT, anneals ssDNA complexed with its cognate ssDNA-binding protein. Nucleic Acids Res 44:5288–5298. doi:10.1093/nar/gkw344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang CH, Lin YS, Yang YL, Huang SW, Chen CW (1998) The telomeres of Streptomyces chromosomes contain conserved palindromic sequences with potential to form complex secondary structures. Mol Microbiol 28:905–926

    Article  CAS  PubMed  Google Scholar 

  • Huang WM, DaGloria J, Fox H, Ruan Q, Tillou J, Shi K, Aihara H, Aron J, Casjens S (2012) Linear chromosome-generating system of Agrobacterium tumefaciens C58: protelomerase generates and protects hairpin ends. J Biol Chem 287:25551–25563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang SH, Cozart MR, Hart MA, Kobryn K: The Borrelia burgdorferi telomere resolvase, ResT, possesses ATP-dependent DNA unwinding activity (2016) Nucleic Acids Res pii: gkw1243.

  • Jeske O, Schueler M, Schumann P, Schneider A, Boedeker C, Jogler M, Bollschweiler D, Rohde M, Mayer C, Engelhardt H, Spring S, Jogler C (2015) Planctomycetes do possess a peptidoglycan cell wall. Nat Commun 6:7116. doi:10.1038/ncomms8116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang B, Yao H, Tong Y, Yang X, Huang Y, Jiang J, Cao W (2012) Genome sequence of Borrelia garinii strain NMJW1, isolated from China. J Bacteriol 194:6660–6661. doi:10.1128/JB.01844-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jogler C (2014) The bacterial ‘mitochondrium’. Mol Microbiol 94:751–755

    Article  CAS  PubMed  Google Scholar 

  • Jogler C, Waldmann J, Huang X, Jogler M, Glöckner FO, Mascher T, Kolter R (2012) Identification of proteins likely to be involved in morphogenesis, cell division, and signal transduction in Planctomycetes by comparative genomics. J Bacteriol 194:6419–6430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johansson J, Dagberg B, Richet E, Uhlin BE (1998) H-NS and StpA proteins stimulate expression of the maltose regulon in Escherichia coli. J Bacteriol 180:6117–6125

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johansson J, Balsalobre C, Wang SY, Urbonaviciene J, Jin DJ, Sondén B, Uhlin BE (2000) Nucleoid proteins stimulate stringently controlled bacterial promoters: a link between the cAMP-CRP and the (p)ppGpp regulons in Escherichia coli. Cell 20102:475–485

    Article  Google Scholar 

  • Jutras BL, Bowman A, Brissette CA, Adams CA, Verma A, Chenail AM, Stevenson B (2012) EbfC (YbaB) is a new type of bacterial nucleoid-associated protein and a global regulator of gene expression in the Lyme disease spirochete. J Bacteriol 194:3395–3406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kahramanoglou C, Seshasayee AS, Prieto AI, Ibberson D, Schmidt S, Zimmermann J, Benes V, Fraser GM, Luscombe NM (2011) Direct and indirect effects of H-NS and Fis on global gene expression control in Escherichia coli. Nucleic Acids Res 39:2073–2091. doi:10.1093/nar/gkq934

    Article  CAS  PubMed  Google Scholar 

  • Katayama T, Takata M, Sekimizu K (1996) The nucleoid protein H-NS facilitates chromosome DNA replication in Escherichia coli dnaA mutants. J Bacteriol 178:5790–5792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kingry LC, Batra D, Replogle A, Rowe LA2, Pritt BS, Petersen JM (2016) Whole genome sequence and comparative genomics of the novel Lyme Borreliosis causing pathogen, Borrelia mayonii. PLoS One 11:e0168994. doi:10.1371/journal.pone.0168994

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • König H, Schlesner H, Hirsch P (1984) Cell wall studies on budding bacteria of the Planctomyces/Pasteuria group and on a Prosthecomicrobium sp. Arch Microbiol 138:200–205

    Article  Google Scholar 

  • Kube M, Schneider B, Kuhl H, Dandekar T, Heitmann K, Migdoll AM, Reinhardt R, Seemüller E (2008) The linear chromosome of the plant-pathogenic mycoplasma ‘Candidatus Phytoplasma mali’. BMC Genomics 9:306

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lang B, Blot N, Bouffartigues E, Buckle M, Geertz M, Gualerzi CO, Mavathur R, Muskhelishvili G, Pon CL, Rimsky S, Stella S, Babu MM, Travers A (2007) High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res 35:6330–6337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le TB, Laub MT (2014) New approaches to understanding the spatial organization of bacterial genomes. Curr Opin Microbiol 22:15–21. doi:10.1016/j.mib.2014.09.014

    Article  CAS  PubMed  Google Scholar 

  • Le TB, Imakaev MV, Mirny LA, Laub MT (2013) High-resolution mapping of the spatial organization of a bacterial chromosome. Science 342:731–734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leake MC (2016) Chromosome architecture. In: Methods in molecular biology, vol 143. Springer, New York

    Google Scholar 

  • Lee KC, Webb RI, Janssen PH, Sangwan P, Romeo T, Staley JT, Fuerst JA (2009) Phylum Verrucomicrobia representatives share a compartmentalized cell plan with members of bacterial phylum Planctomycetes. BMC Microbiol 9:5. doi:10.1186/1471-2180-9-5

    Article  PubMed  PubMed Central  Google Scholar 

  • Lieber A, Leis A, Kushmaro A, Minsky A, Medalia O (2009) Chromatin organization and radio resistance in the bacterium Gemmata obscuriglobus. J Bacteriol 191:1439–1445

    Article  CAS  PubMed  Google Scholar 

  • Liesack W, König H, Schlesner H, Hirsch P (1986) Chemical composition of the peptidoglycan-free cell envelopes of budding bacteria of the Pirella/Planctomyces group. Arch Microbiol 145:361–366

    Article  CAS  Google Scholar 

  • Lin YS, Chen CW (1997) Instability of artificially circularized chromosomes of Streptomyces lividans. Mol Microbiol 26:709–719

    Article  CAS  PubMed  Google Scholar 

  • Lindsay MR, Webb RI, Strous M, Jetten MS, Butler MK, Forde RJ, Fuerst JA (2001) Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch Microbiol 175:413–429

    Article  CAS  PubMed  Google Scholar 

  • Lonhienne TG, Sagulenko E, Webb RI, Lee KC, Franke J, Devos DP, Nouwens A, Carroll BJ, Fuerst JA (2010) Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci U S A 107:12883–12888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lucchini S, Rowley G, Goldberg MD, Hurd D, Harrison M, Hinton JC (2006) H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog 2:e81

    Article  PubMed  PubMed Central  Google Scholar 

  • Lucht JM, Dersch P, Kempf B, Bremer E (1994) Interactions of the nucleoid-associated DNA-binding protein H-NS with the regulatory region of the osmotically controlled proU operon of Escherichia coli. J Biol Chem 269:6578

    CAS  PubMed  Google Scholar 

  • Marbouty M, Le Gall A, Cattoni DI, Cournac A, Koh A, Fiche JB, Mozziconacci J, Murray H, Koszul R, Nollmann M (2015) Condensin- and replication-mediated bacterial chromosome folding and origin condensation revealed by Hi-C and super-resolution imaging. Mol Cell 59:588–602

    Article  CAS  PubMed  Google Scholar 

  • Marconi RT, Casjens S, Munderloh UG, Samuels DS (1996) Analysis of linear plasmid dimers in Borrelia burgdorferi sensu lato isolates: implications concerning the potential mechanism of linear plasmid replication. J Bacteriol 178:3357–3361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McGovern V, Higgins NP, Chiz RS, Jaworski A (1994) H-NS over-expression induces an artificial stationary phase by silencing global transcription. Biochimie 76:1019–1029

    Article  CAS  PubMed  Google Scholar 

  • McInerney JO, Martin WF, Koonin EV, Allen JF, Galperin MY, Lane N, Archibald JM, Embley TM (2011) Planctomycetes and eukaryotes: a case of analogy not homology. BioEssays 33:810–817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller SC, Porcella SF, Raffel SJ, Schwan TG, Barbour AG (2013) Large linear plasmids of Borrelia species that cause relapsing fever. J Bacteriol 195:3629–3639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy LD, Zimmerman SB (2000) Multiple restraints to the unfolding of spermidine nucleoids from Escherichia coli. J Struct Biol 132:46–62

    Article  CAS  PubMed  Google Scholar 

  • Nasser W, Reverchon S (2002) H-NS-dependent activation of pectate lyases synthesis in the phytopathogenic bacterium Erwinia chrysanthemi is mediated by the PecT repressor. Mol Microbiol 43:733–748

    Article  CAS  PubMed  Google Scholar 

  • Nasser W, Faelen M, Hugouvieux-Cotte-Pattat N, Reverchon S (2001) Role of the nucleoid-associated protein H-NS in the synthesis of virulence factors in the phytopathogenic bacterium Erwinia chrysanthemi. Mol Plant-Microbe Interact 14:10–20

    Article  CAS  PubMed  Google Scholar 

  • Nielsen HJ, Ottesen JR, Youngren B, Austin SJ, Hansen FG (2006) The Escherichia coli chromosome is organized with the left and right chromosome arms in separate cell halves. Mol Microbiol 62:331–338

    Article  CAS  PubMed  Google Scholar 

  • Nieto JM, Madrid C, Prenafeta A, Miquelay E, Balsalobre C, Carrascal M, Juárez A (2000) Expression of the hemolysin operon in Escherichia coli is modulated by a nucleoid-protein complex that includes the proteins Hha and H-NS. Mol Gen Genet 263:349–358

    Article  CAS  PubMed  Google Scholar 

  • Nindita Y, Nishikawa T, Arakawa K, Wang G, Ochi K, Qin Z, Kinashi H (2013) Chromosomal circularization of the model Streptomyces species, Streptomyces coelicolor A3(2). FEMS Microbiol Lett 347:149–155. doi:10.1111/1574-6968.12228

    CAS  PubMed  Google Scholar 

  • Nishino K, Yamaguchi A (2004) Role of histone-like protein H-NS in multidrug resistance of Escherichia coli. J Bacteriol 186:1423–1429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishino K, Hayashi-Nishino M, Yamaguchi A (2009) H-NS modulates multidrug resistance of Salmonella enterica serovar typhimurium by repressing multidrug efflux genes acrEF. Antimicrob Agents Chemother 53:3541–3543. doi:10.1128/AAC.00371-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Norris SJ (2014) vls antigenic variation systems of Lyme disease Borrelia: eluding host immunity through both random, segmental gene conversion and framework heterogeneity. Microbiol Spectr. doi:10.1128/microbiolspec.MDNA3-0038-2014

    PubMed  PubMed Central  Google Scholar 

  • Nye MB, Pfau JD, Skorupski K, Taylor RK (2000) Vibrio cholerae H-NS silences virulence gene expression at multiple steps in the ToxR regulatory cascade. J Bacteriol 182:4295–4303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O'Byrne CP, Dorman CJ (1994) Transcription of the Salmonella typhimurium spv virulence locus is regulated negatively by the nucleoid-associated protein H-NS. FEMS Microbiol Lett 121:99–105

    Article  PubMed  Google Scholar 

  • O'Gara JP, Dorman CJ (2000) Effects of local transcription and H-NS on inversion of the fim switch of Escherichia coli. Mol Microbiol 36:457–466

    Article  PubMed  Google Scholar 

  • Oh TJ, Jung IL, Kim IG (2001) The Escherichia coli SOS gene sbmC is regulated by H-NS and RpoS during the SOS induction and stationary growth phase. Biochem Biophys Res Commun 288:1052–1058

  • Olekhnovich IN, Kadner RJ (2007) Role of nucleoid-associated proteins Hha and H-NS in expression of Salmonella enterica activators HilD, HilC, and RtsA required for cell invasion. J Bacteriol 189:6882–6890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olsen PB, Klemm P (1994) Localization of promoters in the fim gene cluster and the effect of H-NS on the transcription of fimB and fimE. FEMS Microbiol Lett 116:95–100

  • Ono S, Goldberg MD, Olsson T, Esposito D, Hinton JC, Ladbury JE (2005) H-NS is a part of a thermally controlled mechanism for bacterial gene regulation. Biochem J 391:203–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oshima T, Ishikawa S, Kurokawa K, Aiba H, Ogasawara N (2006) Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res 13:141–153

    Article  CAS  PubMed  Google Scholar 

  • Pearson A, Budin M, Brocks JJ (2003) Phylogenetic and biochemical evidence for sterol synthesis in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci U S A 100:15352–15357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petersen C, Møller LB, Valentin-Hansen P (2002) The cryptic adenine deaminase gene of Escherichia coli. Silencing by the nucleoid-associated DNA-binding protein, H-NS, and activation by insertion elements. J Biol Chem 277:31373–31380

    Article  CAS  PubMed  Google Scholar 

  • Picardeau M, Lobry JR, Hinnebusch BJ (1999) Physical mapping of an origin of bidirectional replication at the centre of the Borrelia burgdorferi linear chromosome. Mol Microbiol 32:437–445

    Article  CAS  PubMed  Google Scholar 

  • Pilhofer M, Rappl K, Eckl C, Bauer AP, Ludwig W, Schleifer KH, Petroni G (2008) Characterization and evolution of cell division and cell wall synthesis genes in the bacterial phyla Verrucomicrobia, Lentisphaerae, Chlamydiae, and Planctomycetes and phylogenetic comparison with rRNA genes. J Bacteriol 190:3192–3202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pilhofer M, Aistleitner K, Biboy J, Gray J, Kuru E, Hall E, Brun YV, Van Nieuwenhze MS, Vollmer W, Horn M, Jensen GJ (2013) Discovery of chlamydial peptidoglycan reveals bacteria with murein sacculi but without FtsZ. Nat Commun 4:2856

    Article  PubMed  CAS  Google Scholar 

  • Postow L, Hardy CD, Arsuaga J, Cozzarelli NR (2004) Topological domain structure of the Escherichia coli chromosome. Genes Dev 18:1766–1779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prieto AI, Kahramanoglou C, Ali RM, Fraser GM, Seshasayee AS, Luscombe NM (2012) Genomic analysis of DNA binding and gene regulation by homologous nucleoid-associated proteins IHF and HU in Escherichia coli K12. Nucleic Acids Res 40:3524–3537. doi:10.1093/nar/gkr1236

    Article  CAS  PubMed  Google Scholar 

  • Pul U, Wurm R, Arslan Z, Geissen R, Hofmann N, Wagner R (2010) Identification and characterization of E. coli CRISPR-cas promoters and their silencing by H-NS. Mol Microbiol 75:1495–1512. doi:10.1111/j.1365-2958.2010.07073.x

    Article  CAS  PubMed  Google Scholar 

  • Rajkumari K, Kusano S, Ishihama A, Mizuno T, Gowrishankar (1996) Effects of H-NS and potassium glutamate on sigmaS- and sigma70-directed transcription in vitro from osmotically regulated P1 and P2 promoters of proU in Escherichia coli. J Bacteriol 178:4176–4181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynaud EG, Devos DP (2011) Transitional forms between the three domains of life and evolutionary implications. Proc R Soc B Biol Sci 278:3321–3328

    Article  Google Scholar 

  • Ricci DP, Melfi MD, Lasker K, Dill DL, McAdams HH, Shapiro L (2016) Cell cycle progression in Caulobacter requires a nucleoid-associated protein with high AT sequence recognition. Proc Nat Acad Sci USA 113:E5952–E5961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riley SP, Bykowski T, Cooley AE, Burns LH, Babb K, Brissette CA, Bowman A, Rotondi M, Miller MC, DeMoll E, Lim K, Fried MG, Stevenson B (2009) Borrelia burgdorferi EbfC defines a newly-identified, widespread family of bacterial DNA-binding proteins. Nucleic Acids Res 37:1973–1983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivas-Marín E, Canosa I, Devos DP (2016) Evolutionary cell biology of division mode in the bacterial Planctomycetes-Verrucomicrobia-Chlamydiae superphylum. Front Microbiol 7:1964

    PubMed  PubMed Central  Google Scholar 

  • Rouviere-Yaniv J, Yaniv M, Germond JE (1979) E. coli DNA binding protein HU forms nucleosome like structure with circular double-stranded DNA. Cell 17:265–274

    Article  CAS  PubMed  Google Scholar 

  • Sagulenko E, Morgan GP, Webb RI, Yee B, Lee KC, Fuerst JA (2014) Structural studies of planctomycete Gemmata obscuriglobus support cell compartmentalisation in a bacterium. PLoS One 9:e91344. doi:10.1371/journal.pone.0091344

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Salomon D, Klimko JA, Orth K (2014) H-NS regulates the Vibrio parahaemolyticus type VI secretion system 1. Microbiology 160:1867–1873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santarella-Mellwig R, Pruggnaller S, Roos N, Mattaj IW, Devos DP (2013) Three-dimensional reconstruction of bacteria with a complex endomembrane system. PLoS Biol 11:e1001565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlesner H, Stackebrandt E (1986) Assignment of the genera Planctomyces and Pirella to a new family Planctomycetaceae fam. nov. and description of the order Planctomycetales ord. nov. Syst Appl Microbiol 8:174–176

    Article  Google Scholar 

  • Schüler W, Bunikis I, Weber-Lehman J, Comstedt P, Kutschan-Bunikis S, Stanek G, Huber J, Meinke A, Bergström S, Lundberg U (2015) Complete genome sequence of Borrelia afzelii K78 and comparative genome analysis. PLoS One 10:e0120548

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shiga Y, Sekine Y, Kano Y, Ohtsubo E (2001) Involvement of H-NS in transpositional recombination mediated by IS1. J Bacteriol 183:2476–2484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shintani M, Suzuki-Minakuchi C, Nojiri H (2015) Nucleoid-associated proteins encoded on plasmids. Occurrence and mode of function. Plasmid 80:32–44. doi:10.1016/j.plasmid.2015.04.008

    Article  CAS  PubMed  Google Scholar 

  • Singh RK, Liburd J, Wardle SJ, Haniford DB (2008) The nucleoid binding protein H-NS acts as an anti-channeling factor to favor intermolecular Tn10 transposition and dissemination. J Mol Biol 376:950–962

    Article  CAS  PubMed  Google Scholar 

  • Song D, Loparo JJ (2015) Building bridges within the bacterial chromosome. Trends Genet 31:164–173. doi:10.1016/j.tig.2015.01.003

    Article  CAS  PubMed  Google Scholar 

  • Soutourina O, Kolb A, Krin E, Laurent-Winter C, Rimsky S, Danchin A, Bertin P (1999) Multiple control of flagellum biosynthesis in Escherichia coli: role of H-NS protein and the cyclic AMP-catabolite activator protein complex in transcription of the flhDC master operon. J Bacteriol 181:7500–7508

  • Stanier RY, Van Niel CB (1962) The concept of a bacterium. Arch Mikrobiol 42:17–35

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Ueguchi C, Mizuno T (1996) H-NS regulates OmpF expression through micF antisense RNA in Escherichia coli. J Bacteriol 178:3650–3653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Teeseling MCF, Mesman RJ, Kuru E, Espaillat A, Cava F, Brun YV, Vannieuwenhze MS, Kartal B, van Niftrik L (2015) Anammox Planctomycetes have a peptidoglycan cell wall. Nat Commun 6:6878

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thibessard A, Leblond P (2016) Complete genome sequence of Streptomyces ambofaciens DSM 40697, a paradigm for genome plasticity studies. Genome Announc 4:e00470–e00416. doi:10.1128/genomeA.00470-16

    Article  PubMed  PubMed Central  Google Scholar 

  • Thibessard A, Haas D, Gerbaud C, Aigle B, Lautru S, Pernodet JL, Leblond P (2015) Complete genome sequence of Streptomyces ambofaciens ATCC 23877, the spiramycin producer. J Biotechnol 214:117–118. doi:10.1016/j.jbiotec.2015.09.020

    Article  CAS  PubMed  Google Scholar 

  • Tolstorukov MY, Virnik KM, Adhya S, Zhurkin VB (2005) A-tract clusters may facilitate DNA packaging in bacterial nucleoid. Nucleic Acids Res 33:3907–3918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tolstorukov MY, Virnik K, Zhurkin VB, Adhya S (2016) Organization of DNA in a bacterial nucleoid. BMC Microbiol 16:22

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tong H, Mrazek J (2014) Investigating the interplay between nucleoid-associated proteins, DNA curvature, and CRISPR elements using comparative genomics. PLoS One 9:e90940

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tourand Y, Deneke J, Moriarty TJ, Chaconas G (2009) Characterization and in vitro reaction properties of 19 unique hairpin telomeres from the linear plasmids of the Lyme disease spirochete. J Biol Chem 284:7264–7272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valens M, Penaud S, Rossignol M, Cornet F, Boccard F (2004) Macrodomain organization of the Escherichia coli chromosome. EMBO J 23:4330–4341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vallet-Gely I, Donovan KE, Fang R, Joung JK, Dove SL (2005) Repression of phase-variable cup gene expression by H-NS-like proteins in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 102:11082–11087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volff JN, Viell P, Altenbuchner J (1997) Artificial circularization of the chromosome with concomitant deletion of its inverted repeats enhances genetic instability and genome rearrangement in Streptomyces lividans. Mol Gen Genet 253:753–760

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Ayala JC, Silva AJ, Benitez JA (2012) The histone-like nucleoid structuring protein (H-NS) is a repressor of Vibrio cholerae exopolysaccharide biosynthesis (vps) genes. Appl Environ Microbiol 78:2482–2488

  • Wardle SJ, O'Carroll M, Derbyshire KM, Haniford DB (2005) The global regulator H-NS acts directly on the transpososome to promote Tn10 transposition. Genes Dev 19:2224–2235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warnecke T, Supek F, Lehner B (2012) Nucleoid-associated proteins affect mutation dynamics in E. coli in a growth phase-specific manner. PLoS Comput Biol 8:e1002846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westermark M, Oscarsson J, Mizunoe Y, Urbonaviciene J, Uhlin BE (2000) Silencing and activation of ClyA cytotoxin expression in Escherichia coli. J Bacteriol 182:6347–6357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White-Ziegler CA, Angus Hill ML, Braaten BA, van der Woude MW, Low DA (1998) Thermoregulation of Escherichia coli pap transcription: H-NS is a temperature-dependent DNA methylation blocking factor. Mol Microbiol 28:1121–1113

    Article  CAS  PubMed  Google Scholar 

  • Whitfield CR, Wardle SJ, Haniford DB (2009) The global bacterial regulator H-NS promotes transpososome formation and transposition in the Tn5 system. Nucleic Acids Res 37:309–321

    Article  CAS  PubMed  Google Scholar 

  • Will WR, Lu J, Frost LS (2004) The role of H-NS in silencing F transfer gene expression during entry into stationary phase. Mol Microbiol 54:769–782

    Article  CAS  PubMed  Google Scholar 

  • Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A 74:5088–5090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A 87:4576–4579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada H, Muramatsu S, Mizuno T (1990) An Escherichia coli protein that preferentially binds to sharply curved DNA. J Biochem 108:420–425

    Article  CAS  PubMed  Google Scholar 

  • Yamashino T, Ueguchi C, Mizuno T (1995) Quantitative control of the stationary phase-specific sigma factor, sigma S, in Escherichia coli: involvement of the nucleoid protein H-NS. EMBO J 14:594–602

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang CC, Huang CH, Li CY, Tsay YG, Lee SC, Chen CW (2002) The terminal proteins of linear Streptomyces chromosomes and plasmids: a novel class of replication priming proteins. Mol Microbiol 43:297–305

    Article  PubMed  Google Scholar 

  • Yang J, Tauschek M, Strugnell R, Robins-Browne RM (2005) The H-NS protein represses transcription of the eltAB operon, which encodes heat-labile enterotoxin in enterotoxigenic Escherichia coli, by binding to regions downstream of the promoter. Microbiology 151:1199–1208

    Article  CAS  PubMed  Google Scholar 

  • Yang CC, Tseng SM, Chen CW (2015) Telomere-associated proteins add deoxynucleotides to terminal proteins during replication of the telomeres of linear chromosomes and plasmids in Streptomyces. Nucleic Acids Res 43:6373–6383. doi:10.1093/nar/gkv302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yee B, Sagulenko E, Fuerst JA (2011) Making heads or tails of the HU proteins in the planctomycete Gemmata obscuriglobus. Microbiology 157:2012–2021

    Article  CAS  PubMed  Google Scholar 

  • Yoshida T, Yamashino T, Ueguchi C, Mizuno T (1993a) Expression of the Escherichia coli dimorphic glutamic acid decarboxylases is regulated by the nucleoid protein H-NS. Biosci Biotechnol Biochem 57:1568–1569

    Article  CAS  PubMed  Google Scholar 

  • Yoshida T, Ueguchi C, Mizuno T (1993b) Physical map location of a set of Escherichia coli genes (hde) whose expression is affected by the nucleoid protein H-NS. J Bacteriol 175:7747–7748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng Z, Liu X, Yao J, Guo Y, Li B, Li Y, Jiao N, Wang X (2016) Cold adaptation regulated by cryptic prophage excision in Shewanella oneidensis. The ISME Journal 10:2787–2800

    Article  PubMed  PubMed Central  Google Scholar 

  • Zimmerman SB (2006) Shape and compaction of Escherichia coli nucleoids. J Struct Biol 156:255–261

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to express their gratitude to Prof. Arnold Demain from Drew University (USA) for his help with the English version of the manuscript and for his criticisms. They also want to thank Jose Manuel Ageitos for his drawing of Fig. 2

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors, whatsoever.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tomás G. Villa.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Feijoo-Siota, L., Rama, J.L.R., Sánchez-Pérez, A. et al. Considerations on bacterial nucleoids. Appl Microbiol Biotechnol 101, 5591–5602 (2017). https://doi.org/10.1007/s00253-017-8381-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-017-8381-7

Keywords

Navigation