1887

Abstract

Temperature serves as a cue to regulate gene expression in and other bacteria. Using DNA microarrays, we identified 297 genes whose expression is increased at 23 °C compared to 37 °C in K-12. Of these genes, 122 are RpoS-controlled, confirming genome-wide the model that low temperature serves as a primary cue to trigger the general stress response. Several genes expressed at 23 °C overlap with the cold-shock response, suggesting that strategies used to adapt to sudden shifts in temperature also mediate long-term growth at 23 °C. Another category of genes more highly expressed at 23 °C are associated with biofilm development, implicating temperature as an important cue influencing this developmental pathway. In a candidate set of genes tested, the biofilm genes (, , , , , / and cold-shock genes (, / were found to be RpoS- and DsrA-dependent for their transcription at 23 °C. In contrast, transcription of three genes (, and ) was either partially or fully independent of these regulators, signifying there is an alternative thermoregulatory mechanism(s) that increases gene expression at 23 °C. Increased expression at 23 °C compared to 37 °C is retained in various media tested for most of the genes, supporting the relative importance of this cue in adaptation to changing environments. Both the RpoS-dependent gene and the RpoS-independent gene demonstrated increased expression levels within 1 h after a shift from 37 to 23 °C, indicating a rapid response to this environmental cue. Despite changes in gene expression for many RpoS-dependent genes, experiments assessing growth rate at 23 °C and viability at 4 °C did not demonstrate significant impairment in  : : Tn or  : :  mutant strains in comparison to the wild-type strain. Biofilm formation was favoured at low temperature and is moderately impaired in both the  : : Tn and  : :  mutants at 23 °C, suggesting genes controlled by these regulators play a role necessary for optimal biofilm formation at 23 °C. Taken together, our data demonstrate that a large number of genes are increased in expression at 23 °C to globally respond to this environmental change and that at least two thermoregulatory pathways are involved in co-ordinating this response – the RpoS/DsrA pathway and an alternative thermoregulatory pathway, independent of these regulators.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/012021-0
2008-01-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/1/148.html?itemId=/content/journal/micro/10.1099/mic.0.2007/012021-0&mimeType=html&fmt=ahah

References

  1. Adams J. L., McLean R. J. 1999; Impact of rpoS deletion on Escherichia coli biofilms. Appl Environ Microbiol 65:4285–4287
    [Google Scholar]
  2. Berney M., Weilenmann H. U., Ihssen J., Bassin C., Egli T. 2006; Specific growth rate determines the sensitivity of Escherichia coli to thermal, UVA, and solar disinfection. Appl Environ Microbiol 72:2586–2593
    [Google Scholar]
  3. Braaten B. A., Nou X., Kaltenbach L. S., Low D. A. 1994; Methylation patterns in pap regulatory DNA control pyelonephritis-associated pili phase variation in E. coli . Cell 76:577–588
    [Google Scholar]
  4. Brombacher E., Dorel C., Zehnder A. J., Landini P. 2003; The curli biosynthesis regulator CsgD co-ordinates the expression of both positive and negative determinants for biofilm formation in Escherichia coli . Microbiology 149:2847–2857
    [Google Scholar]
  5. Brooks C. S., Hefty P. S., Jolliff S. E., Akins D. R. 2003; Global analysis of Borrelia burgdorferi genes regulated by mammalian host-specific signals. Infect Immun 71:3371–3383
    [Google Scholar]
  6. Brown P. K., Dozois C. M., Nickerson C. A., Zuppardo A., Terlonge J., Curtiss R. III 2001; MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Mol Microbiol 41:349–363
    [Google Scholar]
  7. Casadaban M. J. 1976; Transposition and fusion of the lac genes to selected promoters in E. coli using bacteriophage lambda and Mu. J Mol Biol 104:541–555
    [Google Scholar]
  8. Checroun C., Gutierrez C. 2004; σ S-dependent regulation of yehZYXW , which encodes a putative osmoprotectant ABC transporter of Escherichia coli . FEMS Microbiol Lett 236:221–226
    [Google Scholar]
  9. Cheville A. M., Arnold K. W., Buchrieser C., Cheng C. M., Kaspar C. W. 1996; rpoS regulation of acid, heat, and salt tolerance in Escherichia coli O157: H7. Appl Environ Microbiol 62:1822–1824
    [Google Scholar]
  10. Conter A., Menchon C., Gutierrez C. 1997; Role of DNA supercoiling and rpoS sigma factor in the osmotic and growth phase-dependent induction of the gene osmE of Escherichia coli K12. J Mol Biol 273:75–83
    [Google Scholar]
  11. Cookson A. L., Cooley W. A., Woodward M. J. 2002; The role of type 1 and curli fimbriae of Shiga toxin-producing Escherichia coli in adherence to abiotic surfaces. Int J Med Microbiol 292:195–205
    [Google Scholar]
  12. Corona-Izquierdo F. P., Membrillo-Hernandez J. 2002; A mutation in rpoS enhances biofilm formation in Escherichia coli during exponential phase of growth. FEMS Microbiol Lett 211:105–110
    [Google Scholar]
  13. Cotter P. A., Miller J. F. 1998; In vivo and ex vivo regulation of bacterial virulence gene expression. Curr Opin Microbiol 1:17–26
    [Google Scholar]
  14. Domka J., Lee J., Wood T. K. 2006; YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl Environ Microbiol 72:2449–2459
    [Google Scholar]
  15. Ferenci T. 2003; What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli ?. Trends Microbiol 11:457–461
    [Google Scholar]
  16. Garcia B., Latasa C., Solano C., Garcia-del Portillo F., Gamazo C., Lasa I. 2004; Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol Microbiol 54:264–277
    [Google Scholar]
  17. Goller C., Wang X., Itoh Y., Romeo T. 2006; The cation-responsive protein NhaR of Escherichia coli activates pgaABCD transcription, required for production of the biofilm adhesin poly- β -1,6- N -acetyl-d-glucosamine. J Bacteriol 188:8022–8032
    [Google Scholar]
  18. Grogan D. W., Cronan J. E. Jr 1984; Genetic characterization of the Escherichia coli cyclopropane fatty acid (cfa) locus and neighboring loci. Mol Gen Genet 196:367–372
    [Google Scholar]
  19. Grogan D. W., Cronan J. E. Jr 1997; Cyclopropane ring formation in membrane lipids of bacteria. Microbiol Mol Biol Rev 61:429–441
    [Google Scholar]
  20. Gross C. others 1996; Function and regulation of the heat shock proteins. In Escherichia coli and Salmonella typhimurium Cellular and Molecular Biology . pp 1382–1399 Edited by Neihardt F. C. Curtiss R. C. III, Ingraham J. L. Washington, DC: American Society for Microbiology;
  21. Gualerzi C. O., Giuliodori A. M., Pon C. L. 2003; Transcriptional and post-transcriptional control of cold-shock genes. J Mol Biol 331:527–539
    [Google Scholar]
  22. Han Y., Zhou D., Pang X., Song Y., Zhang L., Bao J., Tong Z., Wang J., Guo Z. other authors 2004; Microarray analysis of temperature-induced transcriptome of Yersinia pestis . Microbiol Immunol 48:791–805
    [Google Scholar]
  23. Hashimoto W., Suzuki H., Yamamoto K., Kumagai H. 1997; Analysis of low temperature inducible mechanism of gamma-glutamyltranspeptidase of Escherichia coli K-12. Biosci Biotechnol Biochem 61:34–39
    [Google Scholar]
  24. Hirakawa H., Inazumi Y., Senda Y., Kobayashi A., Hirata T., Nishino K., Yamaguchi A. 2006; N -Acetyl-d-glucosamine induces the expression of multidrug exporter genes, mdtEF , via catabolite activation in Escherichia coli . J Bacteriol 188:5851–5858
    [Google Scholar]
  25. Kandror O., DeLeon A., Goldberg A. L. 2002; Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci U S A 99:9727–9732
    [Google Scholar]
  26. Lacour S., Landini P. 2004; SigmaS-dependent gene expression at the onset of stationary phase in Escherichia coli : function of sigmaS-dependent genes and identification of their promoter sequences. J Bacteriol 186:7186–7195
    [Google Scholar]
  27. Lange R., Hengge-Aronis R. 1991; Identification of a central regulator of stationary-phase gene expression in Escherichia coli . Mol Microbiol 5:49–59
    [Google Scholar]
  28. Lease R. A., Belfort M. 2000; Riboregulation by DsrA RNA: trans-actions for global economy. Mol Microbiol 38:667–672
    [Google Scholar]
  29. Livak K. J., Schmittgen T. D. 2001; Analysis of relative gene expression data using real-time quantitative PCR and the method. Methods 25:402–408
    [Google Scholar]
  30. Mahan M. J., Slauch J. M., Mekalanos J. J. others 1996 Environmental regulation of virulence gene expression in Escherichia , Salmonella , and Shigella spp. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp 2803–2816 Edited by Neidhardt F. C. Curtiss R. III, Ingraham J. L. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  31. Marschall C., Hengge-Aronis R. 1995; Regulatory characteristics and promoter analysis of csiE , a stationary phase-inducible gene under the control of sigma S and the cAMP-CRP complex in Escherichia coli . Mol Microbiol 18:175–184
    [Google Scholar]
  32. McMeechan A., Roberts M., Cogan T. A., Jorgensen F., Stevenson A., Lewis C., Rowley G., Humphrey T. J. 2007; Role of the alternative sigma factors sigmaE and sigmaS in survival of Salmonella enterica serovar Typhimurium during starvation, refrigeration and osmotic shock. Microbiology 153:263–269
    [Google Scholar]
  33. Mekalanos J. J. 1992; Environmental signals controlling expression of virulence determinants in bacteria. J Bacteriol 174:1–7
    [Google Scholar]
  34. Mellies J., Wise A., Villarejo M. 1995; Two different Escherichia coli proP promoters respond to osmotic and growth phase signals. J Bacteriol 177:144–151
    [Google Scholar]
  35. Metzner M., Germer J., Hengge R. 2004; Multiple stress signal integration in the regulation of the complex sigma S-dependent csiD - ygaF - gabDTP operon in Escherichia coli . Mol Microbiol 51:799–811
    [Google Scholar]
  36. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  37. Motin V. L., Georgescu A. M., Fitch J. P., Gu P. P., Nelson D. O., Mabery S. L., Garnham J. B., Sokhansanj B. A., Ott L. L. other authors 2004; Temporal global changes in gene expression during temperature transition in Yersinia pestis . J Bacteriol 186:6298–6305
    [Google Scholar]
  38. Muffler A., Barth M., Marschall C., Hengge-Aronis R. 1997; Heat shock regulation of sigmaS turnover: a role for DnaK and relationship between stress responses mediated by sigmaS and sigma32 in Escherichia coli . J Bacteriol 179:445–452
    [Google Scholar]
  39. O'Toole G. A., Kolter R. 1998; Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28:449–461
    [Google Scholar]
  40. Olsen A., Arnqvist A., Hammar M., Normark S. 1993a; Environmental regulation of curli production in Escherichia coli . Infect Agents Dis 2:272–274
    [Google Scholar]
  41. Olsen A., Arnqvist A., Hammar M., Sukupolvi S., Normark S. 1993b; The RpoS sigma factor relieves H-NS-mediated transcriptional repression of csgA, the subunit gene of fibronectin-binding curli in Escherichia coli . Mol Microbiol 7:523–536
    [Google Scholar]
  42. Otto K., Hermansson M. 2004; Inactivation of ompX causes increased interactions of type 1 fimbriated Escherichia coli with abiotic surfaces. J Bacteriol 186:226–234
    [Google Scholar]
  43. Peters J. E., Thate T. E., Craig N. L. 2003; Definition of the Escherichia coli MC4100 genome by use of a DNA array. J Bacteriol 185:2017–2021
    [Google Scholar]
  44. Phadtare S., Inouye M. 2004; Genome-wide transcriptional analysis of the cold shock response in wild-type and cold-sensitive, quadruple-csp-deletion strains of Escherichia coli . J Bacteriol 186:7007–7014
    [Google Scholar]
  45. Phadtare S., Yamanaka K., Inouye M. 2000; The cold shock response. In Bacterial Stress Responses pp 33–46 Edited by Storz G. Hengge-Aronis R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  46. Polissi A., De Laurentis W., Zangrossi S., Briani F., Longhi V., Pesole G., Deho G. 2003; Changes in Escherichia coli transcriptome during acclimatization at low temperature. Res Microbiol 154:573–580
    [Google Scholar]
  47. Prigent-Combaret C., Brombacher E., Vidal O., Ambert A., Lejeune P., Landini P., Dorel C. 2001; Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J Bacteriol 183:7213–7223
    [Google Scholar]
  48. Rajkumari K., Gowrishankar J. 2001; In vivo expression from the RpoS-dependent P1 promoter of the osmotically regulated proU operon in Escherichia coli and Salmonella enterica serovar Typhimurium: activation by rho and hns mutations and by cold stress. J Bacteriol 183:6543–6550
    [Google Scholar]
  49. Rajkumari K., Gowrishankar J. 2002; An N-terminally truncated RpoS ( σ S) protein in Escherichia coli is active in vivo and exhibits normal environmental regulation even in the absence of rpoS transcriptional and translational control signals. J Bacteriol 184:3167–3175
    [Google Scholar]
  50. Ren D., Bedzyk L. A., Thomas S. M., Ye R. W., Wood T. K. 2004; Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol 64:515–524
    [Google Scholar]
  51. Repoila F., Majdalani N., Gottesman S. 2003; Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli : the RpoS paradigm. Mol Microbiol 48:855–861
    [Google Scholar]
  52. Revel A. T., Talaat A. M., Norgard M. V. 2002; DNA microarray analysis of differential gene expression in Borrelia burgdorferi , the Lyme disease spirochete. Proc Natl Acad Sci U S A 99:1562–1567
    [Google Scholar]
  53. Romling U., Bian Z., Hammar M., Sierralta W. D., Normark S. 1998; Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180:722–731
    [Google Scholar]
  54. Romling U., Rohde M., Olsen A., Normark S., Reinkoster J. 2000; AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 36:10–23
    [Google Scholar]
  55. Santos J. M., Freire P., Vicente M., Arraiano C. M. 1999; The stationary-phase morphogene bolA from Escherichia coli is induced by stress during early stages of growth. Mol Microbiol 32:789–798
    [Google Scholar]
  56. Silhavy T. J., Berman M. L., Enquist L. W. 1984 Experiments with Gene Fusions Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  57. Sledjeski D. D., Gupta A., Gottesman S. 1996; The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli . EMBO J 15:3993–4000
    [Google Scholar]
  58. Smoot L. M., Smoot J. C., Graham M. R., Somerville G. A., Sturdevant D. E., Migliaccio C. A., Sylva G. L., Musser J. M. 2001; Global differential gene expression in response to growth temperature alteration in group A Streptococcus . Proc Natl Acad Sci U S A 98:10416–10421
    [Google Scholar]
  59. Soupene E., King N., Lee H., Kustu S. 2002; Aquaporin Z of Escherichia coli : reassessment of its regulation and physiological role. J Bacteriol 184:4304–4307
    [Google Scholar]
  60. Stokes N. R., Murray H. D., Subramaniam C., Gourse R. L., Louis P., Bartlett W., Miller S., Booth I. R. 2003; A role for mechanosensitive channels in survival of stationary phase: regulation of channel expression by RpoS. Proc Natl Acad Sci U S A 100:15959–15964
    [Google Scholar]
  61. Tatusov R. L., Koonin E. V., Lipman D. J. 1997; A genomic perspective on protein families. Science 278:631–637
    [Google Scholar]
  62. Toesca I., Perard C., Bouvier J., Gutierrez C., Conter A. 2001; The transcriptional activator NhaR is responsible for the osmotic induction of osmC(p1), a promoter of the stress-inducible gene osmC in Escherichia coli . Microbiology 147:2795–2803
    [Google Scholar]
  63. Tusher V. G., Tibshirani R., Chu G. 2001; Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98:5116–5121
    [Google Scholar]
  64. Vidal O., Longin R., Prigent-Combaret C., Dorel C., Hooreman M., Lejeune P. 1998; Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J Bacteriol 180:2442–2449
    [Google Scholar]
  65. Vieira H. L., Freire P., Arraiano C. M. 2004; Effect of Escherichia coli morphogene bolA on biofilms. Appl Environ Microbiol 70:5682–5684
    [Google Scholar]
  66. Wang N., Yamanaka K., Inouye M. 1999; CspI, the ninth member of the CspA family of Escherichia coli , is induced upon cold shock. J Bacteriol 181:1603–1609
    [Google Scholar]
  67. Weber H., Polen T., Heuveling J., Wendisch V. F., Hengge R. 2005; Genome-wide analysis of the general stress response network in Escherichia coli : sigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187:1591–1603
    [Google Scholar]
  68. White-Ziegler C. A., Villapakkam A., Ronaszeki K., Young S. D. 2000; H-NS controls pap and daa fimbrial transcription Escherichia coli in response to multiple environmental cues. J Bacteriol 182:6391–6400
    [Google Scholar]
  69. White-Ziegler C. A., Malhowski A. J., Young S. 2007; Human body temperature (3 °C) increases the expression of iron, carbohydrate, and amino acid utilization genes in Escherichia coli K-12. J Bacteriol 189:5429–5440
    [Google Scholar]
  70. Xu J., Johnson R. C. 1995; Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli . J Bacteriol 177:938–947
    [Google Scholar]
  71. Yura T., Kanemori M., Morita M. T. 2000; The heat shock response: regulation and function. In Bacterial Stress Responses pp 3–18 Edited by Storz G. Hengge-Aronis R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  72. Zhao Y., Hindorff L. A., Chuang A., Monroe-Augustus M., Lyristis M., Harrison M. L., Rudolph F. B., Bennett G. N. 2003; Expression of a cloned cyclopropane fatty acid synthase gene reduces solvent formation in Clostridium acetobutylicum ATCC 824. Appl Environ Microbiol 69:2831–2841
    [Google Scholar]
  73. Zogaj X., Nimtz M., Rohde M., Bokranz W., Romling U. 2001; The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39:1452–1463
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/012021-0
Loading
/content/journal/micro/10.1099/mic.0.2007/012021-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error