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Chromosomal organization of transcription: in a nutshell

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Abstract

Early studies of transcriptional regulation focused on individual gene promoters defined specific transcription factors as central agents of genetic control. However, recent genome-wide data propelled a different view by linking spatially organized gene expression patterns to chromosomal dynamics. Therefore, the major problem in contemporary molecular genetics concerned with transcriptional gene regulation is to establish a unifying model that reconciles these two views. This problem, situated at the interface of polymer physics and network theory, requires development of an integrative methodology. In this review, we discuss recent achievements in classical model organism E. coli and provide some novel insights gained from studies of a bacterial plant pathogen, D. dadantii. We consider DNA topology and the basal transcription machinery as key actors of regulation, in which activation of functionally relevant genes is coupled to and coordinated with the establishment of extended chromosomal domains of coherent transcription. We argue that the spatial organization of genome plays a fundamental role in its own regulation.

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References

  • Amariei C, Machné R, Stolc V, Soga T, Tomita M, Murray DB (2014) Time resolved DNA occupancy dynamics during the respiratory oscillation uncover a global reset point in the yeast growth program. Microb Cell 1:279–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balke VL, Gralla JD (1987) Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli. J Bacteriol 169:4499–4506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beber ME, Muskhelishvili G, Hütt M-T (2015) Interplay of digital and analog control in gene expression profiles. EPJ Nonlinear Biomed Phys 4(1):8

    Article  Google Scholar 

  • Bednar J, Furrer P, Stasiak A, Dubochet J, Egelman EH, Bates AD (1994) The twist, writhe and overall shape of supercoiled DNA change during counterion-induced transition from a loosely to a tightly interwound superhelix. Possible implications for DNA structure in vivo. J Mol Biol 235:825–847

    Article  CAS  PubMed  Google Scholar 

  • Bendich AJ, Drlica K (2000) Prokaryotic and eukaryotic chromosomes: what’s the difference? Bioessays 22:481–486

    Article  CAS  PubMed  Google Scholar 

  • Berger M, Farcas A, Geertz M, Zhelyaskova P, Brix K, Travers A, Muskhelishvili G (2010) Coordination of genomic structure and function by the main bacterial nucleoid-associated protein HU. EMBO Rep 11:59–64

    Article  CAS  PubMed  Google Scholar 

  • Berger M, Gerganova V, Berger P, Rapiteanu R, Lisicovas V, Dobrindt U (2016) Genes on a wire: the nucleoid-associated protein HU insulates transcription units in Escherichia coli. Sci Rep 6:31512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berthoumieux S, de Jong H, Baptist G, Pinel C, Ranquet C, Ropers D, Geiselmann J (2013) Shared control of gene expression in bacteria by transcription factors and global physiology of the cell. Mol Syst Biol 9:634

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Blot N, Mavathur R, Geertz M, Travers A, Muskhelishvili G (2006) Homeostatic regulation of supercoiling sensitivity coordinates transcription of the bacterial genome. EMBO Rep 7:710–715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Booker BM, Deng S, Higgins NP (2010) DNA topology of highly transcribed operons in Salmonella enterica serovar Typhimurium. Mol Microbiol 78:1348–1364

    Article  CAS  PubMed  Google Scholar 

  • Bordes P, Conter A, Morales V, Bouvier J, Kolb A, Gutierrez C (2003) DNA supercoiling contributes to disconnect sigmaS accumulation from sigmaS-dependent transcription in Escherichia coli. Mol Microbiol 48:561–571

    Article  CAS  PubMed  Google Scholar 

  • Bouyioukos C, Reverchon S, Képès F (2016) From multiple pathogenicity islands to a unique organized pathogenicity archipelago. Sci Rep 6:27978

    Article  PubMed  PubMed Central  Google Scholar 

  • Bracco L, Kotlarz D, Kolb A, Diekmann S, Buc H (1989) Synthetic curved DNA sequences can act as transcriptional activators in Escherichia coli. EMBO J 8:4289–4296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brambilla E, Sclavi B (2015) Gene regulation by H-NS as a function of growth conditions depends on chromosomal position in Escherichia coli. G3 (Bethesda) 5:605–614

    Article  CAS  Google Scholar 

  • Bryant JA, Sellars LE, Busby SJ, Lee DJ (2014) Chromosome position effects on gene expression in Escherichia coli K-12. Nucleic Acids Res 42:11383–11392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cameron ADS, Dillon SC, Kroger C, Beran L, Dorman CJ (2017) Broad-scale redistribution of mRNA abundance and transcriptional machinery in response to growth rate in Salmonella enterica serovar Typhimurium. Microbial Genom. https://doi.org/10.1099/mgen.0.000127

    Article  Google Scholar 

  • Carpentier A-S, Torresani B, Grossmann A, He´naut A (2005) Decoding the nucleoid organization of Bacillus subtilis and Escherichia coli through gene expression data. BMC Genom 6:84

    Article  CAS  Google Scholar 

  • Cevost J, Vaillant C, Meyer S (2017) ThreaDNA: predicting DNA mechanics’ contribution to sequence selectivity of proteins along whole genomes. Bioinformatics. https://doi.org/10.1093/bioinformatics

    Article  Google Scholar 

  • Chen B, Xiao Y, Liu C, Li C, Leng F (2010) DNA linking number change induced by sequence-specific DNA-binding proteins. Nucleic Acids Res 38:3643–3654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crisona NJ, Weinberg RL, Peter BJ, Sumners DW, Cozzarelli NR (1999) The topological mechanism of phage λ integrase. J Mol Biol 289:747–775

    Article  CAS  PubMed  Google Scholar 

  • Dame RT, Kalmykowa OJ, Grainger DC (2011) Chromosomal macrodomains and associated proteins: implications for DNA organization and replication in gram negative bacteria. PLoS Genet 7:e1002123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Del Campo C, Ignatova Z (2016) Probing dimensionality beyond the linear sequence of mRNA. Curr Genet 62:331–334

    Article  PubMed  CAS  Google Scholar 

  • Deng S, Stein RA, Higgins NP (2004) Transcription-induced barriers to supercoil diffusion in the Salmonella typhimurium chromosome. Proc Natl Acad Sci USA 101:3398–3403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding Y, Manzo C, Fulcrand G, Leng F, Dunlap D, Finzi L (2014) DNA supercoiling: a regulatory signal for the λ repressor. Proc Natl Acad Sci USA 111(43):15402–15407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dorman CJ (2006) DNA supercoiling and bacterial gene expression. Sci Prog 89:151–166

    Article  CAS  PubMed  Google Scholar 

  • Dorman CJ, Dorman MJ (2016) DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression. Biophys Rev 8:209–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drew HR, Weeks JR, Travers AA (1985) Negative supercoiling induces spontaneous unwinding of a bacterial promoter. EMBO J 4:1025–1032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duprey A, Muskhelishvili G, Reverchon S, Nasser W (2016) Temporal control of Dickeya dadantii main virulence gene expression by growth phase-dependent alteration of regulatory nucleoprotein complexes. Biochim Biophys Acta 1859:1470–1480

    Article  CAS  PubMed  Google Scholar 

  • Feijoo-Siota L, Rama JLR, Sánchez-Pérez A, Villa TG (2017) Considerations on bacterial nucleoids. Appl Microbiol Biotechnol 101:5591–5602

    Article  CAS  PubMed  Google Scholar 

  • Ferrándiz MJ, Martín-Galiano AJ, Arnanz C, Camacho-Soguero I, Tirado-Vélez JM, de la Campa AG (2016) An increase in negative supercoiling in bacteria reveals topology-reacting gene clusters and a homeostatic response mediated by the DNA topoisomerase I gene. Nucleic Acids Res 44:7292–7303

    PubMed  PubMed Central  Google Scholar 

  • Finzi L, Dunlap D (2016) Supercoiling biases the formation of loops involved in gene regulation. Biophys Rev 8:S65–S74

    Article  CAS  Google Scholar 

  • Fitzgerald S, Dillon SC, Chao TC, Wiencko HL, Hokamp K, Cameron AD, Dorman CJ (2015) Re-engineering cellular physiology by rewiring high-level global regulatory genes. Sci Rep 5:17653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fogg JM, Randall GL, Pettitt BM, Sumners DWL, Harris SA, Zechiedrich L (2012) Bullied no more: when and how DNA shoves proteins around. Q Rev Biophys 45:257–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fritsche M, Li S, Heermann DW, Wiggins PA (2012) A model for Escherichia coli chromosome packaging supports transcription factor-induced DNA domain formation. Nucleic Acids Res 40:972–980

    Article  CAS  PubMed  Google Scholar 

  • Fulcrand G, Zhi X, Leng F (2013) Transcription-coupled DNA supercoiling in defined protein systems and in E. coli topA mutant strains. IUBMB Life 65:615–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geertz M, Travers A, Mehandziska S, Janga SC, Shimamoto N, Muskhelishvili G (2011) Structural coupling between RNA polymerase composition and DNA supercoiling in coordinating transcription: a global role for the omega subunit? MBio 2(4) e00034–e00011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gerganova V, Berger M, Zaldastanishvili E, Sobetzko P, Lafon C, Mourez M, Travers A, Muskhelishvili G (2015a) Chromosomal position shift of a regulatory gene alters the bacterial phenotype. Nucl Acids Res 43:8215–8226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gerganova V, Maurer S, Stoliar L, Japaridze A, Nasser W, Kutateladze T, Travers A, Muskhelishvili G (2015b) Upstream binding of idling RNA polymerase modulates transcription initiation from a nearby promoter. J Biol Chem 290:8095–8109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilbert N, Allan J (2014) Supercoiling in DNA and chromatin. Curr Opin Genet Dev 25:15–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez-Gil G, Kahmann R, Muskhelishvili G (1998) Regulation of crp transcription by oscillation between distinct nucleoprotein complexes. EMBO J 17:2877–2885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grainger DC, Hurd D, Harrison M, Holdstock J, Busby SJ (2005) Studies of the distriution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc Natl Acad Sci USA 102:17693–17698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Güell M, van Noort V, Yus E, Chen WH, Leigh-Bell J, Michalodimitrakis K, Yamada T, Arumugam M, Doerks T, Kühner S, Rode M, Suyama M, Schmidt S, Gavin AC, Bork P, Serrano L (2009) Transcriptome complexity in a genome-reduced bacterium. Science 326:1268–1271

    Article  PubMed  CAS  Google Scholar 

  • Gummesson B, Magnusson LU, Lovmar M, Kvint K, Persson O, Ballesteros M, Farewell A, Nyström T (2009) Increased RNA polymerase availability directs resources towards growth at the expense of maintenance. EMBO J 28:2209–2219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hacker J, Kaper JB (2000) Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54:641–679

    Article  CAS  PubMed  Google Scholar 

  • Hanamura A, Aiba H (1991) Molecular mechanism of negative autoregulation of Escherichia coli crp gene. Nucleic Acids Res 19:4413–4419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hatfield GW, Benham CJ (2002) DNA topology-mediated control of global gene expression in Escherichia coli. Annu Rev Genet 36:175–203

    Article  CAS  PubMed  Google Scholar 

  • Hsieh LS, Burger RM, Drlica K (1991a) Bacterial DNA supercoiling and [ATP]/[ADP]. Changes associated with a transition to anaerobic growth. J Mol Biol 219:443–450

    Article  CAS  PubMed  Google Scholar 

  • Hsieh LS, Rouviere-Yaniv J, Drlica K (1991b) Bacterial DNA supercoiling and [ATP]/[ADP] ratio: changes associated with salt shock. J Bacteriol 173:3914–3917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huerta A, Francino MP, Morett E, Collado-Vides J (2006) Selection for unequal densities of σ70 promoter-like signals in different regions of large bacterial genomes. PLoS Genet 2:e185

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jacob F, Monod J (1961) Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 3:318–356

    Article  CAS  PubMed  Google Scholar 

  • Janga SC, Salgado H, Martínez-Antonio A (2009) Transcriptional regulation shapes the organization of genes on bacterial chromosomes. Nucleic Acids Res 37(11):3680–3688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Japaridze A, Muskhelishvili G, Benedetti F, Gavriilidou AF, Zenobi R, De Los Rios P, Longo G, Dietler G (2017a) Hyperplectonemes: a higher order compact and dynamic DNA self-organization. Nano Lett 17:1938–1948

    Article  CAS  PubMed  Google Scholar 

  • Japaridze A, Renevey S, Sobetzko P, Stoliar L, Nasser W, Dietler G, Muskhelishvili G (2017b) DNA sequence organization directs the assembly of various H-NS bridged filaments. J Biol Chem 292:7607–7618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong KS, Ahn J, Khodursky AB (2004) Spatial patterns of transcriptional activity in the chromosome of Escherichia coli. Genome Biol 5:R86

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang X, Sobetzko P, Nasser W, Reverchon S, Muskhelishvili G (2015) Chromosomal “stress-response” domains govern the spatiotemporal expression of the bacterial virulence program. mBio 6(3):e00353–e00315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang X, Zghidi-Abouzid O, Oger-Desfeux C, Hommais F, Greliche N, Muskhelishvili G, Nasser W, Reverchon S (2016) Global transcriptional response of Dickeya dadantii to environmental stimuli relevant to the plant infection. Environ Microbiol 18:3651–3672

    Article  CAS  PubMed  Google Scholar 

  • Junier I, Rivoire O (2016) Conserved units of co-expression in bacterial genomes: an evolutionary insight into transcriptional regulation. PLOS One 11:e0155740

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Junier I, Unal EB, Yus E, Lloréns-Rico V, Serrano L (2016) Insights into the mechanisms of basal coordination of transcription using a genome-reduced bacterium. Cell Syst 2:391–401

    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

    Article  CAS  PubMed  Google Scholar 

  • Képès F (2004) Periodic transcriptional organization of the E.coli genome. J Mol Biol 340:957–964

    Article  PubMed  CAS  Google Scholar 

  • Kouzine F, Wojtowicz D, Yamane A, Resch W, Kieffer-Kwon KR, Bandle R, Nelson S, Nakahashi H. Awasthi P. Feigenbaum L et al (2013a) Global regulation of promoter melting in naive lymphocytes. Cell 153:988–999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kouzine F, Gupta A, Baranello L, Wojtowicz D, Ben-Aissa K, Liu J, Przytycka TM, Levens D (2013b) Transcription-dependent dynamic supercoiling is a short-range genomic force. Nat Struct Mol Biol 20:396–403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kouzine F, Wojtowicz D, Baranello L, Yamane A, Nelson S, Resch W, Kieffer-Kwon KR, Benham CJ, Casellas R, Przytycka TM, Levens D (2017) Permanganate/S1 nuclease footprinting reveals non-B DNA structures with regulatory potential across a mammalian genome. Cell Syst 4:344–356.e7

    Article  CAS  PubMed  Google Scholar 

  • Kovács ÁT (2016) Bacterial differentiation via gradual activation of global regulators. Curr Genet 62:125–128

    Article  PubMed  CAS  Google Scholar 

  • Kuhlman TE, Cox EC (2012) Gene location and DNA density determine transcription factor distributions in Escherichia coli. Mol Syst Biol 8:610

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kusano S, Ding Q, Fujita N, Ishihama A (1996) Promoter selectivity of Escherichia coli RNA polymerase E sigma 70 and E sigma 38 holoenzymes. Effect of DNA supercoiling. J Biol Chem 271:1998–2004

    Article  CAS  PubMed  Google Scholar 

  • Lagomarsino MC, Espéli O, Junier I (2015) From structure to function of bacterial chromosomes: evolutionary perspectives and ideas for new experiments. FEBS Lett 589:2996–3004

    Article  CAS  PubMed  Google Scholar 

  • Lal A, Dhar A, Trostel A, Kouzine F, Seshasayee AS, Adhya S (2016) Genome scale patterns of supercoiling in a bacterial chromosome. Nat Commun 7:11055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le TB, Laub MT (2016) Transcription rate and transcript length drive formation of chromosomal interaction domain boundaries. EMBO J 35:1582–1595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leng F (2016) Protein-induced DNA linking number change by sequence-specific DNA binding proteins and its biological effects. Biophys Rev 8:197–207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leng F, McMacken R (2002) Potent stimulation of transcription-coupled DNA supercoiling by sequence-specific DNA-binding proteins. Proc Natl Acad Sci USA 99:9139–9144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lia G, Bensimon D, Croquette V, Allemand JF, Dunlap D, Lewis DE, Adhya S, Finzi L (2003) Supercoiling and denaturation in Gal repressor/heat unstable nucleoid protein (HU)-mediated DNA looping. Proc Natl Acad Sci USA 100:11373–11377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu LF, Wang JC (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci USA 84:7024–7027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Llopis PM, Jackson AF, Sliusarenko O et al (2010) Spatial organization of the flow of genetic information in bacteria. Nature 466:77–81

    Article  CAS  PubMed Central  Google Scholar 

  • Løbner-Olesen A, Marinus MG, Hansen FG (2003) Role of SeqA and Dam in Escherichia coli gene expression: a global/microarray analysis. Proc Natl Acad Sci USA 100:4672–4677

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • López-García P, Forterre P (1997) DNA topology in hyperthermophilic archaea: reference states and their variation with growth phase, growth temperature, and temperature stresses. Mol Microbiol 23:1267–1279

    Article  PubMed  Google Scholar 

  • Ma Q, Yin Y, Schell MA, Zhang H, Li G, Ying X (2013) Computational analyses of transcriptomic data reveal the dynamic organization of the Escherichia coli chromosome under different conditions. Nucl Acids Res 41:5595–5603

    Google Scholar 

  • Machné R, Murray DB (2012) The yin and yang of yeast transcription: elements of a global feedback system between metabolism and chromatin. PLoS One 7:e37906

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marr C, Geertz M, Hütt M, Muskhelishvili G (2008) Two distinct logical types of network control in gene expression profiles. BMC Syst Biol 2:18

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Martín-Galiano AJ, Ferrándiz MJ, de la Campa AG (2017) Bridging chromosomal architecture and pathophysiology of Streptococcus pneumoniae. Genome Biol Evol. https://doi.org/10.1093/gbe/evw299

    Article  PubMed  PubMed Central  Google Scholar 

  • Mathelier A, Carbone A (2010) Chromosomal periodicity and positional networks of genes in Escherichia coli. Mol Syst Biol 6:366

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mercier R, Petit MA, Schbath S, Robin S, El Karoui M et al (2008) The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135:475–485

    Article  CAS  PubMed  Google Scholar 

  • Meyer S, Beslon G (2014) Torsion-mediated interaction between adjacent genes. PloS Comput Biol 10:e1003785

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mooney RA, Davis SE, Peters JM, Rowland JL, Ansari AZ, Landick R (2009) Regulator trafficking on bacterial transcription units in vivo. Mol Cell 33:97–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muskhelishvili G, Travers A (2013) Integration of syntactic and semantic properties of the DNA code reveals chromosomes as thermodynamic machines converting energy into information. Cell Mol Life Sci 70:4555–4567

    Article  CAS  PubMed  Google Scholar 

  • Muskhelishvili G, Travers A (2014) Order from the order: how a spatiotemporal genetic program is encoded in a 2D genetic map of the bacterial chromosome. J Mol Microbiol Biotechnol 24:332–343

    Article  CAS  PubMed  Google Scholar 

  • Muskhelishvili G, Travers A (2016) The regulatory role of DNA supercoiling in nucleoprotein complex assembly and genetic activity. Biophys Rev 8:5–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muskhelishvili G, Travers AA, Heumann H, Kahmann R (1995) FIS and RNA polymerase form a specific nucleoprotein complex at a stable RNA promoter. EMBO J 14:1446–1452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muskhelishvili G, Buckle M, Heumann H, Kahmann R, Travers AA (1997) FIS activates sequential steps during transcription initiation at a stable RNA promoter. EMBO J 16:3655–3665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muskhelishvili G, Sobetzko P, Geertz M, Berger M (2010) General organisational principles of the transcriptional regulation system: a tree or a circle? Mol Biosyst 6:662–676

    Article  CAS  PubMed  Google Scholar 

  • Nasser W, Rochman M, Muskhelishvili G (2002) Transcriptional regulation of the fis operon involves a module of multiple coupled promoters. EMBO J 21:715–724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naughton C, Avlonitis N, Corless S, Prendergast JG, Mati IK, Eijk PP, Cockroft SL, Bradley M, Ylstra B, Gilbert N (2013) Transcription forms and remodels supercoiling domains unfolding large-scale chromatin structures. Nat Struct Mol Biol 20:387–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ni Bhriain N, Dorman CJ, Higgins CF (1996) An overlap between osmotic and anaerobic stress responses: a potential role for DNA supercoiling in the coordinate regulation of gene expression. Mol Microbiol 3:933–942

    Article  Google Scholar 

  • Nigatu D, Henkel W, Sobetzko P, Muskhelishvili G (2016) Relationship between digital information and thermodynamic stability in bacterial genomes. EURASIP J Bioinform Syst Biol 1:4

    Article  CAS  Google Scholar 

  • Noy A, Sutthibutpong T, Harris SA (2016) Protein DNA interactions in complex DNA topologies: expect the unexpected. Biophys Rev 8:S145–S155

    Article  CAS  Google Scholar 

  • Ouafa ZA, Reverchon S, Lautier T, Muskhelishvili G, Nasser W (2012) Bacterial nucleoid-associated proteins modulate the DNA supercoiling response of major virulence genes in the plant pathogen Dickeya dadantii. Nucleic Acids Res 40:4306–4319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peter BJ, Arsuaga J, Breier AM, Khodursky AB, Brown PO, Cozzarelli NR (2004) Genomic transcriptional response to loss of chromosomal supercoiling in Escherichia coli. Genome Biol 5:R87

    Article  PubMed  PubMed Central  Google Scholar 

  • Redder P (2016) How does sub-cellular localization affect the fate of bacterial mRNA? Current Genet 62:687–690

    Article  CAS  Google Scholar 

  • Reppas NB, Wade JT, Church GM, Struhl K (2006) The transition between transcriptional initiation and elongation in E. coli is highly variable and often rate limiting. Mol Cell 24:747–757

    Article  CAS  PubMed  Google Scholar 

  • Reverchon S, Sobetzko P, Nasser W, Muskhelishvili G (2015) Rethinking the bacterial genetic regulation. Biochem Anal Biochem 4:193

    Article  CAS  Google Scholar 

  • Rocha EP, Sekowska A, Danchin A (2000) Sulphur islands in the Escherichia coli genome: markers of the cell’s architecture? FEBS Lett 476:8–11

    Article  CAS  PubMed  Google Scholar 

  • Rochman M, Aviv M, Glaser G, Muskhelishvili G (2002) Promoter protection by a transcription factor acting as a local topological homeostat. EMBO reports 3:355–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samul R, Leng F (2007) Transcription-coupled hypernegative supercoiling of plasmid DNA by T7 RNA polymerase in Escherichia coli topoisomerase I-deficient strains. J Mol Biol 374:925–935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanchez-Romero MA, Busby SJ, Dyer NP, Ott S, Millard AD et al (2010) Dynamic distribution of SeqA protein across the chromosome of Escherichia coli K-12. mBio 1:e00012–e00010

    Article  PubMed  PubMed Central  Google Scholar 

  • Schneider R, Travers AA, Muskhelishvili G (1997) FIS regulates the bacterial growth phase-dependent topological transitions in DNA. Mol Microbiol 26:519–530

    Article  CAS  PubMed  Google Scholar 

  • Shavkunov KS, Masulis IS, Tutukina MN, Deev AA, Ozoline ON (2009) Gains and unexpected lessons from genomes-scale promoter mapping. Nucleic Acids Res 37:4914–4931

    Article  CAS  Google Scholar 

  • Sheridan SD, Benham CJ, Hatfield GW (1998) Activation of gene expression by a novel DNA structural transmission mechanism that requires supercoiling-induced DNA duplex destabilization in an upstream activating sequence. J Biol Chem 273:21298–21308

    Article  CAS  PubMed  Google Scholar 

  • Snoep JL, van der Weijden CC, Andersen HW, Westerhoff HV, Jensen PR (2002) DNA supercoiling in Escherichia coli is under tight and subtle homeostatic control, involving gene-expression and metabolic regulation of both topoisomerase I and DNA gyrase. Eur J Biochem 269:1662–1669

    Article  CAS  PubMed  Google Scholar 

  • Sobetzko P (2016) Transcription-coupled DNA supercoiling dictates the chromosomal arrangement of bacterial genes. Nucleic Acids Res 44:1514–1524

    Article  PubMed  PubMed Central  Google Scholar 

  • Sobetzko P, Travers A, Muskhelishvili G (2012) Gene order and chromosome dynamics coordinate gene expression during the bacterial growth cycle. Proc Nat Acad Sci USA 109:E42–E50

    Article  CAS  PubMed  Google Scholar 

  • Sobetzko P, Glinkowska M, Travers A, Muskhelishvili G (2013) DNA thermodynamic stability and supercoil dynamics determine the gene expression program during the bacterial growth cycle. Mol BioSyst 9:1643–1651

    Article  CAS  PubMed  Google Scholar 

  • Soler-Bistué A, Mondotte JA, Bland MJ, Val ME, Saleh MC, Mazel D (2015) Genomic location of the major ribosomal protein gene locus determines Vibrio cholerae global growth and infectivity. PLoS Genet 11:e1005156

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sonnenschein N, Hütt MT, Stoyan H, Stoyan D (2009) Ranges of control in the transcriptional regulation of Escherichia coli. BMC Syst Biol 3:119

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sonnenschein N, Geertz M, Muskhelishvili G, Hütt MT (2011) Analog regulation of metabolic demand. BMC Syst Biol 5:40

    Article  PubMed  PubMed Central  Google Scholar 

  • Stracy M, Lesterlin C, Garza de Leon F, Uphoff S, Zawadzki P, Kapanidis AN (2015) Live-cell superresolution microscopy reveals the organization of RNA polymerase in the bacterial nucleoid. Proc Natl Acad Sci USA 112:E4390–E4399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutthibutpong T, Matek C, Benham C, Slade GG, Noy A, Laughton C, K Doye JP, Louis AA, Harris SA (2016) Long-range correlations in the mechanics of small DNA circles under topological stress revealed by multi-scale simulation. Nucleic Acids Res 44:9121–9130

    CAS  PubMed  PubMed Central  Google Scholar 

  • Todolli S, Perez PJ, Clauvelin N, Olson WK (2017) Contributions of sequence to the higher-order structures of DNA. Biophys J 112:416–426

    Article  CAS  PubMed  Google Scholar 

  • Travers AA, Muskhelishvili G (1998) DNA microloops and microdomains—a general mechanism for transcription activation by torsional transmission. J Mol Biol 279:1027–1043

    Article  CAS  PubMed  Google Scholar 

  • Travers A, Muskhelishvili G (2005) DNA supercoiling—a global transcriptional regulator for enterobacterial growth? Nature Rev Microbiol 3:157–169

    Article  CAS  Google Scholar 

  • Travers A, Muskhelishvili G (2007) A common topology for bacterial and eukaryotic transcription initiation? EMBO rep 8:147–151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Travers AA, Muskhelishvili G (2015) DNA structure and function. FEBS J 282:2279–2295

    Article  CAS  PubMed  Google Scholar 

  • Travers AA, Muskhelishvili G, Thompson JMT (2012) DNA Information: from digital code to analogue structure. Philos Transact A Math Phys Eng Sci 370:2960–2986

    Article  CAS  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 

  • van Workum M, van Dooren SJ, Oldenburg N, Molenaar D, Jensen PR, Snoep JL, Westerhoff HV (1996) DNA supercoiling depends on the phosphorylation potential in Escherichia coli. Mol Microbiol 20:351–360

    Article  PubMed  Google Scholar 

  • Visweswariah SS, Busby SJW (2015) Evolution of bacterial transcription factors: how proteins take on new tasks, but do not always stop doing the old ones. Trends Microbiol 23:463–467

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Irobalieva RN, Chiu W, Schmid MF, Fogg JM, Zechiedrich L, Pettitt BM (2017) Influence of DNA sequence on the structure of minicircles under torsional stress. Nucleic Acids Res 45:7633–7642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei C, Price M (2003) Protecting the terminus: t-loops and telomere end-binding proteins. Cell Mol Life Sci 60:2283–2294

    Article  CAS  PubMed  Google Scholar 

  • Wei J, Czapla L, Grosner MA, Swigon D, Olson WK (2014) DNA topology confers sequence specificity to nonspecific architectural proteins. Proc Natl Acad Sci USA 111:16742–16747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Ames GF-L (1990) In Riley M, Drlica K (eds) The bacterial chromosome. American Society of Microbiology, Washington DC, pp 211–225

    Google Scholar 

  • Zhi X, Leng F (2013) Dependence of transcription-coupled DNA supercoiling on promoter strength in Escherichia coli topoisomerase I deficient strains. Gene 514:82–90

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Patrick Sobetzko for calculation of genomic melting energy distributions. G. M. thanks the Deutsche Forschungsgemeinschaft (DFG) for financial support (DFG grant MU 1549/11-1). This work was supported in part by the Invited Researcher Grant of INSA de Lyon to G. M. and by an INSA BQR 2016 Grant to S. M.

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Correspondence to Georgi Muskhelishvili.

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Communicated by M. Kupiec.

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Meyer, S., Reverchon, S., Nasser, W. et al. Chromosomal organization of transcription: in a nutshell. Curr Genet 64, 555–565 (2018). https://doi.org/10.1007/s00294-017-0785-5

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  • DOI: https://doi.org/10.1007/s00294-017-0785-5

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