Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1993 Aug;175(16):5009–5021. doi: 10.1128/jb.175.16.5009-5021.1993

Identification and transcriptional analysis of the Escherichia coli htrE operon which is homologous to pap and related pilin operons.

S Raina 1, D Missiakas 1, L Baird 1, S Kumar 1, C Georgopoulos 1
PMCID: PMC204966  PMID: 8102362

Abstract

We have characterized a new Escherichia coli operon consisting of two genes, ecpD and htrE. The ecpD gene encodes a 27-kDa protein which is 40% identical at the amino acid level to the pilin chaperone PapD family of proteins. Immediately downstream of the ecpD gene is the htrE gene. The htrE gene encodes a polypeptide of 95 kDa which is processed to a 92-kDa mature species. The HtrE protein is 38% identical to the type II pilin porin protein PapC. The ecpD htrE operon is located at 3.3 min on the genetic map, corresponding to the region from kbp 153 to 157 of the E. coli physical map. The htrE gene was identified on the basis of a Tn5 insertion mutation which resulted in a temperature-sensitive growth phenotype above 43.5 degrees C. The transcription of this operon is induced with a temperature shift from 22 to 37 or 42 degrees C but not to higher temperatures, e.g., 50 degrees C. Consistent with this result, the temperature-induced transcription was shown to be independent of the rpoH gene product (sigma 32). The transcription of this operon was further shown to require functional integration host factor protein, since himA or himD mutant bacteria possessed lower levels of ecpD htrE transcripts. Among the three transcriptional start sites discovered, one, defined by the P2 promoter, was found to be under the positive regulation of the katF (rpoS) gene, which encodes a putative sigma factor required for the transcription of many growth phase-regulated genes.

Full text

PDF
5009

Images in this article

5016Image
on p.5016
5016Image
on p.5016
5017Image
on p.5017
5017Image
on p.5017
5018Image
on p.5018
5018Image
on p.5018
5019Image
on p.5019

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abraham J. M., Freitag C. S., Clements J. R., Eisenstein B. I. An invertible element of DNA controls phase variation of type 1 fimbriae of Escherichia coli. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5724–5727. doi: 10.1073/pnas.82.17.5724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allen B. L., Gerlach G. F., Clegg S. Nucleotide sequence and functions of mrk determinants necessary for expression of type 3 fimbriae in Klebsiella pneumoniae. J Bacteriol. 1991 Jan;173(2):916–920. doi: 10.1128/jb.173.2.916-920.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Arnqvist A., Olsén A., Pfeifer J., Russell D. G., Normark S. The Crl protein activates cryptic genes for curli formation and fibronectin binding in Escherichia coli HB101. Mol Microbiol. 1992 Sep;6(17):2443–2452. doi: 10.1111/j.1365-2958.1992.tb01420.x. [DOI] [PubMed] [Google Scholar]
  4. Braaten B. A., Platko J. V., van der Woude M. W., Simons B. H., de Graaf F. K., Calvo J. M., Low D. A. Leucine-responsive regulatory protein controls the expression of both the pap and fan pili operons in Escherichia coli. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4250–4254. doi: 10.1073/pnas.89.10.4250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Churchward G., Belin D., Nagamine Y. A pSC101-derived plasmid which shows no sequence homology to other commonly used cloning vectors. Gene. 1984 Nov;31(1-3):165–171. doi: 10.1016/0378-1119(84)90207-5. [DOI] [PubMed] [Google Scholar]
  6. Dodson K. W., Jacob-Dubuisson F., Striker R. T., Hultgren S. J. Outer-membrane PapC molecular usher discriminately recognizes periplasmic chaperone-pilus subunit complexes. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3670–3674. doi: 10.1073/pnas.90.8.3670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dorman C. J., Higgins C. F. Fimbrial phase variation in Escherichia coli: dependence on integration host factor and homologies with other site-specific recombinases. J Bacteriol. 1987 Aug;169(8):3840–3843. doi: 10.1128/jb.169.8.3840-3843.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Duguid J. P., Clegg S., Wilson M. I. The fimbrial and non-fimbrial haemagglutinins of Escherichia coli. J Med Microbiol. 1979 May;12(2):213–227. doi: 10.1099/00222615-12-2-213. [DOI] [PubMed] [Google Scholar]
  9. Fellay R., Frey J., Krisch H. Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria. Gene. 1987;52(2-3):147–154. doi: 10.1016/0378-1119(87)90041-2. [DOI] [PubMed] [Google Scholar]
  10. Friedman D. I., Olson E. J., Carver D., Gellert M. Synergistic effect of himA and gyrB mutations: evidence that him functions control expression of ilv and xyl genes. J Bacteriol. 1984 Feb;157(2):484–489. doi: 10.1128/jb.157.2.484-489.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Giampapa C. S., Abraham S. N., Chiang T. M., Beachey E. H. Isolation and characterization of a receptor for type 1 fimbriae of Escherichia coli from guinea pig erythrocytes. J Biol Chem. 1988 Apr 15;263(11):5362–5367. [PubMed] [Google Scholar]
  12. Göransson M., Sondén B., Nilsson P., Dagberg B., Forsman K., Emanuelsson K., Uhlin B. E. Transcriptional silencing and thermoregulation of gene expression in Escherichia coli. Nature. 1990 Apr 12;344(6267):682–685. doi: 10.1038/344682a0. [DOI] [PubMed] [Google Scholar]
  13. Hacker J. Genetic determinants coding for fimbriae and adhesins of extraintestinal Escherichia coli. Curr Top Microbiol Immunol. 1990;151:1–27. doi: 10.1007/978-3-642-74703-8_1. [DOI] [PubMed] [Google Scholar]
  14. Hengge-Aronis R., Klein W., Lange R., Rimmele M., Boos W. Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli. J Bacteriol. 1991 Dec;173(24):7918–7924. doi: 10.1128/jb.173.24.7918-7924.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Holmgren A., Bränden C. I. Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature. 1989 Nov 16;342(6247):248–251. doi: 10.1038/342248a0. [DOI] [PubMed] [Google Scholar]
  16. Holmgren A., Kuehn M. J., Brändén C. I., Hultgren S. J. Conserved immunoglobulin-like features in a family of periplasmic pilus chaperones in bacteria. EMBO J. 1992 Apr;11(4):1617–1622. doi: 10.1002/j.1460-2075.1992.tb05207.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hultgren S. J., Normark S., Abraham S. N. Chaperone-assisted assembly and molecular architecture of adhesive pili. Annu Rev Microbiol. 1991;45:383–415. doi: 10.1146/annurev.mi.45.100191.002123. [DOI] [PubMed] [Google Scholar]
  18. Klemm P., Christiansen G. The fimD gene required for cell surface localization of Escherichia coli type 1 fimbriae. Mol Gen Genet. 1990 Jan;220(2):334–338. doi: 10.1007/BF00260505. [DOI] [PubMed] [Google Scholar]
  19. Klemm P., Jørgensen B. J., van Die I., de Ree H., Bergmans H. The fim genes responsible for synthesis of type 1 fimbriae in Escherichia coli, cloning and genetic organization. Mol Gen Genet. 1985;199(3):410–414. doi: 10.1007/BF00330751. [DOI] [PubMed] [Google Scholar]
  20. Kohara Y., Akiyama K., Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
  21. Koomey J. M., Gill R. E., Falkow S. Genetic and biochemical analysis of gonococcal IgA1 protease: cloning in Escherichia coli and construction of mutants of gonococci that fail to produce the activity. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7881–7885. doi: 10.1073/pnas.79.24.7881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kuehn M. J., Normark S., Hultgren S. J. Immunoglobulin-like PapD chaperone caps and uncaps interactive surfaces of nascently translocated pilus subunits. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10586–10590. doi: 10.1073/pnas.88.23.10586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lange R., Hengge-Aronis R. Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor sigma S. J Bacteriol. 1991 Jul;173(14):4474–4481. doi: 10.1128/jb.173.14.4474-4481.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lindberg F., Tennent J. M., Hultgren S. J., Lund B., Normark S. PapD, a periplasmic transport protein in P-pilus biogenesis. J Bacteriol. 1989 Nov;171(11):6052–6058. doi: 10.1128/jb.171.11.6052-6058.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lipinska B., Fayet O., Baird L., Georgopoulos C. Identification, characterization, and mapping of the Escherichia coli htrA gene, whose product is essential for bacterial growth only at elevated temperatures. J Bacteriol. 1989 Mar;171(3):1574–1584. doi: 10.1128/jb.171.3.1574-1584.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Liu J. D., Parkinson J. S. Genetics and sequence analysis of the pcnB locus, an Escherichia coli gene involved in plasmid copy number control. J Bacteriol. 1989 Mar;171(3):1254–1261. doi: 10.1128/jb.171.3.1254-1261.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Malo M. S. A rapid and efficient method for transcript mapping. Nucleic Acids Res. 1990 Oct 25;18(20):6159–6159. doi: 10.1093/nar/18.20.6159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. McCann M. P., Kidwell J. P., Matin A. The putative sigma factor KatF has a central role in development of starvation-mediated general resistance in Escherichia coli. J Bacteriol. 1991 Jul;173(13):4188–4194. doi: 10.1128/jb.173.13.4188-4194.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mooi F. R., Claassen I., Bakker D., Kuipers H., de Graaf F. K. Regulation and structure of an Escherichia coli gene coding for an outer membrane protein involved in export of K88ab fimbrial subunits. Nucleic Acids Res. 1986 Mar 25;14(6):2443–2457. doi: 10.1093/nar/14.6.2443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Norgren M., Båga M., Tennent J. M., Normark S. Nucleotide sequence, regulation and functional analysis of the papC gene required for cell surface localization of Pap pili of uropathogenic Escherichia coli. Mol Microbiol. 1987 Sep;1(2):169–178. doi: 10.1111/j.1365-2958.1987.tb00509.x. [DOI] [PubMed] [Google Scholar]
  31. O'Connor M., Gesteland R. F., Atkins J. F. tRNA hopping: enhancement by an expanded anticodon. EMBO J. 1989 Dec 20;8(13):4315–4323. doi: 10.1002/j.1460-2075.1989.tb08618.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Olsén A., Arnqvist A., Hammar M., Sukupolvi S., Normark S. The RpoS sigma factor relieves H-NS-mediated transcriptional repression of csgA, the subunit gene of fibronectin-binding curli in Escherichia coli. Mol Microbiol. 1993 Feb;7(4):523–536. doi: 10.1111/j.1365-2958.1993.tb01143.x. [DOI] [PubMed] [Google Scholar]
  33. Olsén A., Jonsson A., Normark S. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature. 1989 Apr 20;338(6217):652–655. doi: 10.1038/338652a0. [DOI] [PubMed] [Google Scholar]
  34. Raina S., Georgopoulos C. A new Escherichia coli heat shock gene, htrC, whose product is essential for viability only at high temperatures. J Bacteriol. 1990 Jun;172(6):3417–3426. doi: 10.1128/jb.172.6.3417-3426.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Raina S., Georgopoulos C. The htrM gene, whose product is essential for Escherichia coli viability only at elevated temperatures, is identical to the rfaD gene. Nucleic Acids Res. 1991 Jul 25;19(14):3811–3819. doi: 10.1093/nar/19.14.3811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rioux C. R., Friedrich M. J., Kadner R. J. Genes on the 90-kilobase plasmid of Salmonella typhimurium confer low-affinity cobalamin transport: relationship to fimbria biosynthesis genes. J Bacteriol. 1990 Nov;172(11):6217–6222. doi: 10.1128/jb.172.11.6217-6222.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Roosendaal B., de Graaf F. K. The nucleotide sequence of the fanD gene encoding the large outer membrane protein involved in the biosynthesis of K99 fimbriae. Nucleic Acids Res. 1989 Feb 11;17(3):1263–1263. doi: 10.1093/nar/17.3.1263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Singer M., Baker T. A., Schnitzler G., Deischel S. M., Goel M., Dove W., Jaacks K. J., Grossman A. D., Erickson J. W., Gross C. A. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev. 1989 Mar;53(1):1–24. doi: 10.1128/mr.53.1.1-24.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. de Graaf F. K., Krenn B. E., Klaasen P. Organization and expression of genes involved in the biosynthesis of K99 fimbriae. Infect Immun. 1984 Feb;43(2):508–514. doi: 10.1128/iai.43.2.508-514.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. van der Woude M. W., Braaten B. A., Low D. A. Evidence for global regulatory control of pilus expression in Escherichia coli by Lrp and DNA methylation: model building based on analysis of pap. Mol Microbiol. 1992 Sep;6(17):2429–2435. doi: 10.1111/j.1365-2958.1992.tb01418.x. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES