1887

Abstract

The flagellar system in K12 is expressed under the control of the -encoded master regulator FlhDC. Transposition of insertion sequence (IS) elements to the upstream promoter region up-regulates transcription of this operon, resulting in a more rapid motility. Wang and Wood ( 2011;5:1517–1525) provided evidence that insertion of IS into upstream activating sites occurs at higher rates in semi-solid agar media in which swarming behaviour is allowed as compared with liquid or solid media where swarming cannot occur. We confirm this conclusion and show that three IS elements, IS, IS and IS, transpose to multiple upstream sites within a 370 bp region of the operon control region. Hot spots for IS insertion correlate with positions of stress-induced DNA duplex destabilization (SIDD). We show that IS insertion occurs at maximal rates in 0.24 % agar, with rates decreasing dramatically with increasing or decreasing agar concentrations. In mixed cultures, we show that these mutations preferentially arise from the wild-type parent at frequencies of up to 3×10 cell day when the inoculated parental and co-existing IS-activated mutant cells are entering the stationary growth phase. We rigorously show that the apparent increased mutation frequencies cannot be accounted for by increased swimming or by increased growth under the selective conditions used. Thus, our data are consistent with the possibility that appropriate environmental conditions, namely those that permit but hinder flagellar rotation, result in the activation of a mutational pathway that involves IS element insertion upstream of the operon.

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2017-04-01
2020-01-24
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References

  1. Muñoz-Lopez M, Vilar-Astasio R, Tristan-Ramos P, Lopez-Ruiz C, Garcia-Pérez JL. Study of transposable elements and their genomic impact. Methods Mol Biol 2016;1400:1–19 [CrossRef][PubMed]
    [Google Scholar]
  2. Blot M. Transposable elements and adaptation of host bacteria. Genetica 1994;93:5–12 [CrossRef][PubMed]
    [Google Scholar]
  3. Bonchev G, Parisod C. Transposable elements and microevolutionary changes in natural populations. Mol Ecol Resour 2013;13:765–775 [CrossRef][PubMed]
    [Google Scholar]
  4. Zhang Z, Saier MH Jr. Transposon-mediated adaptive and directed mutations and their potential evolutionary benefits. J Mol Microbiol Biotechnol 2011;21:59–70 [CrossRef][PubMed]
    [Google Scholar]
  5. Derbyshire KM, Grindley ND. Replicative and conservative transposition in bacteria. Cell 1986;47:325–327 [CrossRef][PubMed]
    [Google Scholar]
  6. Haniford DB, Ellis MJ. Transposons Tn10 and Tn5. Microbiol Spectr 2015;3:MDNA3-0002-2014 [CrossRef][PubMed]
    [Google Scholar]
  7. Skipper KA, Andersen PR, Sharma N, Mikkelsen JG. DNA transposon-based gene vehicles – scenes from an evolutionary drive. J Biomed Sci 2013;20:92 [CrossRef][PubMed]
    [Google Scholar]
  8. Chandler M, Fayet O, Rousseau P, Ton Hoang B, Duval-Valentin G. Copy-out–paste-in transposition of IS911: a major transposition pathway. Microbiol Spectr 2015;3: [CrossRef][PubMed]
    [Google Scholar]
  9. Sousa A, Bourgard C, Wahl LM, Gordo I. Rates of transposition in Escherichia coli. Biol Lett 2013;9:20130838 [CrossRef][PubMed]
    [Google Scholar]
  10. Zhang Z, Yen MR, Saier MH Jr. Precise excision of IS5 from the intergenic region between the fucPIK and the fucAO operons and mutational control of fucPIK operon expression in Escherichia coli. J Bacteriol 2010;192:2013–2019 [CrossRef][PubMed]
    [Google Scholar]
  11. Ziebuhr W, Krimmer V, Rachid S, Lössner I, Götz F et al. A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256. Mol Microbiol 1999;32:345–356 [CrossRef][PubMed]
    [Google Scholar]
  12. Siguier P, Gourbeyre E, Chandler M. Bacterial insertion sequences: their genomic impact and diversity. FEMS Microbiol Rev 2014;38:865–891 [CrossRef][PubMed]
    [Google Scholar]
  13. Gaffé J, Mckenzie C, Maharjan RP, Coursange E, Ferenci T et al. Insertion sequence-driven evolution of Escherichia coli in chemostats. J Mol Evol 2011;72:398–412 [CrossRef][PubMed]
    [Google Scholar]
  14. Bonnefoy V, Fons M, Ratouchniak J, Pascal MC, Chippaux M. Aerobic expression of the nar operon of Escherichia coli in a fnr mutant. Mol Microbiol 1988;2:419–425 [CrossRef][PubMed]
    [Google Scholar]
  15. Sawers RG. Expression of fnr is constrained by an upstream IS5 insertion in certain Escherichia coli K-12 strains. J Bacteriol 2005;187:2609–2617 [CrossRef][PubMed]
    [Google Scholar]
  16. Li B, Li N, Wang F, Guo L, Huang Y et al. Structural insight of a concentration-dependent mechanism by which YdiV inhibits Escherichia coli flagellum biogenesis and motility. Nucleic Acids Res 2012;40:11073–11085 [CrossRef][PubMed]
    [Google Scholar]
  17. Lee C, Park C. Mutations upregulating the flhDC operon of Escherichia coli K-12. J Microbiol 2013;51:140–144 [CrossRef][PubMed]
    [Google Scholar]
  18. Chen YM, Lu Z, Lin EC. Constitutive activation of the fucAO operon and silencing of the divergently transcribed fucPIK operon by an IS5 element in Escherichia coli mutants selected for growth on l-1,2-propanediol. J Bacteriol 1989;171:6097–6105 [CrossRef][PubMed]
    [Google Scholar]
  19. Hall BG. Activation of the bgl operon by adaptive mutation. Mol Biol Evol 1998;15:1–5 [CrossRef][PubMed]
    [Google Scholar]
  20. Barker CS, Prüss BM, Matsumura P. Increased motility of Escherichia coli by insertion sequence element integration into the regulatory region of the flhD operon. J Bacteriol 2004;186:7529–7537 [CrossRef][PubMed]
    [Google Scholar]
  21. Saier MH Jr, Zhang Z. Transposon-mediated directed mutation controlled by DNA binding proteins in Escherichia coli. Front Microbiol 2014;5:390 [CrossRef][PubMed]
    [Google Scholar]
  22. Saier MH Jr, Zhang Z. Control of transposon-mediated directed mutation by the Escherichia coli phosphoenolpyruvate:sugar phosphotransferase system. J Mol Microbiol Biotechnol 2015;25:226–233 [CrossRef][PubMed]
    [Google Scholar]
  23. Zhang Z, Saier MH Jr. A novel mechanism of transposon- mediated gene activation. PLoS Genet 2009;5:e1000689 [CrossRef][PubMed]
    [Google Scholar]
  24. Zhang Z, Saier MH Jr. A mechanism of transposon-mediated directed mutation. Mol Microbiol 2009;74:29–43 [CrossRef][PubMed]
    [Google Scholar]
  25. Zhang Z, Saier MH Jr. Transposon-mediated activation of the Escherichia coli glpFK operon is inhibited by specific DNA-binding proteins: Implications for stress-induced transposition events. Mutat Res 2016;793-794:22–31 [CrossRef][PubMed]
    [Google Scholar]
  26. Soutourina OA, Bertin PN. Regulation cascade of flagellar expression in Gram-negative bacteria. FEMS Microbiol Rev 2003;27:505–523 [CrossRef][PubMed]
    [Google Scholar]
  27. Fitzgerald DM, Bonocora RP, Wade JT. Comprehensive mapping of the Escherichia coli flagellar regulatory network. PLoS Genet 2014;10:e1004649 [CrossRef][PubMed]
    [Google Scholar]
  28. Fahrner KA, Berg HC. Mutations that stimulate flhDC expression in Escherichia coli K-12. J Bacteriol 2015;197:3087–3096 [CrossRef][PubMed]
    [Google Scholar]
  29. Rahimpour M, Montero M, Almagro G, Viale AM, Sevilla Á et al. GlgS, described previously as a glycogen synthesis control protein, negatively regulates motility and biofilm formation in Escherichia coli. Biochem J 2013;452:559–573 [CrossRef][PubMed]
    [Google Scholar]
  30. Vikram A, Jayaprakasha GK, Uckoo RM, Patil BS. Inhibition of Escherichia coli O157:H7 motility and biofilm by β-sitosterol glucoside. Biochim Biophys Acta 2013;1830:5219–5228[CrossRef]
    [Google Scholar]
  31. Allison SE, Silphaduang U, Mascarenhas M, Konczy P, Quan Q et al. Novel repressor of Escherichia coli O157:H7 motility encoded in the putative fimbrial cluster OI-1. J Bacteriol 2012;194:5343–5352 [CrossRef][PubMed]
    [Google Scholar]
  32. Kitagawa R, Takaya A, Yamamoto T. Dual regulatory pathways of flagellar gene expression by ClpXP protease in enterohaemorrhagic Escherichia coli. Microbiology 2011;157:3094–3103 [CrossRef][PubMed]
    [Google Scholar]
  33. Lehti TA, Bauchart P, Dobrindt U, Korhonen TK, Westerlund-Wikström B. The fimbriae activator MatA switches off motility in Escherichia coli by repression of the flagellar master operon flhDC. Microbiology 2012;158:1444–1455 [CrossRef][PubMed]
    [Google Scholar]
  34. Reiss DJ, Mobley HL. Determination of target sequence bound by PapX, repressor of bacterial motility, in flhD promoter using systematic evolution of ligands by exponential enrichment (SELEX) and high throughput sequencing. J Biol Chem 2011;286:44726–44738 [CrossRef][PubMed]
    [Google Scholar]
  35. Theodorou MC, Theodorou EC, Kyriakidis DA. Involvement of AtoSC two-component system in Escherichia coli flagellar regulon. Amino Acids 2012;43:833–844 [CrossRef][PubMed]
    [Google Scholar]
  36. Wiebe H, Gürlebeck D, Groß J, Dreck K, Pannen D et al. YjjQ represses transcription of flhDC and additional loci in Escherichia coli. J Bacteriol 2015;197:2713–2720 [CrossRef][PubMed]
    [Google Scholar]
  37. Wada T, Hatamoto Y, Kutsukake K. Functional and expressional analyses of the anti-FlhD4C2 factor gene ydiV in Escherichia coli. Microbiology 2012;158:1533–1542 [CrossRef][PubMed]
    [Google Scholar]
  38. De Lay N, Gottesman S. A complex network of small non-coding RNAs regulate motility in Escherichia coli. Mol Microbiol 2012;86:524–538 [CrossRef][PubMed]
    [Google Scholar]
  39. Thomason MK, Fontaine F, De Lay N, Storz G. A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli. Mol Microbiol 2012;84:17–35 [CrossRef][PubMed]
    [Google Scholar]
  40. Chilcott GS, Hughes KT. Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar Typhimurium and Escherichia coli. Microbiol Mol Biol Rev 2000;64:694–708 [CrossRef][PubMed]
    [Google Scholar]
  41. Guttenplan SB, Kearns DB. Regulation of flagellar motility during biofilm formation. FEMS Microbiol Rev 2013;37:849–871 [CrossRef][PubMed]
    [Google Scholar]
  42. Sule P, Horne SM, Logue CM, Prüss BM. Regulation of cell division, biofilm formation, and virulence by FlhC in Escherichia coli O157:H7 grown on meat. Appl Environ Microbiol 2011;77:3653–3662 [CrossRef][PubMed]
    [Google Scholar]
  43. Copeland MF, Weibel DB. Bacterial swarming: a model system for studying dynamic self-assembly. Soft Matter 2009;5:1174–1187[CrossRef]
    [Google Scholar]
  44. Wang X, Wood TK. IS5 inserts upstream of the master motility operon flhDC in a quasi-Lamarckian way. ISME J 2011;5:1517–1525 [CrossRef][PubMed]
    [Google Scholar]
  45. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 2000;97:6640–6645 [CrossRef][PubMed]
    [Google Scholar]
  46. Wang H, Noordewier M, Benham CJ. Stress-induced DNA duplex destabilization (SIDD) in the E. coli genome: SIDD sites are closely associated with promoters. Genome Res 2004;14:1575–1584 [CrossRef][PubMed]
    [Google Scholar]
  47. Zhabinskaya D, Madden S, Benham CJ. SIST: stress-induced structural transitions in superhelical DNA. Bioinformatics 2015;31:421–422 [CrossRef][PubMed]
    [Google Scholar]
  48. Benham CJ. Duplex destabilization in superhelical DNA is predicted to occur at specific transcriptional regulatory regions. J Mol Biol 1996;255:425–434 [CrossRef][PubMed]
    [Google Scholar]
  49. Bi C, Benham CJ. WebSIDD: server for predicting stress-induced duplex destabilized (SIDD) sites in superhelical DNA. Bioinformatics 2004;20:1477–1479 [CrossRef][PubMed]
    [Google Scholar]
  50. Wang H, Benham CJ. Superhelical destabilization in regulatory regions of stress response genes. PLoS Comput Biol 2008;4:e17 [CrossRef][PubMed]
    [Google Scholar]
  51. Zimm BH, Levene SD. Problems and prospects in the theory of gel electrophoresis of DNA. Q Rev Biophys 1992;25:171–204 [CrossRef][PubMed]
    [Google Scholar]
  52. Martinez-Vaz BM, Xie Y, Pan W, Khodursky AB. Genome-wide localization of mobile elements: experimental, statistical and biological considerations. BMC Genomics 2005;6:81 [CrossRef][PubMed]
    [Google Scholar]
  53. Stoebel DM, Hokamp K, Last MS, Dorman CJ. Compensatory evolution of gene regulation in response to stress by Escherichia coli lacking RpoS. PLoS Genet 2009;5:e1000671 [CrossRef][PubMed]
    [Google Scholar]
  54. Gode-Potratz CJ, Kustusch RJ, Breheny PJ, Weiss DS, McCarter LL. Surface sensing in Vibrio parahaemolyticus triggers a programme of gene expression that promotes colonization and virulence. Mol Microbiol 2011;79:240–263 [CrossRef][PubMed]
    [Google Scholar]
  55. Kim YK, McCarter LL. Cross-regulation in Vibrio parahaemolyticus: compensatory activation of polar flagellar genes by the lateral flagellar regulator LafK. J Bacteriol 2004;186:4014–4018 [CrossRef][PubMed]
    [Google Scholar]
  56. McCarter LL. Dual flagellar systems enable motility under different circumstances. J Mol Microbiol Biotechnol 2004;7:18–29 [CrossRef][PubMed]
    [Google Scholar]
  57. Vandecraen J, Monsieurs P, Mergeay M, Leys N, Aertsen A et al. Zinc-induced transposition of insertion sequence elements contributes to increased adaptability of Cupriavidus metallidurans. Front Microbiol 2016;7:359 [CrossRef][PubMed]
    [Google Scholar]
  58. Al-Natour S. Lipoid proteinosis: a report of 2 siblings and a brief review of the literature. Saudi Med J 2008;29:1188–1191
    [Google Scholar]
  59. Teras R, Hõrak R, Kivisaar M. Transcription from fusion promoters generated during transposition of transposon Tn4652 is positively affected by integration host factor in Pseudomonas putida. J Bacteriol 2000;182:589–598 [CrossRef][PubMed]
    [Google Scholar]
  60. Soutourina O, Kolb A, Krin E, Laurent-Winter C, Rimsky S et al. 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 1999;181:7500–7508[PubMed]
    [Google Scholar]
  61. Saier MH Jr. Protein phosphorylation and allosteric control of inducer exclusion and catabolite repression by the bacterial phosphoenolpyruvate: sugar phosphotransferase system. Microbiol Rev 1989;53:109–120[PubMed]
    [Google Scholar]
  62. Stella NA, Kalivoda EJ, O'Dee DM, Nau GJ, Shanks RM. Catabolite repression control of flagellum production by Serratia marcescens. Res Microbiol 2008;159:562–568 [CrossRef][PubMed]
    [Google Scholar]
  63. Lee H, Doak TG, Popodi E, Foster PL, Tang H. Insertion sequence-caused large-scale rearrangements in the genome of Escherichia coli. Nucl Acids Res 2016;44:7109–7119 [CrossRef][PubMed]
    [Google Scholar]
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