1887

Abstract

We have investigated the connection between the four-dimensional architecture of the bacterial nucleoid and the organism's global gene expression programme. By localizing the transcription machinery and the transcriptional outputs across the genome of the model bacterium Salmonella enterica serovar Typhimurium at different stages of the growth cycle, a surprising disconnection between gene dosage and transcriptional output was revealed. During exponential growth, gene output occurred chiefly in the Ori (origin), Ter (terminus) and NSL (non-structured left) domains, whereas the Left macrodomain remained transcriptionally quiescent at all stages of growth. The apparently high transcriptional output in Ter was correlated with an enhanced stability of the RNA expressed there during exponential growth, suggesting that longer mRNA half-lives compensate for low gene dosage. During exponential growth, RNA polymerase (RNAP) was detected everywhere, whereas in stationary phase cells, RNAP was concentrated in the Ter macrodomain. The alternative sigma factors RpoE, RpoH and RpoN were not required to drive transcription in these growth conditions, consistent with their observed binding to regions away from RNAP and regions of active transcription. Specifically, these alternative sigma factors were found in the Ter macrodomain during exponential growth, whereas they were localized at the Ori macrodomain in stationary phase.

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2017-08-04
2019-10-14
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References

  1. Sobetzko P, Travers A, Muskhelishvili G. Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle. Proc Natl Acad Sci USA 2012;109:E42E50 [CrossRef][PubMed]
    [Google Scholar]
  2. Dorman CJ. Genome architecture and global gene regulation in bacteria: making progress towards a unified model?. Nat Rev Microbiol 2013;11:349–355 [CrossRef][PubMed]
    [Google Scholar]
  3. Berlatzky IA, Rouvinski A, Ben-Yehuda S. Spatial organization of a replicating bacterial chromosome. Proc Natl Acad Sci USA 2008;105:14136–14140 [CrossRef][PubMed]
    [Google Scholar]
  4. Janga SC, Salgado H, Martínez-Antonio A. Transcriptional regulation shapes the organization of genes on bacterial chromosomes. Nucleic Acids Res 2009;37:3680–3688 [CrossRef][PubMed]
    [Google Scholar]
  5. Jeong KS, Ahn J, Khodursky AB. Spatial patterns of transcriptional activity in the chromosome of Escherichia coli. Genome Biol 2004;5:R86 [CrossRef][PubMed]
    [Google Scholar]
  6. Junier I, Rivoire O. Conserved units of co-expression in bacterial genomes: an evolutionary insight into transcriptional regulation. PLoS One 2016;11:e0155740 [CrossRef][PubMed]
    [Google Scholar]
  7. Junier I, Hérisson J, Képès F. Genomic organization of evolutionarily correlated genes in bacteria: limits and strategies. J Mol Biol 2012;419:369–386 [CrossRef][PubMed]
    [Google Scholar]
  8. Képès F. Periodic transcriptional organization of the E. coli genome. J Mol Biol 2004;340:957–964 [CrossRef][PubMed]
    [Google Scholar]
  9. Mathelier A, Carbone A. Chromosomal periodicity and positional networks of genes in Escherichia coli. Mol Syst Biol 2010;6:366 [CrossRef][PubMed]
    [Google Scholar]
  10. Wright MA, Kharchenko P, Church GM, Segrè D. Chromosomal periodicity of evolutionarily conserved gene pairs. Proc Natl Acad Sci USA 2007;104:10559–10564 [CrossRef][PubMed]
    [Google Scholar]
  11. Chowdhury C, Chun S, Sawaya MR, Yeates TO, Bobik TA. The function of the PduJ microcompartment shell protein is determined by the genomic position of its encoding gene. Mol Microbiol 2016;101:770–783 [CrossRef][PubMed]
    [Google Scholar]
  12. Fitzgerald S, Dillon SC, Chao TC, Wiencko HL, Hokamp K et al. Re-engineering cellular physiology by rewiring high-level global regulatory genes. Sci Rep 2015;5:17653 [CrossRef][PubMed]
    [Google Scholar]
  13. Hudson RE, Bergthorsson U, Roth JR, Ochman H. Effect of chromosome location on bacterial mutation rates. Mol Biol Evol 2002;19:85–92 [CrossRef][PubMed]
    [Google Scholar]
  14. Mira A, Ochman H. Gene location and bacterial sequence divergence. Mol Biol Evol 2002;19:1350–1358 [CrossRef][PubMed]
    [Google Scholar]
  15. Pavitt GD, Higgins CF. Chromosomal domains of supercoiling in Salmonella typhimurium. Mol Microbiol 1993;10:685–696 [CrossRef][PubMed]
    [Google Scholar]
  16. Schmid MB, Roth JR. Gene location affects expression level in Salmonella typhimurium. J Bacteriol 1987;169:2872–2875 [CrossRef][PubMed]
    [Google Scholar]
  17. Sharp PM, Shields DC, Wolfe KH, Li WH. Chromosomal location and evolutionary rate variation in enterobacterial genes. Science 1989;246:808–810 [CrossRef][PubMed]
    [Google Scholar]
  18. Jacobsen A, Hendriksen RS, Aaresturp FM, Ussery DW, Friis C. The Salmonella enterica pan-genome. Microb Ecol 2011;62:487–504 [CrossRef][PubMed]
    [Google Scholar]
  19. Garcia-Russell N, Harmon TG, Le TQ, Amaladas NH, Mathewson RD et al. Unequal access of chromosomal regions to each other in Salmonella: probing chromosome structure with phage lambda integrase-mediated long-range rearrangements. Mol Microbiol 2004;52:329–344 [CrossRef][PubMed]
    [Google Scholar]
  20. Garcia-Russell N, Orchard SS, Segall AM. Probing nucleoid structure in bacteria using phage lambda integrase-mediated chromosome rearrangements. Methods Enzymol 2007;421:209–226 [CrossRef][PubMed]
    [Google Scholar]
  21. Niki H, Yamaichi Y, Hiraga S. Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev 2000;14:212–223[PubMed]
    [Google Scholar]
  22. Rebollo JE, François V, Louarn JM. Detection and possible role of two large nondivisible zones on the Escherichia coli chromosome. Proc Natl Acad Sci USA 1988;85:9391–9395 [CrossRef][PubMed]
    [Google Scholar]
  23. Rocha EP. The organization of the bacterial genome. Annu Rev Genet 2008;42:211–233 [CrossRef][PubMed]
    [Google Scholar]
  24. Valens M, Penaud S, Rossignol M, Cornet F, Boccard F. Macrodomain organization of the Escherichia coli chromosome. EMBO J 2004;23:4330–4341 [CrossRef][PubMed]
    [Google Scholar]
  25. Esnault E, Valens M, Espéli O, Boccard F. Chromosome structuring limits genome plasticity in Escherichia coli. PLoS Genet 2007;3:e226 [CrossRef][PubMed]
    [Google Scholar]
  26. Messerschmidt SJ, Waldminghaus T. Dynamic organization: chromosome domains in Escherichia coli. J Mol Microbiol Biotechnol 2014;24:301–315 [CrossRef][PubMed]
    [Google Scholar]
  27. Couturier E, Rocha EP. Replication-associated gene dosage effects shape the genomes of fast-growing bacteria but only for transcription and translation genes. Mol Microbiol 2006;59:1506–1518 [CrossRef][PubMed]
    [Google Scholar]
  28. Lesterlin C, Mercier R, Boccard F, Barre FX, Cornet F. Roles for replichores and macrodomains in segregation of the Escherichia coli chromosome. EMBO Rep 2005;6:557–562 [CrossRef][PubMed]
    [Google Scholar]
  29. Reyes-Lamothe R, Wang X, Sherratt D. Escherichia coli and its chromosome. Trends Microbiol 2008;16:238–245 [CrossRef][PubMed]
    [Google Scholar]
  30. Bryant JA, Sellars LE, Busby SJ, Lee DJ. Chromosome position effects on gene expression in Escherichia coli K-12. Nucleic Acids Res 2014;42:11383–11392 [CrossRef][PubMed]
    [Google Scholar]
  31. Gerganova V, Berger M, Zaldastanishvili E, Sobetzko P, Lafon C et al. Chromosomal position shift of a regulatory gene alters the bacterial phenotype. Nucleic Acids Res 2015;43:8215–8226 [CrossRef][PubMed]
    [Google Scholar]
  32. Jiang X, Sobetzko P, Nasser W, Reverchon S, Muskhelishvili G. Chromosomal "stress-response" domains govern the spatiotemporal expression of the bacterial virulence program. MBio 2015;6:e00353-15 [CrossRef][PubMed]
    [Google Scholar]
  33. Lal A, Dhar A, Trostel A, Kouzine F, Seshasayee ASN et al. Genome scale patterns of supercoiling in a bacterial chromosome. Nat Commun 2016;7:11055 [CrossRef][PubMed]
    [Google Scholar]
  34. Pomerantz RT, O'Donnell M. Direct restart of a replication fork stalled by a head-on RNA polymerase. Science 2010;327:590–592 [CrossRef][PubMed]
    [Google Scholar]
  35. Rocha EP, Danchin A. Essentiality, not expressiveness, drives gene-strand bias in bacteria. Nat Genet 2003;34:377–378 [CrossRef][PubMed]
    [Google Scholar]
  36. Montero Llopis P, Jackson AF, Sliusarenko O, Surovtsev I, Heinritz J et al. Spatial organization of the flow of genetic information in bacteria. Nature 2010;466:77–81 [CrossRef][PubMed]
    [Google Scholar]
  37. Parry BR, Surovtsev IV, Cabeen MT, O'Hern CS, Dufresne ER et al. The bacterial cytoplasm has glass-like properties and is fluidized by metabolic activity. Cell 2014;156:183–194 [CrossRef][PubMed]
    [Google Scholar]
  38. Kröger C, Dillon SC, Cameron AD, Papenfort K, Sivasankaran SK et al. The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc Natl Acad Sci USA 2012;109:E1277E1286 [CrossRef][PubMed]
    [Google Scholar]
  39. Kröger C, Colgan A, Srikumar S, Händler K, Sivasankaran SK et al. An infection-relevant transcriptomic compendium for Salmonella enterica serovar Typhimurium. Cell Host Microbe 2013;14:683–695 [CrossRef][PubMed]
    [Google Scholar]
  40. Sezonov G, Joseleau-Petit D, D'Ari R. Escherichia coli physiology in Luria-Bertani broth. J Bacteriol 2007;189:8746–8749 [CrossRef][PubMed]
    [Google Scholar]
  41. Dillon SC, Cameron AD, Hokamp K, Lucchini S, Hinton JC et al. Genome-wide analysis of the H-NS and Sfh regulatory networks in Salmonella Typhimurium identifies a plasmid-encoded transcription silencing mechanism. Mol Microbiol 2010;76:1250–1265 [CrossRef][PubMed]
    [Google Scholar]
  42. Klumpp S, Zhang Z, Hwa T. Growth rate-dependent global effects on gene expression in bacteria. Cell 2009;139:1366–1375 [CrossRef][PubMed]
    [Google Scholar]
  43. Bipatnath M, Dennis PP, Bremer H. Initiation and velocity of chromosome replication in Escherichia coli B/r and K-12. J Bacteriol 1998;180:265–273[PubMed]
    [Google Scholar]
  44. Lucchini S, Rowley G, Goldberg MD, Hurd D, Harrison M et al. H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog 2006;2:e81 [CrossRef][PubMed]
    [Google Scholar]
  45. Bernstein JA, Khodursky AB, Lin PH, Lin-Chao S, Cohen SN. Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays. Proc Natl Acad Sci USA 2002;99:9697–9702 [CrossRef][PubMed]
    [Google Scholar]
  46. Grainger DC, Aiba H, Hurd D, Browning DF, Busby SJ. Transcription factor distribution in Escherichia coli: studies with FNR protein. Nucleic Acids Res 2007;35:269–278 [CrossRef][PubMed]
    [Google Scholar]
  47. Peano C, Wolf J, Demol J, Rossi E, Petiti L et al. Characterization of the Escherichia coli σs core regulon by chromatin immunoprecipitation-sequencing (ChIP-seq) analysis. Sci Rep 2015;5:10469 [CrossRef][PubMed]
    [Google Scholar]
  48. Patrick M, Dennis PP, Ehrenberg M, Bremer H. Free RNA polymerase in Escherichia coli. Biochimie 2015;119:80–91 [CrossRef][PubMed]
    [Google Scholar]
  49. Feklístov A, Sharon BD, Darst SA, Gross CA. Bacterial sigma factors: a historical, structural, and genomic perspective. Annu Rev Microbiol 2014;68:357–376 [CrossRef][PubMed]
    [Google Scholar]
  50. Bush M, Dixon R. The role of bacterial enhancer binding proteins as specialized activators of σ54-dependent transcription. Microbiol Mol Biol Rev 2012;76:497–529 [CrossRef][PubMed]
    [Google Scholar]
  51. Zhang N, Buck M. A perspective on the enhancer dependent bacterial RNA polymerase. Biomolecules 2015;5:1012–1019 [CrossRef][PubMed]
    [Google Scholar]
  52. Buck M, Cannon W. Specific binding of the transcription factor σ54 to promoter DNA. Nature 1992;358:422–424 [CrossRef][PubMed]
    [Google Scholar]
  53. Hartman CE, Samuels DJ, Karls AC. Modulating Salmonella Typhimurium's response to a changing environment through bacterial enhancer-binding proteins and the RpoN regulon. Front Mol Biosci 2016;3:41 [CrossRef][PubMed]
    [Google Scholar]
  54. Samuels DJ, Frye JG, Porwollik S, Mcclelland M, Mrázek J et al. Use of a promiscuous, constitutively-active bacterial enhancer-binding protein to define the σ54 (RpoN) regulon of Salmonella Typhimurium LT2. BMC Genomics 2013;14:602 [CrossRef][PubMed]
    [Google Scholar]
  55. Skovierova H, Rowley G, Rezuchova B, Homerova D, Lewis C et al. Identification of the σE regulon of Salmonella enterica serovar Typhimurium. Microbiology 2006;152:1347–1359 [CrossRef][PubMed]
    [Google Scholar]
  56. Nonaka G, Blankschien M, Herman C, Gross CA, Rhodius VA. Regulon and promoter analysis of the E. coli heat-shock factor, σ32, reveals a multifaceted cellular response to heat stress. Genes Dev 2006;20:1776–1789 [CrossRef][PubMed]
    [Google Scholar]
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