Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1996 Nov;178(22):6525–6538. doi: 10.1128/jb.178.22.6525-6538.1996

Periodic phenomena in Proteus mirabilis swarm colony development.

O Rauprich 1, M Matsushita 1, C J Weijer 1, F Siegert 1, S E Esipov 1, J A Shapiro 1
PMCID: PMC178539  PMID: 8932309

Abstract

Proteus mirabilis colonies exhibit striking geometric regularity. Basic microbiological methods and imaging techniques were used to measure periodic macroscopic events in swarm colony morphogenesis. We distinguished three initial phases (lag phase, first swarming phase, and first consolidation phase) followed by repeating cycles of subsequent swarming plus consolidation phases. Each Proteus swarm colony terrace corresponds to one swarming-plus-consolidation cycle. The duration of the lag phase was dependent upon inoculation density in a way that indicated the operation of both cooperative and inhibitory multicellular effects. On our standard medium, the second and subsequent swarm phases displayed structure in the form of internal waves visible with reflected and dark-field illumination. These internal waves resulted from organization of the migrating bacteria into successively thicker cohorts of swarmer cells. Bacterial growth and motility were independently modified by altering the composition of the growth medium. By varying the glucose concentration in the substrate, it was possible to alter biomass production without greatly affecting the kinetics of colony surface area expansion. By varying the agar concentration in the substrate, initial bacterial biomass production was unaffected but colony expansion dynamics were significantly altered. Higher agar concentrations led to slower, shorter swarm phases and longer consolidation phases. Thus, colony growth was restricted by higher agar concentrations but the overall timing of the swarming-plus-consolidation cycles remained constant. None of a variety of factors which had significant effects on colony expansion altered terracing frequencies at 32 degrees C, but the length of the swarming-plus-consolidation cycle was affected by temperature and medium enrichment. Some clinical isolates displayed significant differences in terracing frequencies at 32 degrees C. Our results defined a number of readily quantifiable parameters in swarm colony development. The data showed no connection between nutrient (glucose) depletion and the onset of different phases in swarm colony morphogenesis. Several observations point to the operation of density-dependent thresholds in controlling the transitions between distinct phases.

Full Text

The Full Text of this article is available as a PDF (1.9 MB).

Selected References

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

  1. Allison C., Hughes C. Bacterial swarming: an example of prokaryotic differentiation and multicellular behaviour. Sci Prog. 1991;75(298 Pt 3-4):403–422. [PubMed] [Google Scholar]
  2. Allison C., Hughes C. Closely linked genetic loci required for swarm cell differentiation and multicellular migration by Proteus mirabilis. Mol Microbiol. 1991 Aug;5(8):1975–1982. doi: 10.1111/j.1365-2958.1991.tb00819.x. [DOI] [PubMed] [Google Scholar]
  3. Belas R., Erskine D., Flaherty D. Proteus mirabilis mutants defective in swarmer cell differentiation and multicellular behavior. J Bacteriol. 1991 Oct;173(19):6279–6288. doi: 10.1128/jb.173.19.6279-6288.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Belas R., Erskine D., Flaherty D. Transposon mutagenesis in Proteus mirabilis. J Bacteriol. 1991 Oct;173(19):6289–6293. doi: 10.1128/jb.173.19.6289-6293.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bisset K. A., Douglas C. W. A continuous study of morphological phase in the swarm of Proteus. J Med Microbiol. 1976 May;9(2):229–231. doi: 10.1099/00222615-9-2-229. [DOI] [PubMed] [Google Scholar]
  6. Bisset K. A. The zonation phenomenon and structure of the swarm colony in Proteus mirabilis. J Med Microbiol. 1973 Nov;6(4):429–433. doi: 10.1099/00222615-6-4-429. [DOI] [PubMed] [Google Scholar]
  7. Eberl L., Winson M. K., Sternberg C., Stewart G. S., Christiansen G., Chhabra S. R., Bycroft B., Williams P., Molin S., Givskov M. Involvement of N-acyl-L-hormoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol Microbiol. 1996 Apr;20(1):127–136. doi: 10.1111/j.1365-2958.1996.tb02495.x. [DOI] [PubMed] [Google Scholar]
  8. FLEMING A. Motilité et cils de Proteus vulgaris. Ann Inst Pasteur (Paris) 1950 Nov;79(5):604–611. [PubMed] [Google Scholar]
  9. Gygi D., Rahman M. M., Lai H. C., Carlson R., Guard-Petter J., Hughes C. A cell-surface polysaccharide that facilitates rapid population migration by differentiated swarm cells of Proteus mirabilis. Mol Microbiol. 1995 Sep;17(6):1167–1175. doi: 10.1111/j.1365-2958.1995.mmi_17061167.x. [DOI] [PubMed] [Google Scholar]
  10. HOENIGER J. F. CELLULAR CHANGES ACCOMPANYING THE SWARMING OF PROTEUS MIRABILIS. I. OBSERVATIONS OF LIVING CULTURES. Can J Microbiol. 1964 Feb;10:1–9. doi: 10.1139/m64-001. [DOI] [PubMed] [Google Scholar]
  11. Jones H. E., Park R. W. The influence of medium composition on the growth and swarming of Proteus. J Gen Microbiol. 1967 Jun;47(3):369–378. doi: 10.1099/00221287-47-3-369. [DOI] [PubMed] [Google Scholar]
  12. Jones H. E., Park R. W. The short forms and long forms of Proteus. J Gen Microbiol. 1967 Jun;47(3):359–367. doi: 10.1099/00221287-47-3-359. [DOI] [PubMed] [Google Scholar]
  13. Nieder M., Shapiro J. Physiological function of the Pseudomonas putida PpG6 (Pseudomonas oleovorans) alkane hydroxylase: monoterminal oxidation of alkanes and fatty acids. J Bacteriol. 1975 Apr;122(1):93–98. doi: 10.1128/jb.122.1.93-98.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Shapiro J. A. Scanning electron microscope study of Pseudomonas putida colonies. J Bacteriol. 1985 Dec;164(3):1171–1181. doi: 10.1128/jb.164.3.1171-1181.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Shapiro J. A. The significances of bacterial colony patterns. Bioessays. 1995 Jul;17(7):597–607. doi: 10.1002/bies.950170706. [DOI] [PubMed] [Google Scholar]
  16. Stahl S. J., Stewart K. R., Williams F. D. Extracellular slime associated with Proteus mirabilis during swarming. J Bacteriol. 1983 May;154(2):930–937. doi: 10.1128/jb.154.2.930-937.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Sturdza S. A. Développement des cultures de Proteus sur gélose nutritive après mise en contact avec un milieu neuf. Arch Roum Pathol Exp Microbiol. 1973 Jun;32(2):179–183. [PubMed] [Google Scholar]
  18. Sturdza S. A. Expansion immédiate des Proteus sur milieux gélosés. Arch Roum Pathol Exp Microbiol. 1973 Dec;32(4):543–562. [PubMed] [Google Scholar]
  19. Sturdza S. A. Recent notes on the mechanism of the Proteus swarming phenomenon. A review. Arch Roum Pathol Exp Microbiol. 1978 Apr-Jun;37(2):97–111. [PubMed] [Google Scholar]
  20. Williams F. D., Schwarzhoff R. H. Nature of the swarming phenomenon in Proteus. Annu Rev Microbiol. 1978;32:101–122. doi: 10.1146/annurev.mi.32.100178.000533. [DOI] [PubMed] [Google Scholar]

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

RESOURCES