Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1988 Sep;170(9):4119–4124. doi: 10.1128/jb.170.9.4119-4124.1988

Organization and temporal expression of a flagellar basal body gene in Caulobacter crescentus.

K M Hahnenberger 1, L Shapiro 1
PMCID: PMC211417  PMID: 2842303

Abstract

Caulobacter crescentus assembles a single polar flagellum at a defined time in the cell cycle. The protein components of the flagellar hook and filament are synthesized just prior to their assembly. We demonstrated that the expression of a gene, flaD, that is involved in the formation of the flagellar basal body is under temporal control and is transcribed relatively early in the cell cycle, before the hook and flagellin genes are transcribed. Thus, the order of flagellar gene transcription reflects the order of assembly of the protein components. A mutation in the flaD gene results in the assembly of a partial basal body which is missing the outermost P and L rings as well as the external hook and filament (K.M. Hahnenberger and L. Shapiro, J. Mol. Biol. 194:91-103, 1987). The flaD gene was cloned and characterized by nucleotide sequencing and S1 nuclease protection assays. In contrast to the protein components of the hook and filament, the protein encoded by the flaD gene contains a hydrophobic leader peptide. The predicted amino acid sequence of the leader peptide of flaD is very similar to the leader peptide of the flagellar basal body P ring of Salmonella typhimurium (M. Homma, Y. Komeda, T. Iino, and R.M. Macnab, J. Bacteriol. 169:1493-1498, 1987).

Full text

PDF
4119

Images in this article

Selected References

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

  1. Agabian N., Evinger M., Parker G. Generation of asymmetry during development. Segregation of type-specific proteins in Caulobacter. J Cell Biol. 1979 Apr;81(1):123–136. doi: 10.1083/jcb.81.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aizawa S. I., Dean G. E., Jones C. J., Macnab R. M., Yamaguchi S. Purification and characterization of the flagellar hook-basal body complex of Salmonella typhimurium. J Bacteriol. 1985 Mar;161(3):836–849. doi: 10.1128/jb.161.3.836-849.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Amemiya K., Bellofatto V., Shapiro L., Feingold J. Transcription initiation in vitro and in vivo at a highly conserved promoter within a 16 S ribosomal RNA gene. J Mol Biol. 1986 Jan 5;187(1):1–14. doi: 10.1016/0022-2836(86)90401-8. [DOI] [PubMed] [Google Scholar]
  4. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  5. Casjens S., King J. Virus assembly. Annu Rev Biochem. 1975;44:555–611. doi: 10.1146/annurev.bi.44.070175.003011. [DOI] [PubMed] [Google Scholar]
  6. Champer R., Bryan R., Gomes S. L., Purucker M., Shapiro L. Temporal and spatial control of flagellar and chemotaxis gene expression during Caulobacter cell differentiation. Cold Spring Harb Symp Quant Biol. 1985;50:831–840. doi: 10.1101/sqb.1985.050.01.101. [DOI] [PubMed] [Google Scholar]
  7. Champer R., Dingwall A., Shapiro L. Cascade regulation of Caulobacter flagellar and chemotaxis genes. J Mol Biol. 1987 Mar 5;194(1):71–80. doi: 10.1016/0022-2836(87)90716-9. [DOI] [PubMed] [Google Scholar]
  8. Chen L. S., Mullin D., Newton A. Identification, nucleotide sequence, and control of developmentally regulated promoters in the hook operon region of Caulobacter crescentus. Proc Natl Acad Sci U S A. 1986 May;83(9):2860–2864. doi: 10.1073/pnas.83.9.2860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Contreras I., Shapiro L., Henry S. Membrane phospholipid composition of Caulobacter crescentus. J Bacteriol. 1978 Sep;135(3):1130–1136. doi: 10.1128/jb.135.3.1130-1136.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Emerson S. U., Tokuyasu K., Simon M. I. Bacterial flagella: polarity of elongation. Science. 1970 Jul 10;169(3941):190–192. doi: 10.1126/science.169.3941.190. [DOI] [PubMed] [Google Scholar]
  11. Evinger M., Agabian N. Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells. J Bacteriol. 1977 Oct;132(1):294–301. doi: 10.1128/jb.132.1.294-301.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gill P. R., Agabian N. The nucleotide sequence of the Mr = 28,500 flagellin gene of Caulobacter crescentus. J Biol Chem. 1983 Jun 25;258(12):7395–7401. [PubMed] [Google Scholar]
  13. Gussin G. N., Ronson C. W., Ausubel F. M. Regulation of nitrogen fixation genes. Annu Rev Genet. 1986;20:567–591. doi: 10.1146/annurev.ge.20.120186.003031. [DOI] [PubMed] [Google Scholar]
  14. Hahnenberger K. M., Shapiro L. Identification of a gene cluster involved in flagellar basal body biogenesis in Caulobacter crescentus. J Mol Biol. 1987 Mar 5;194(1):91–103. doi: 10.1016/0022-2836(87)90718-2. [DOI] [PubMed] [Google Scholar]
  15. Homma M., Komeda Y., Iino T., Macnab R. M. The flaFIX gene product of Salmonella typhimurium is a flagellar basal body component with a signal peptide for export. J Bacteriol. 1987 Apr;169(4):1493–1498. doi: 10.1128/jb.169.4.1493-1498.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Homma M., Ohnishi K., Iino T., Macnab R. M. Identification of flagellar hook and basal body gene products (FlaFV, FlaFVI, FlaFVII and FlaFVIII) in Salmonella typhimurium. J Bacteriol. 1987 Aug;169(8):3617–3624. doi: 10.1128/jb.169.8.3617-3624.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Iino T. Polarity of flagellar growth in salmonella. J Gen Microbiol. 1969 May;56(2):227–239. doi: 10.1099/00221287-56-2-227. [DOI] [PubMed] [Google Scholar]
  18. Johnson R. C., Walsh M. P., Ely B., Shapiro L. Flagellar hook and basal complex of Caulobacter crescentus. J Bacteriol. 1979 Jun;138(3):984–989. doi: 10.1128/jb.138.3.984-989.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jones C. J., Homma M., Macnab R. M. Identification of proteins of the outer (L and P) rings of the flagellar basal body of Escherichia coli. J Bacteriol. 1987 Apr;169(4):1489–1492. doi: 10.1128/jb.169.4.1489-1492.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kaplan J. B., Goncharoff P., Seibold A. M., Nichols B. P. Nucleotide sequence of the Acinetobacter calcoaceticus trpGDC gene cluster. Mol Biol Evol. 1984 Nov;1(6):456–472. doi: 10.1093/oxfordjournals.molbev.a040331. [DOI] [PubMed] [Google Scholar]
  21. Kaplan J. B., Merkel W. K., Nichols B. P. Evolution of glutamine amidotransferase genes. Nucleotide sequences of the pabA genes from Salmonella typhimurium, Klebsiella aerogenes and Serratia marcescens. J Mol Biol. 1985 Jun 5;183(3):327–340. doi: 10.1016/0022-2836(85)90004-x. [DOI] [PubMed] [Google Scholar]
  22. King J., Lenk E. V., Botstein D. Mechanism of head assembly and DNA encapsulation in Salmonella phage P22. II. Morphogenetic pathway. J Mol Biol. 1973 Nov 15;80(4):697–731. doi: 10.1016/0022-2836(73)90205-2. [DOI] [PubMed] [Google Scholar]
  23. Laemmli U. K., Beguin F., Gujer-Kellenberger G. A factor preventing the major head protein of bacteriophage T4 from random aggregation. J Mol Biol. 1970 Jan 14;47(1):69–85. doi: 10.1016/0022-2836(70)90402-x. [DOI] [PubMed] [Google Scholar]
  24. Lagenaur C., Agabian N. Caulobacter flagellar organelle: synthesis, compartmentation, and assembly. J Bacteriol. 1978 Sep;135(3):1062–1069. doi: 10.1128/jb.135.3.1062-1069.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Loewy Z. G., Bryan R. A., Reuter S. H., Shapiro L. Control of synthesis and positioning of a Caulobacter crescentus flagellar protein. Genes Dev. 1987 Aug;1(6):626–635. doi: 10.1101/gad.1.6.626. [DOI] [PubMed] [Google Scholar]
  26. Macnab R. M., Aizawa S. Bacterial motility and the bacterial flagellar motor. Annu Rev Biophys Bioeng. 1984;13:51–83. doi: 10.1146/annurev.bb.13.060184.000411. [DOI] [PubMed] [Google Scholar]
  27. Mansour J. D., Henry S., Shapiro L. Differential membrane phospholipid synthesis during the cell cycle of Caulobacter crescentus. J Bacteriol. 1980 Jan;141(1):262–269. doi: 10.1128/jb.141.1.262-269.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Minnich S. A., Newton A. Promoter mapping and cell cycle regulation of flagellin gene transcription in Caulobacter crescentus. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1142–1146. doi: 10.1073/pnas.84.5.1142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mullin D., Minnich S., Chen L. S., Newton A. A set of positively regulated flagellar gene promoters in Caulobacter crescentus with sequence homology to the nif gene promoters of Klebsiella pneumoniae. J Mol Biol. 1987 Jun 20;195(4):939–943. doi: 10.1016/0022-2836(87)90497-9. [DOI] [PubMed] [Google Scholar]
  30. Nichols B. P., Blumenberg M., Yanofsky C. Comparison of the nucleoside sequence of trpA and sequences immediately beyond the trp operon of Klebsiella aerogenes. Salmonella typhimurium and Escherichia coli. Nucleic Acids Res. 1981 Apr 10;9(7):1743–1755. doi: 10.1093/nar/9.7.1743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ohta N., Chen L. S., Swanson E., Newton A. Transcriptional regulation of a periodically controlled flagellar gene operon in Caulobacter crescentus. J Mol Biol. 1985 Nov 5;186(1):107–115. doi: 10.1016/0022-2836(85)90261-x. [DOI] [PubMed] [Google Scholar]
  32. Oliver D. Protein secretion in Escherichia coli. Annu Rev Microbiol. 1985;39:615–648. doi: 10.1146/annurev.mi.39.100185.003151. [DOI] [PubMed] [Google Scholar]
  33. Osley M. A., Newton A. Temporal control of the cell cycle in Caulobacter crescentus: roles of DNA chain elongation and completion. J Mol Biol. 1980 Mar 25;138(1):109–128. doi: 10.1016/s0022-2836(80)80007-6. [DOI] [PubMed] [Google Scholar]
  34. Osley M. A., Sheffery M., Newton A. Regulation of flagellin synthesis in the cell cycle of caulobacter: dependence on DNA replication. Cell. 1977 Oct;12(2):393–400. doi: 10.1016/0092-8674(77)90115-5. [DOI] [PubMed] [Google Scholar]
  35. Ross C. M., Winkler M. E. Structure of the Caulobacter crescentus trpFBA operon. J Bacteriol. 1988 Feb;170(2):757–768. doi: 10.1128/jb.170.2.757-768.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Shapiro L., Maizel J. V., Jr Synthesis and structure of Caulobacter crescentus flagella. J Bacteriol. 1973 Jan;113(1):478–485. doi: 10.1128/jb.113.1.478-485.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sheffery M., Newton A. Regulation of periodic protein synthesis in the cell cycle: control of initiation and termination of flagellar gene expression. Cell. 1981 Apr;24(1):49–57. doi: 10.1016/0092-8674(81)90500-6. [DOI] [PubMed] [Google Scholar]
  39. Suzuki T., Iino T., Horiguchi T., Yamaguchi S. Incomplete flagellar structures in nonflagellate mutants of Salmonella typhimurium. J Bacteriol. 1978 Feb;133(2):904–915. doi: 10.1128/jb.133.2.904-915.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Suzuki T., Komeda Y. Incomplete flagellar structures in Escherichia coli mutants. J Bacteriol. 1981 Feb;145(2):1036–1041. doi: 10.1128/jb.145.2.1036-1041.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Szekely E., Simon M. DNA sequence adjacent to flagellar genes and evolution of flagellar-phase variation. J Bacteriol. 1983 Jul;155(1):74–81. doi: 10.1128/jb.155.1.74-81.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wei L. N., Joys T. M. Covalent structure of three phase-1 flagellar filament proteins of Salmonella. J Mol Biol. 1985 Dec 20;186(4):791–803. doi: 10.1016/0022-2836(85)90397-3. [DOI] [PubMed] [Google Scholar]

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

RESOURCES