Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 Jan;179(1):148–156. doi: 10.1128/jb.179.1.148-156.1997

Fine-structure evidence for cell membrane partitioning of the nucleoid and cytoplasm during bud formation in Hyphomonas species.

P M Zerfas 1, M Kessel 1, E J Quintero 1, R M Weiner 1
PMCID: PMC178673  PMID: 8981992

Abstract

Hyphomonas spp. reproduce by budding from the tip of the prosthecum, distal to the main body of the reproductive cell; thus, the chromosome must travel through the prosthecum to enter the progeny, the swarm cell. When viewed by electron microscopy, negatively stained whole cells, ultrathin-sectioned cells, and freeze-etched and frozen hydrated cells all had marked swellings of the cytoplasmic membrane (CM) in the prosthecum which are termed pseudovesicles (PV). PV were separated by constrictions in the contiguous CM. In replicating cells, PV housed ribosomes and DNA, which was identified by its fibrillar appearance and by lactoferrin-gold labeling. The micrographs also revealed that the CM bifurcates at the origin of the prosthecum so that one branch partitions the main body of the reproductive cell from the prosthecum and swarm cell. The results of this fine-structure analysis suggest models explaining DNA segregation and the marked asymmetric polarity of the budding reproductive cell.

Full Text

The Full Text of this article is available as a PDF (2.1 MB).

Selected References

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

  1. BOATMAN E. S., DOUGLAS H. C. Fine structure of the photosynthetic bacterium Rhodomicrobium vannielii. J Biophys Biochem Cytol. 1961 Nov;11:469–483. doi: 10.1083/jcb.11.2.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bendayan M. Ultrastructural localization of nuclei acids by the use of enzyme-gold complexes. J Histochem Cytochem. 1981 Apr;29(4):531–541. doi: 10.1177/29.4.6265546. [DOI] [PubMed] [Google Scholar]
  3. Benhamou N. Ultrastructural localization of DNA on ultrathin sections of resin-embedded tissues by the lactoferrin-gold complex. J Electron Microsc Tech. 1989 May;12(1):1–10. doi: 10.1002/jemt.1060120102. [DOI] [PubMed] [Google Scholar]
  4. CONTI S. F., HIRSCH P. BIOLOGY OF BUDDING BACTERIA. 3. FINE STRUCTURE OF RHODOMICROBIUM AND HYPHOMICROBIUM SPP. J Bacteriol. 1965 Feb;89:503–512. doi: 10.1128/jb.89.2.503-512.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cavalier-Smith T. Bacterial DNA segregation: its motors and positional control. J Theor Biol. 1987 Aug 7;127(3):361–372. doi: 10.1016/s0022-5193(87)80112-1. [DOI] [PubMed] [Google Scholar]
  6. Emala M. A., Weiner R. M. Modulation of adenylate energy charge during the swarmer cycle of Hyphomicrobium neptunium. J Bacteriol. 1983 Mar;153(3):1558–1561. doi: 10.1128/jb.153.3.1558-1561.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hiraga S., Ogura T., Niki H., Ichinose C., Mori H. Positioning of replicated chromosomes in Escherichia coli. J Bacteriol. 1990 Jan;172(1):31–39. doi: 10.1128/jb.172.1.31-39.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Moore R. L., Hirsch P. Nuclear apparatus of Hyphomicrobium. J Bacteriol. 1973 Dec;116(3):1447–1455. doi: 10.1128/jb.116.3.1447-1455.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Norris V. DNA replication in Escherichia coli is initiated by membrane detachment of oriC. A model. J Mol Biol. 1990 Sep 5;215(1):67–71. doi: 10.1016/s0022-2836(05)80095-6. [DOI] [PubMed] [Google Scholar]
  10. Peebles C. L., Higgins N. P., Kreuzer K. N., Morrison A., Brown P. O., Sugino A., Cozzarelli N. R. Structure and activities of Escherichia coli DNA gyrase. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 1):41–52. doi: 10.1101/sqb.1979.043.01.008. [DOI] [PubMed] [Google Scholar]
  11. Quintero E. J., Weiner R. M. Evidence for the Adhesive Function of the Exopolysaccharide of Hyphomonas Strain MHS-3 in Its Attachment to Surfaces. Appl Environ Microbiol. 1995 May;61(5):1897–1903. doi: 10.1128/aem.61.5.1897-1903.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. RYTER A., KELLENBERGER E., BIRCHANDERSEN A., MAALOE O. Etude au microscope électronique de plasmas contenant de l'acide désoxyribonucliéique. I. Les nucléoides des bactéries en croissance active. Z Naturforsch B. 1958 Sep;13B(9):597–605. [PubMed] [Google Scholar]
  13. Shen N., Dagasan L., Sledjeski D., Weiner R. M. Major outer membrane proteins unique to reproductive cells of Hyphomonas jannaschiana. J Bacteriol. 1989 Apr;171(4):2226–2228. doi: 10.1128/jb.171.4.2226-2228.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Spurr A. R. A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res. 1969 Jan;26(1):31–43. doi: 10.1016/s0022-5320(69)90033-1. [DOI] [PubMed] [Google Scholar]
  15. Wali T. M., Hudson G. R., Danald D. A., Weiner R. M. Timing of swarmer cell cycle morphogenesis and macromolecular synthesis by Hyphomicrobium neptunium in synchronous culture. J Bacteriol. 1980 Oct;144(1):406–412. doi: 10.1128/jb.144.1.406-412.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Weiner R. M., Blackman M. A. Inhibition of deoxyribonucleic acid synthesis and bud formation by nalidixic acid in Hyphomicrobium neptunium. J Bacteriol. 1973 Dec;116(3):1398–1404. doi: 10.1128/jb.116.3.1398-1404.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Whittenbury R., Dow C. S. Morphogenesis and differentiation in Rhodomicrobium vannielii and other budding and prosthecate bacteria. Bacteriol Rev. 1977 Sep;41(3):754–808. doi: 10.1128/br.41.3.754-808.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Woldringh C. L., Zaritsky A., Grover N. B. Nucleoid partitioning and the division plane in Escherichia coli. J Bacteriol. 1994 Oct;176(19):6030–6038. doi: 10.1128/jb.176.19.6030-6038.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Wu L. J., Errington J. Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division. Science. 1994 Apr 22;264(5158):572–575. doi: 10.1126/science.8160014. [DOI] [PubMed] [Google Scholar]
  20. de Boer P. A. Chromosome segregation and cytokinesis in bacteria. Curr Opin Cell Biol. 1993 Apr;5(2):232–237. doi: 10.1016/0955-0674(93)90108-3. [DOI] [PubMed] [Google Scholar]

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

RESOURCES