DNA supercoiling differences in bacteria result from disparate DNA gyrase activation by polyamines

English version

Autoři: Alexandre Duprey ^aff001; Eduardo A. Groisman ^aff001
Působiště autorů: Department of Microbial Pathogenesis, Yale School of Medicine, New Haven, CT, United States of America ^aff001; Yale Microbial Sciences Institute, West Haven, CT, United States of America ^aff002
Vyšlo v časopise: DNA supercoiling differences in bacteria result from disparate DNA gyrase activation by polyamines. PLoS Genet 16(10): e32767. doi:10.1371/journal.pgen.1009085
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009085

Souhrn

DNA supercoiling is essential for all living cells because it controls all processes involving DNA. In bacteria, global DNA supercoiling results from the opposing activities of topoisomerase I, which relaxes DNA, and DNA gyrase, which compacts DNA. These enzymes are widely conserved, sharing >91% amino acid identity between the closely related species Escherichia coli and Salmonella enterica serovar Typhimurium. Why, then, do E. coli and Salmonella exhibit different DNA supercoiling when experiencing the same conditions? We now report that this surprising difference reflects disparate activation of their DNA gyrases by the polyamine spermidine and its precursor putrescine. In vitro, Salmonella DNA gyrase activity was sensitive to changes in putrescine concentration within the physiological range, whereas activity of the E. coli enzyme was not. In vivo, putrescine activated the Salmonella DNA gyrase and spermidine the E. coli enzyme. High extracellular Mg²⁺ decreased DNA supercoiling exclusively in Salmonella by reducing the putrescine concentration. Our results establish the basis for the differences in global DNA supercoiling between E. coli and Salmonella, define a signal transduction pathway regulating DNA supercoiling, and identify potential targets for antibacterial agents.

Klíčová slova:

DNA – Gel electrophoresis – Gene expression – Oat – Reproductive physiology – Salmonella – Salmonella typhimurium – DNA purification

Zdroje

1. Stuger R, Woldringh CL, Weijden CC van der, Vischer NOE, Bakker BM, Spanning RJM van, et al. DNA Supercoiling by Gyrase is Linked to Nucleoid Compaction. Mol Biol Rep. 2002;29:79–82. doi: 10.1023/a:1020318705894 12241080

2. Pruss GJ, Drlica K. DNA supercoiling and prokaryotic transcription. Cell. 1989;56:521–523. doi: 10.1016/0092-8674(89)90574-6 2645054

3. Dorman CJ. DNA supercoiling and transcription in bacteria: a two-way street. BMC Mol Cell Biol. 2019;20:26. doi: 10.1186/s12860-019-0211-6 31319794

4. Dunaway M, Ostrander EA. Local domains of supercoiling activate a eukaryotic promoter in vivo. Nature. 1993;361:746–748. doi: 10.1038/361746a0 8441472

5. Higgins NP. Measuring In Vivo Supercoil Dynamics and Transcription Elongation Rates in Bacterial Chromosomes. The Bacterial Nucleoid. Humana Press, New York, NY; 2017. pp. 17–27. doi: 10.1007/978-1-4939-7098-8_2 28842872

6. Benjamin KR, Abola PA, Kanaar R, Cozzarelli NR. Contributions of Supercoiling to Tn3 Resolvase and Phage Mu Gin Site-specific Recombination. J Mol Biol. 1996;256:50–65. doi: 10.1006/jmbi.1996.0067 8609613

7. Carteau S, Mouscadet JF, Goulaouic H, Subra F, Auclair C. Effect of Topoisomerase Inhibitors on the in Vitro HIV DNA Integration Reaction. Biochem Biophys Res Commun. 1993;192:1409–1414. doi: 10.1006/bbrc.1993.1573 8389550

8. Holmes VF, Cozzarelli NR. Closing the ring: Links between SMC proteins and chromosome partitioning, condensation, and supercoiling. Proc Natl Acad Sci. 2000;97:1322–1324. doi: 10.1073/pnas.040576797 10677457

9. Champoux JJ. DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem. 2001;70:369–413. doi: 10.1146/annurev.biochem.70.1.369 11395412

10. Pedro-Botet ML, Yu VL. Treatment strategies for Legionella infection. Expert Opin Pharmacother. 2009;10:1109–1121. doi: 10.1517/14656560902900820 19405787

11. Zechiedrich EL, Khodursky AB, Bachellier S, Schneider R, Chen D, Lilley DMJ, et al. Roles of Topoisomerases in Maintaining Steady-state DNA Supercoiling in Escherichia coli. J Biol Chem. 2000;275:8103–8113. doi: 10.1074/jbc.275.11.8103 10713132

12. Gilbert N, Allan J. Supercoiling in DNA and chromatin. Curr Opin Genet Dev. 2014;25:15–21. doi: 10.1016/j.gde.2013.10.013 24584092

13. Verma SC, Qian Z, Adhya SL. Architecture of the Escherichia coli nucleoid. PLoS Genet. 2019;15. doi: 10.1371/journal.pgen.1008456 31830036

14. Gellert M, Mizuuchi K, O’Dea MH, Nash HA. DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc Natl Acad Sci. 1976;73:3872–3876. doi: 10.1073/pnas.73.11.3872 186775

15. Shah P, Swiatlo E. A multifaceted role for polyamines in bacterial pathogens. Mol Microbiol. 2008;68:4–16. doi: 10.1111/j.1365-2958.2008.06126.x 18405343

16. Noble CG, Maxwell A. The Role of GyrB in the DNA Cleavage-religation Reaction of DNA Gyrase: A Proposed Two Metal-ion Mechanism. J Mol Biol. 2002;318:361–371. doi: 10.1016/S0022-2836(02)00049-9 12051843

17. Basu A, Parente AC, Bryant Z. Structural Dynamics and Mechanochemical Coupling in DNA Gyrase. J Mol Biol. 2016;428:1833–1845. doi: 10.1016/j.jmb.2016.03.016 27016205

18. Wang JC. Interaction between DNA and an Escherichia coli protein omega. J Mol Biol. 1971;55:523–533. doi: 10.1016/0022-2836(71)90334-2 4927945

19. Nitiss JL, Soans E, Rogojina A, Seth A, Mishina M. Topoisomerase Assays. Curr Protoc Pharmacol. 2012;CHAPTER: Unit3.3. doi: 10.1002/0471141755.ph0303s57 22684721

20. Tse-Dinh Y-C, Beran RK. Multiple promoters for transcription of the Escherichia coli DNA topoisomerase I gene and their regulation by DNA supercoiling. J Mol Biol. 1988;202:735–742. doi: 10.1016/0022-2836(88)90554-2 2845101

21. Michael AJ. Polyamines in Eukaryotes, Bacteria, and Archaea. J Biol Chem. 2016;291:14896–14903. doi: 10.1074/jbc.R116.734780 27268252

22. Gevrekci AÖ. The roles of polyamines in microorganisms. World J Microbiol Biotechnol. 2017;33:204. doi: 10.1007/s11274-017-2370-y 29080149

23. Igarashi K, Kashiwagi K. Polyamine Modulon in Escherichia coli: Genes Involved in the Stimulation of Cell Growth by Polyamines. J Biochem (Tokyo). 2006;139:11–16. doi: 10.1093/jb/mvj020 16428314

24. Tabor CW, Tabor H. Polyamines in microorganisms. Microbiol Mol Biol Rev. 1985;49:81–99.

25. Jung IL, Kim IG. Polyamines and Glutamate Decarboxylase-based Acid Resistance in Escherichia coli. J Biol Chem. 2003;278:22846–22852. doi: 10.1074/jbc.M212055200 12670930

26. Tkachenko AG, Akhova AV, Shumkov MS, Nesterova LY. Polyamines reduce oxidative stress in Escherichia coli cells exposed to bactericidal antibiotics. Res Microbiol. 2012;163:83–91. doi: 10.1016/j.resmic.2011.10.009 22138596

27. Brickman TJ, Armstrong SK. The ornithine decarboxylase gene odc is required for alcaligin siderophore biosynthesis in Bordetella spp.: putrescine is a precursor of alcaligin. J Bacteriol. 1996;178:54–60. doi: 10.1128/jb.178.1.54-60.1996 8550442

28. Jelsbak L, Thomsen LE, Wallrodt I, Jensen PR, Olsen JE. Polyamines Are Required for Virulence in Salmonella enterica Serovar Typhimurium. PLOS ONE. 2012;7:e36149. doi: 10.1371/journal.pone.0036149 22558361

29. Parra-Lopez C, Baer MT, Groisman EA. Molecular genetic analysis of a locus required for resistance to antimicrobial peptides in Salmonella typhimurium. EMBO J. 1993;12:4053–4062. 8223423

30. Rovinskiy NS, Agbleke AA, Chesnokova ON, Higgins NP. Supercoil Levels in E. coli and Salmonella Chromosomes Are Regulated by the C-Terminal 35–38 Amino Acids of GyrA. Microorganisms. 2019;7:81. doi: 10.3390/microorganisms7030081 30875939

31. Adeolu M, Alnajar S, Naushad S, Gupta RS. Genome based phylogeny and taxonomy of the “Enterobacteriales”: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol. 2016 [cited 22 Sep 2016]. Available: http://ijs.microbiologyresearch.org/content/journal/ijsem/10.1099/ijsem.0.001485?crawler=true

32. Webber MA, Buckner MMC, Redgrave LS, Ifill G, Mitchenall LA, Webb C, et al. Quinolone-resistant gyrase mutants demonstrate decreased susceptibility to triclosan. J Antimicrob Chemother. 2017;72:2755–2763. doi: 10.1093/jac/dkx201 29091182

33. Champion K, Higgins NP. Growth Rate Toxicity Phenotypes and Homeostatic Supercoil Control Differentiate Escherichia coli from Salmonella enterica Serovar Typhimurium. J Bacteriol. 2007;189:5839–5849. doi: 10.1128/JB.00083-07 17400739

34. Vetcher AA, McEwen AE, Abujarour R, Hanke A, Levene SD. Gel mobilities of linking-number topoisomers and their dependence on DNA helical repeat and elasticity. Biophys Chem. 2010;148:104–111. doi: 10.1016/j.bpc.2010.02.016 20346570

35. Tabor CW, Tabor H, Xie QW. Spermidine synthase of Escherichia coli: localization of the speE gene. Proc Natl Acad Sci. 1986;83:6040–6044. doi: 10.1073/pnas.83.16.6040 3526348

36. Charlier D, Bervoets I. Regulation of arginine biosynthesis, catabolism and transport in Escherichia coli. Amino Acids. 2019;51:1103–1127. doi: 10.1007/s00726-019-02757-8 31267155

37. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, et al. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature. 2001;413:852–856. doi: 10.1038/35101614 11677609

38. Sugiyama Y, Nakamura A, Matsumoto M, Kanbe A, Sakanaka M, Higashi K, et al. A Novel Putrescine Exporter SapBCDF of Escherichia coli. J Biol Chem. 2016;291:26343–26351. doi: 10.1074/jbc.M116.762450 27803167

39. Husna AU, Wang N, Cobbold SA, Newton HJ, Hocking DM, Wilksch JJ, et al. Methionine biosynthesis and transport are functionally redundant for the growth and virulence of Salmonella Typhimurium. J Biol Chem. 2018; jbc.RA118.002592. doi: 10.1074/jbc.RA118.002592 29720401

40. Alatossava T, Jütte H, Kuhn A, Kellenberger E. Manipulation of intracellular magnesium content in polymyxin B nonapeptide-sensitized Escherichia coli by ionophore A23187. J Bacteriol. 1985;162:413–419. doi: 10.1128/JB.162.1.413-419.1985 2984182

41. Fang S-B, Huang C-J, Huang C-H, Wang K-C, Chang N-W, Pan H-Y, et al. speG Is Required for Intracellular Replication of Salmonella in Various Human Cells and Affects Its Polyamine Metabolism and Global Transcriptomes. Front Microbiol. 2017;8. doi: 10.3389/fmicb.2017.02245 29187844

42. Miyamoto S, Kashiwagi K, Ito K, Watanabe S, Igarashi K. Estimation of Polyamine Distribution and Polyamine Stimulation of Protein Synthesis in Escherichia coli. Arch Biochem Biophys. 1993;300:63–68. doi: 10.1006/abbi.1993.1009 7678729

43. Romani AM, Scarpa A. Regulation of cellular magnesium. Front Biosci J Virtual Libr. 2000;5:D720–734. doi: 10.2741/romani 10922296

44. Rowatt E, Williams RJP. The binding of polyamines and magnesium to DNA. J Inorg Biochem. 1992;46:87–97. doi: 10.1016/0162-0134(92)80012-k 1522415

45. Kongsoi S, Yokoyama K, Suprasert A, Utrarachkij F, Nakajima C, Suthienkul O, et al. Characterization of Salmonella Typhimurium DNA gyrase as a target of quinolones. Drug Test Anal. 2015;7:714–720. doi: 10.1002/dta.1744 25381884

46. Workum M, Dooren SJ, Oldenburg N, Molenaar D, Jensen PR, Snoep JL, et al. DNA supercoiling depends on the phosphorylation potential in Escherichia coli. Mol Microbiol. 1996;20:351–360. doi: 10.1111/j.1365-2958.1996.tb02622.x 8733233

47. Kurihara S, Suzuki H, Oshida M, Benno Y. A Novel Putrescine Importer Required for Type 1 Pili-driven Surface Motility Induced by Extracellular Putrescine in Escherichia coli K-12. J Biol Chem. 2011;286:10185–10192. doi: 10.1074/jbc.M110.176032 21266585

48. Michael AJ. Polyamine function in archaea and bacteria. J Biol Chem. 2018; jbc.TM118.005670. doi: 10.1074/jbc.TM118.005670 30254075

49. Duprey A, Reverchon S, Nasser W. Bacterial virulence and Fis: adapting regulatory networks to the host environment. Trends Microbiol. 2014;22:92–99. doi: 10.1016/j.tim.2013.11.008 24370464

50. Colgan AM, Quinn HJ, Kary SC, Mitchenall LA, Maxwell A, Cameron ADS, et al. Negative supercoiling of DNA by gyrase is inhibited in Salmonella enterica serovar Typhimurium during adaptation to acid stress. Mol Microbiol. 2018;107:734–746. doi: 10.1111/mmi.13911 29352745

51. Pomares MF, Corbalán NS, Adler C, de Cristóbal R, Farías RN, Delgado MA, et al. Macrophage environment turns otherwise MccJ25-resistant Salmonella into sensitive. BMC Microbiol. 2013;13:95. doi: 10.1186/1471-2180-13-95 23634875

52. Duprey A, Nasser W, Léonard S, Brochier-Armanet C, Reverchon S. Transcriptional start site turnover in the evolution of bacterial paralogous genes–the pelE-pelD virulence genes in Dickeya. FEBS J. 2016;283:4192–4207. doi: 10.1111/febs.13921 27727510

53. Chen HD, Jewett MW, Groisman EA. Ancestral Genes Can Control the Ability of Horizontally Acquired Loci to Confer New Traits. PLOS Genet. 2011;7:e1002184. doi: 10.1371/journal.pgen.1002184 21811415

54. Maxwell A. DNA gyrase as a drug target. Trends Microbiol. 1997;5:102–109. doi: 10.1016/S0966-842X(96)10085-8 9080608

55. Rubinstein E. History of Quinolones and Their Side Effects. Chemotherapy. 2001;47:3–8. doi: 10.1159/000057838 11549783

56. WHO Advisory Group on Integrated Surveillance of Antimicrobial Resistance, World Health Organization. Critically important antimicrobials for human medicine: ranking of antimicrobial agents for risk management of antimicrobial resistance due to non-human use. 2017. Available: http://apps.who.int/iris/bitstream/10665/255027/1/9789241512220-eng.pdf

57. Shapiro A, Jahic H, Prasad S, Ehmann D, Thresher J, Gao N, et al. A Homogeneous, High-Throughput Fluorescence Anisotropy-Based DNA Supercoiling Assay. J Biomol Screen. 2010;15:1088–1098. doi: 10.1177/1087057110378624 20930214

58. Galán JE, Curtiss R. Expression of Salmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling. Infect Immun. 1990;58:1879–1885. doi: 10.1128/IAI.58.6.1879-1885.1990 2160435

59. Ó Cróinín T, Carroll RK, Kelly A, Dorman CJ. Roles for DNA supercoiling and the Fis protein in modulating expression of virulence genes during intracellular growth of Salmonella enterica serovar Typhimurium. Mol Microbiol. 2006;62:869–882. doi: 10.1111/j.1365-2958.2006.05416.x 16999831

60. Datta S, Costantino N, Court DL. A set of recombineering plasmids for gram-negative bacteria. Gene. 2006;379:109–115. doi: 10.1016/j.gene.2006.04.018 16750601

61. Davis RW, Botstein D, Roth JR. Advanced Bacterial Genetics: A Manual for Genetic Engineering. Cold Spring Harbor, N.Y: Cold Spring Harbor Laboratory Pr; 1980.

62. Snavely MD, Miller CG, Maguire ME. The mgtB Mg2+ transport locus of Salmonella typhimurium encodes a P-type ATPase. J Biol Chem. 1991;266:815–823. 1824701

63. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–359. doi: 10.1038/nmeth.1923 22388286

64. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7:562–578. doi: 10.1038/nprot.2012.016 22383036

65. Carvajal N, López V, Salas M, Uribe E, Herrera P, Cerpa J. Manganese Is Essential for Catalytic Activity ofEscherichia coliAgmatinase. Biochem Biophys Res Commun. 1999;258:808–811. doi: 10.1006/bbrc.1999.0709 10329468

66. Ngo TT, Brillhart KL, Davis RH, Wong RC, Bovaird JH, Digangi JJ, et al. Spectrophotometric assay for ornithine decarboxylase. Anal Biochem. 1987;160:290–293. doi: 10.1016/0003-2697(87)90049-2 3578755

Článek Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots

Článek A single Ho-induced double-strand break at the MAT locus is lethal in Candida glabrata

Článek A Rad51-independent pathway promotes single-strand template repair in gene editing

Článek Novel loci for childhood body mass index and shared heritability with adult cardiometabolic traits

Článek C. elegans CLASP/CLS-2 negatively regulates membrane ingression throughout the oocyte cortex and is required for polar body extrusion

Článek The O-GlcNAc transferase OGT is a conserved and essential regulator of the cellular and organismal response to hypertonic stress

Článek Drosophila phosphatidylinositol-4 kinase fwd promotes mitochondrial fission and can suppress Pink1/parkin phenotypes

Článek A new domestic cat genome assembly based on long sequence reads empowers feline genomic medicine and identifies a novel gene for dwarfism

Článek Chromosome separation during Drosophila male meiosis I requires separase-mediated cleavage of the homolog conjunction protein UNO

Článek How noncrossover homologs are conjoined and segregated in Drosophila male meiosis I: Stable but reversible homolog linkers require a novel Separase target protein

Článek Predominance of positive epistasis among drug resistance-associated mutations in HIV-1 protease

Článek Human ABCB1 with an ABCB11-like degenerate nucleotide binding site maintains transport activity by avoiding nucleotide occlusion