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. 1989 Sep;171(9):4814–4820. doi: 10.1128/jb.171.9.4814-4820.1989

Cell-cycle-dependent polar morphogenesis in Caulobacter crescentus: roles of phospholipid, DNA, and protein syntheses.

E A O'Neill 1, R A Bender 1
PMCID: PMC210284  PMID: 2768189

Abstract

During swarmer cell differentiation in Caulobacter crescentus, morphogenesis at the swarmer pole is characterized by the loss of the flagellum, by the loss of phage receptor activity (PRA) (the ability of the cell to adsorb phage phi CbK), and finally by the initiation of stalk outgrowth at the site formerly occupied by the flagellum and the PRA. We show here that each of these events is a cell cycle-dependent event requiring continuous protein synthesis for its execution but occurring normally in the absence of DNA synthesis or phospholipid synthesis. During stalked-cell differentiation, the flagellum and PRA reappear and the stalk elongates considerably. We show here that these events are also cell cycle dependent, requiring not only de novo protein synthesis but also DNA and phospholipid syntheses. When synchronous cells dividing 160 min after collection were used, PRA reappearance occurred at 110 min. This PRA reappearance was dependent on a phospholipid synthesis-requiring event occurring at 70 min, a DNA synthesis-requiring event occurring at 95 min, and a protein synthesis-requiring event occurring at 108 min. In the absence of net phospholipid synthesis, stalk elongation appeared more or less normal, but the stalks eventually became fragile, and by 240 min, most of the stalks had broken off, leaving only stubs attached to the cell body.

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Selected References

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  1. Agabian-Keshishian N., Shapiro L. Bacterial differentiation and phage infection. Virology. 1971 Apr;44(1):46–53. doi: 10.1016/0042-6822(71)90151-6. [DOI] [PubMed] [Google Scholar]
  2. Agabian-Keshishian N., Shapiro L. Stalked bacteria: properties of deoxriybonucleic acid bacteriophage phiCbK. J Virol. 1970 Jun;5(6):795–800. doi: 10.1128/jvi.5.6.795-800.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bender R. A., Refson C. M., O'Neill E. A. Role of the flagellum in cell-cycle-dependent expression of bacteriophage receptor activity in Caulobacter crescentus. J Bacteriol. 1989 Feb;171(2):1035–1040. doi: 10.1128/jb.171.2.1035-1040.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Contreras I., Bender R. A., Mansour J., Henry S., Shapiro L. Caulobacter cresentus mutant defective in membrane phospholipid synthesis. J Bacteriol. 1979 Nov;140(2):612–619. doi: 10.1128/jb.140.2.612-619.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Contreras I., Weissborn A., Amemiya K., Mansour J., Henry S., Shapiro L., Bender R. The effect of termination of membrane phospholipid synthesis on cell-dependent events in Caulobacter. J Mol Biol. 1980 Apr;138(2):401–409. doi: 10.1016/0022-2836(80)90295-8. [DOI] [PubMed] [Google Scholar]
  7. Degnen S. T., Newton A. Chromosome replication during development in Caulobacter crescentus. J Mol Biol. 1972 Mar 14;64(3):671–680. doi: 10.1016/0022-2836(72)90090-3. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. Huguenel E. D., Newton A. Localization of surface structures during procaryotic differentiation: role of cell division in Caulobacter crescentus. Differentiation. 1982;21(2):71–78. doi: 10.1111/j.1432-0436.1982.tb01199.x. [DOI] [PubMed] [Google Scholar]
  11. Johnson R. C., Ely B. Isolation of spontaneously derived mutants of Caulobacter crescentus. Genetics. 1977 May;86(1):25–32. doi: 10.1093/genetics/86.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Johnson R. C., Ferber D. M., Ely B. Synthesis and assembly of flagellar components by Caulobacter crescentus motility mutants. J Bacteriol. 1983 Jun;154(3):1137–1144. doi: 10.1128/jb.154.3.1137-1144.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lagenaur C., Agabian N. Physical characterization of Caulobacter crescentus flagella. J Bacteriol. 1976 Oct;128(1):435–444. doi: 10.1128/jb.128.1.435-444.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lagenaur C., Farmer S., Agabian N. Adsorption properties of stage-specific Caulobacter phage phiCbK. Virology. 1977 Mar;77(1):401–407. doi: 10.1016/0042-6822(77)90436-6. [DOI] [PubMed] [Google Scholar]
  15. Newton A. Role of transcription in the temporal control of development in Caulobacter crescentus (stalk-rifampin-RNA synthesis-DNA synthesis-motility). Proc Natl Acad Sci U S A. 1972 Feb;69(2):447–451. doi: 10.1073/pnas.69.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. O'Neill E. A., Bender R. A. Periodic synthesis of phospholipids during the Caulobacter crescentus cell cycle. J Bacteriol. 1987 Jun;169(6):2618–2623. doi: 10.1128/jb.169.6.2618-2623.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. POINDEXTER J. S. BIOLOGICAL PROPERTIES AND CLASSIFICATION OF THE CAULOBACTER GROUP. Bacteriol Rev. 1964 Sep;28:231–295. doi: 10.1128/br.28.3.231-295.1964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Poindexter J. S. The caulobacters: ubiquitous unusual bacteria. Microbiol Rev. 1981 Mar;45(1):123–179. doi: 10.1128/mr.45.1.123-179.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Shapiro L., Agabian-Keshishian N., Bendis I. Bacterial differentiation. Science. 1971 Sep 3;173(4000):884–892. doi: 10.1126/science.173.4000.884. [DOI] [PubMed] [Google Scholar]
  22. Shapiro L. Differentiation in the Caulobacter cell cycle. Annu Rev Microbiol. 1976;30:377–407. doi: 10.1146/annurev.mi.30.100176.002113. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Sommer J. M., Newton A. Sequential regulation of developmental events during polar morphogenesis in Caulobacter crescentus: assembly of pili on swarmer cells requires cell separation. J Bacteriol. 1988 Jan;170(1):409–415. doi: 10.1128/jb.170.1.409-415.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Weissborn A., Steinmann H. M., Shapiro L. Characterization of the proteins of the Caulobacter crescentus flagellar filament. Peptide analysis and filament organization. J Biol Chem. 1982 Feb 25;257(4):2066–2074. [PubMed] [Google Scholar]

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