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. 1990 Nov;172(11):6476–6493. doi: 10.1128/jb.172.11.6476-6493.1990

Defects in contact-stimulated gliding during aggregation by Myxococcus xanthus.

M Kalos 1, J F Zissler 1
PMCID: PMC526836  PMID: 2172215

Abstract

During development, Myxococcus xanthus cells glide toward foci of aggregation and produce compact multicellular mounds. We studied development in strains with defects in contact-stimulated gliding. Contact stimulation involves a mechanism influenced by contacts between neighboring cells which stimulates the gliding motility of single cells (Hodgkin and Kaiser, Proc. Natl. Acad. Sci. USA 74:2938-2942, 1977; Hodgkin and Kaiser, Mol. Gen. Genet. 171:167-176, 1979). Most mutants containing a mutation in a single gene affecting contact stimulation (cgl gene) were able to form foci of aggregation during development. However, the aggregates were diffuse, suggesting that contact stimulation is important for morphogenetic movements during aggregation. A mutant containing a mutation in the cglF3 gene showed a striking delay in aggregation, suggesting that the cglF3 gene affects a mechanism stimulating cells moving to foci or affects a mechanism for coordinating early cell behavior. Mutants containing the cglF3 mutation in combination with a cglB, cglC, cglE, or cglF1 mutation had severe defects in aggregation and failed to recover from the early delay. The severity of the defects in mutants containing two cgl mutations suggests that cgl genes are critical for development. We propose that cgl genes stimulate cell movement or control specific contacts between cells during aggregation.

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Selected References

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

  1. Blackhart B. D., Zusman D. R. "Frizzy" genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8767–8770. doi: 10.1073/pnas.82.24.8767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burchard A. C., Burchard R. P., Kloetzel J. A. Intracellular, periodic structures in the gliding bacterium Myxococcus xanthus. J Bacteriol. 1977 Nov;132(2):666–672. doi: 10.1128/jb.132.2.666-672.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burchard R. P. Gliding motility of prokaryotes: ultrastructure, physiology, and genetics. Annu Rev Microbiol. 1981;35:497–529. doi: 10.1146/annurev.mi.35.100181.002433. [DOI] [PubMed] [Google Scholar]
  4. DWORKIN M. Nutritional requirements for vegetative growth of Myxococcus xanthus. J Bacteriol. 1962 Aug;84:250–257. doi: 10.1128/jb.84.2.250-257.1962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Doetsch R. N., Hageage G. J. Motility in procaryotic organisms: problems, points of view, and perspectives. Biol Rev Camb Philos Soc. 1968 Aug;43(3):317–362. doi: 10.1111/j.1469-185x.1968.tb00963.x. [DOI] [PubMed] [Google Scholar]
  6. Dworkin M., Keller K. H., Weisberg D. Experimental observations consistent with a surface tension model of gliding motility of Myxococcus xanthus. J Bacteriol. 1983 Sep;155(3):1367–1371. doi: 10.1128/jb.155.3.1367-1371.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fink J. M., Kalos M., Zissler J. F. Isolation of cell surface antigen mutants of Myxococcus xanthus by use of monoclonal antibodies. J Bacteriol. 1989 Apr;171(4):2033–2041. doi: 10.1128/jb.171.4.2033-2041.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fink J. M., Zissler J. F. Characterization of lipopolysaccharide from Myxococcus xanthus by use of monoclonal antibodies. J Bacteriol. 1989 Apr;171(4):2028–2032. doi: 10.1128/jb.171.4.2028-2032.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fink J. M., Zissler J. F. Defects in motility and development of Myxococcus xanthus lipopolysaccharide mutants. J Bacteriol. 1989 Apr;171(4):2042–2048. doi: 10.1128/jb.171.4.2042-2048.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gill J. S., Dworkin M. Cell surface antigens during submerged development of Myxococcus xanthus examined with monoclonal antibodies. J Bacteriol. 1986 Nov;168(2):505–511. doi: 10.1128/jb.168.2.505-511.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gill J., Stellwag E., Dworkin M. Monoclonal antibodies against cell-surface antigens of developing cells of Myxococcus xanthus. Ann Inst Pasteur Microbiol. 1985 Jan-Feb;136A(1):11–18. doi: 10.1016/s0769-2609(85)80015-6. [DOI] [PubMed] [Google Scholar]
  12. Henrichsen J. Bacterial surface translocation: a survey and a classification. Bacteriol Rev. 1972 Dec;36(4):478–503. doi: 10.1128/br.36.4.478-503.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hodgkin J., Kaiser D. Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2938–2942. doi: 10.1073/pnas.74.7.2938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kaiser D. Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5952–5956. doi: 10.1073/pnas.76.11.5952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kim S. K., Kaiser D. C-factor: a cell-cell signaling protein required for fruiting body morphogenesis of M. xanthus. Cell. 1990 Apr 6;61(1):19–26. doi: 10.1016/0092-8674(90)90211-v. [DOI] [PubMed] [Google Scholar]
  16. Kroos L., Hartzell P., Stephens K., Kaiser D. A link between cell movement and gene expression argues that motility is required for cell-cell signaling during fruiting body development. Genes Dev. 1988 Dec;2(12A):1677–1685. doi: 10.1101/gad.2.12a.1677. [DOI] [PubMed] [Google Scholar]
  17. Kroos L., Kaiser D. Expression of many developmentally regulated genes in Myxococcus depends on a sequence of cell interactions. Genes Dev. 1987 Oct;1(8):840–854. doi: 10.1101/gad.1.8.840. [DOI] [PubMed] [Google Scholar]
  18. Kroos L., Kuspa A., Kaiser D. A global analysis of developmentally regulated genes in Myxococcus xanthus. Dev Biol. 1986 Sep;117(1):252–266. doi: 10.1016/0012-1606(86)90368-4. [DOI] [PubMed] [Google Scholar]
  19. Kuner J. M., Kaiser D. Fruiting body morphogenesis in submerged cultures of Myxococcus xanthus. J Bacteriol. 1982 Jul;151(1):458–461. doi: 10.1128/jb.151.1.458-461.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lapidus I. R., Berg H. C. Gliding motility of Cytophaga sp. strain U67. J Bacteriol. 1982 Jul;151(1):384–398. doi: 10.1128/jb.151.1.384-398.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Manoil C., Beckwith J. TnphoA: a transposon probe for protein export signals. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8129–8133. doi: 10.1073/pnas.82.23.8129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Martin S., Sodergren E., Masuda T., Kaiser D. Systematic isolation of transducing phages for Myxococcus xanthus. Virology. 1978 Jul 1;88(1):44–53. doi: 10.1016/0042-6822(78)90108-3. [DOI] [PubMed] [Google Scholar]
  23. McBride M. J., Weinberg R. A., Zusman D. R. "Frizzy" aggregation genes of the gliding bacterium Myxococcus xanthus show sequence similarities to the chemotaxis genes of enteric bacteria. Proc Natl Acad Sci U S A. 1989 Jan;86(2):424–428. doi: 10.1073/pnas.86.2.424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. O'Connor K. A., Zusman D. R. Patterns of cellular interactions during fruiting-body formation in Myxococcus xanthus. J Bacteriol. 1989 Nov;171(11):6013–6024. doi: 10.1128/jb.171.11.6013-6024.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Shimkets L. J. Control of morphogenesis in myxobacteria. Crit Rev Microbiol. 1987;14(3):195–227. doi: 10.3109/10408418709104439. [DOI] [PubMed] [Google Scholar]
  26. Shimkets L. J. Correlation of energy-dependent cell cohesion with social motility in Myxococcus xanthus. J Bacteriol. 1986 Jun;166(3):837–841. doi: 10.1128/jb.166.3.837-841.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shimkets L. J., Gill R. E., Kaiser D. Developmental cell interactions in Myxococcus xanthus and the spoC locus. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1406–1410. doi: 10.1073/pnas.80.5.1406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shimkets L. J., Kaiser D. Induction of coordinated movement of Myxococcus xanthus cells. J Bacteriol. 1982 Oct;152(1):451–461. doi: 10.1128/jb.152.1.451-461.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shimkets L. J. Role of cell cohesion in Myxococcus xanthus fruiting body formation. J Bacteriol. 1986 Jun;166(3):842–848. doi: 10.1128/jb.166.3.842-848.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sodergren E., Kaiser D. Insertions of Tn5 near genes that govern stimulatable cell motility in Myxococcus. J Mol Biol. 1983 Jun 25;167(2):295–310. doi: 10.1016/s0022-2836(83)80337-4. [DOI] [PubMed] [Google Scholar]
  31. Vasquez G. M., Qualls F., White D. Morphogenesis of Stigmatella aurantiaca fruiting bodies. J Bacteriol. 1985 Aug;163(2):515–521. doi: 10.1128/jb.163.2.515-521.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Weinberg R. A., Zusman D. R. Alkaline, acid, and neutral phosphatase activities are induced during development in Myxococcus xanthus. J Bacteriol. 1990 May;172(5):2294–2302. doi: 10.1128/jb.172.5.2294-2302.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Weinberg R. A., Zusman D. R. Evidence that the Myxococcus xanthus frz genes are developmentally regulated. J Bacteriol. 1989 Nov;171(11):6174–6186. doi: 10.1128/jb.171.11.6174-6186.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Zusman D. R. "Frizzy" mutants: a new class of aggregation-defective developmental mutants of Myxococcus xanthus. J Bacteriol. 1982 Jun;150(3):1430–1437. doi: 10.1128/jb.150.3.1430-1437.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]

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