1887

Microbiology Society logo

Volume 143, Issue 12

A mutation that affects fibril protein, development, cohesion and gene expression in Free

Abstract

Extracellular matrix fibrils are involved in the cell-cell interactions of the social prokaryote, The fibrils are composed of a carbohydrate backbone and a set of five integral fibrillar proteins (IFPs) ranging from 14 to 66 kDa. As part of an attempt to understand the function(s) of the IFPs, a mutant (-1:20) was generated that lacks IFP-1:20, one of the fibril proteins, as shown by Western blot analysis of both whole cells and isolated fibrils. Unlike those of the parent strain, the fibrils of the mutant were removed easily from the cells by shear forces. Development in was aberrant - aggregation and early mound formation were delayed by 6-10 h and mature fruiting bodies never formed. Myxospore production was also greatly reduced. Additionally, fibril-mediated cohesion in was changed. Cohesion resulted in chains of cells rather than the characteristic clumps of cells seen for the parent strain. Isolated fibrils, unlike wild-type fibrils, could not rescue cohesion of non-cohesive, fibril-negative cells, supporting the notion that the fibrils were functionally altered. The mutation also reduced developmental gene expression by three- to fourfold in Ω4521, a transposon insertion mutant expressed early in development. Expression of a later developmental gene fusion was not affected, suggesting that the fibrils may not be required for later developmental gene expression. These data suggest that intact fibrils may function early in development to facilitate close cell proximity for signal exchange.

  • Published Online:
Keyword(s): end-to-end cohesion , fibrils , Myxococcus xanthus and pili
© Society For General Microbiology 1997
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-143-12-3683
1997-12-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/143/12/mic-143-12-3683.html?itemId=/content/journal/micro/10.1099/00221287-143-12-3683&mimeType=html&fmt=ahah

References

  1. Arnold J.W., Shimkets LJ. 1988a; Cell surface properties correlated with cohesion in Myxococcus xanthus. . J Bacterial 170:5771–5777
     [Google Scholar]
  2. Arnold J.W., Shimkets LJ. 1988b; Inhibition of cell-cell interactions in Myxococcus xanthus by Congo red.. J Bacterial 170:5765–5770
     [Google Scholar]
  3. Behmlander R.M., Dworkin M. 1991; Extracellular fibrils and contact-mediated cell interactions in Myxococcus xanthus. . J Bacterial 173:7810–7821
     [Google Scholar]
  4. Behmlander R.M., Dworkin M. 1994a; Biochemical and structural analysis of the extracellular matrix fibrils of Myxococcus xanthus. . J Bacteriol 176:6295–6303
     [Google Scholar]
  5. Behmlander R.M., Dworkin M. 1994b; Integral proteins of the extracellular matrix fibrils of Myxococcus xanthus. . J Bacteriol 176:6304–6311
     [Google Scholar]
  6. Campos J.M., Gersselsoder J., Zusman D.R. 1978; Isolation of bacteriophage MX4, a generalized transducing phage for Myxococcus xanthus. . J Mol Biol 119:167–178
     [Google Scholar]
  7. Chang B.Y., Dworkin M. 1994; Isolated fibrils rescue cohesion and development in the dsp mutant of Myxococcus xanthus. . J Bacteriol 176:7190–7196
     [Google Scholar]
  8. Chang B.Y., White D. 1992; Cell-surface modifications induced by calcium ion in the myxobacterium Stigmatella aurantiaca. . J Bacteriol 174:5780–5787
     [Google Scholar]
  9. Clemens D.L, Chance C. M., Dworkin M. 1991; A develop-ment-specific protein in Myxococcus xanthus is associated with the extracellular fibrils.. J Bacteriol 173:6749–6759
     [Google Scholar]
  10. Dworkin M. 1996; Recent advances in the social and developmental biology of the Myxobacteria.. Microbiol Rev 60:70–102
     [Google Scholar]
  11. Dworkin M., Kaiser D. 1993 Myxobacteria II Washington, DC: American Society for Microbiology;
     [Google Scholar]
  12. Emerson D., Ghiorse W.C. 1993; Role of disulfide bonds in maintaining the structural integrity of the sheath of Leptothrix discophora SP-6.. J Bacteriol 175:7819–7827
     [Google Scholar]
  13. Gill J., Stellwag E., Dworkin M. 1985; Monoclonal antibodies against cell surface antigens of developing cells of Myxococcus xanthus. . Ann Inst Pasteur Microbiol 136A:11–18
     [Google Scholar]
  14. Ginocchio C.C., Olmsted S.B., Wells C.L., Galán j.E. 1994; Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. . Cell 76:717–724
     [Google Scholar]
  15. Hodge J.E., Hofreiter B.T. 1962; Determination of reducing sugar and carbohydrates.. Methods Carbohydr Chem 1:380–394
     [Google Scholar]
  16. Hodgkin J., Kaiser D. 1977; Cell-cell stimulation of movement in nonmotile mutants of Myxococcus. . Proc Natl Acad Sci USA 742938–2942
     [Google Scholar]
  17. Kaiser D. 1979; Social gliding is correlated with the presence of pili in Myxococcus xantbus. . Proc Natl Acad Set USA 765952–5956
     [Google Scholar]
  18. Kaiser D., Kroos L. 1993; Intercellular signalling.. In Myxo- bacteria II pp. 257–283 Edited by Dworkin M., Kaiser D. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  19. Kaplan H.B., Plamann L. 1996; A Myxococcus xantbus cell density-sensing system required for multicellular development.. FEMS Microbiol Lett 139:89–95
     [Google Scholar]
  20. Kaplan H.B., Kuspa A., Kaiser D. 1991; Suppressors that permit A-signal-independent developmental gene expression in Myxococcus xantbus. . J Bacteriol 173:1460–1470
     [Google Scholar]
  21. Kashefi K., Hartzell P.L. 1995; Genetic suppression and phenotypic masking of a Myxococcus xantbus FrzF (−) defect.. Mol Microbiol 15:483–494
     [Google Scholar]
  22. Kim S.K., Kaiser D. 1990; Cell alignment required in differentiation of Myxococcus xantbus. . Science 249:926–928
     [Google Scholar]
  23. Kuspa A., Kroos L., Kaiser D. 1986; Intercellular signalling is required for developmental gene expression in Myxococcus xantbus. . Dev Biol 117:267–276
     [Google Scholar]
  24. Kuspa A., Plamann L., Kaiser D. 1992; A-signalling and the cell density requirement for Myxococcus xantbus development.. J Bacteriol 174:7360–7369
     [Google Scholar]
  25. Laemmli U.K. 1970; Cleavage of structural proteins during assembly of the head of bacteriophage T4.. Nature 227:680–685
     [Google Scholar]
  26. McBride M.J., Hartzell P., Zusman D.R. 1993; Motility and tactic behavior in Myxococcus xantbus. . In Myxobacteria II pp. 285–305 Edited by Dworkin M., Kaiser D. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  27. Mackie E.B., Brown K.N., Lam J., Costerton J.W. 1979; Morphological stabilization of capsules of group B streptococci, Types la, lb, and III, with specific antibody.. J Bacteriol 138:609–617
     [Google Scholar]
  28. Morrison C., Zusman D. 1979; Mutants with temperature- sensitive stage-specific defects: evidence for independent pathways in development.. J Bacteriol 140:1036–1042
     [Google Scholar]
  29. Munoz-Dorado J., Inouye S., Inouye M. 1991; A gene encoding a protein serine/ threonine kinase is required for normal development of M.xantbus, a Gram-negative bacterium.. Cell 67:995–1006
     [Google Scholar]
  30. Prentki P., Krisch M. 1984; In vitro insertional mutagenesis with a selectable DNA fragment.. Gene 29:303–313
     [Google Scholar]
  31. Sambrook J., Fritsch E.F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  32. Shimkets L.J. 1984; Nutrition, metabolism, and the initiation of development.. In Myxobacteria: Development and Cell Interactions pp. 91–107 Edited by Rosenberg E. New York: Springer;
     [Google Scholar]
  33. Shimkets L.J. 1986; Role of cell cohesion in Myxococcus xantbus fruiting-body formation.. J Bacteriol 166:842–848
     [Google Scholar]
  34. Shimkets L.J. 1990; Social and developmental biology of the Myxobacteria. . Microbiol Rev 54:473–501
     [Google Scholar]
  35. Shimkets L.J., Rafiee H. 1990; CsgA, an extracellular protein essential for Myxococcus xantbus development.. J Bacteriol 172:5299–5306
     [Google Scholar]
  36. Segaard-Andersen L., Kaiser D. 1996; C factor, a cell-surface- associated intercellular signalling protein, stimulates the cytoplasmic Frz signal transduction system in Myxococcus xantbus. . Proc Natl Acad Sci USA 932675–2679
     [Google Scholar]
  37. Wu S.S., Wu J., Kaiser D. 1997; The Myxococcus xantbus pilT locus is required for social gliding motility although pili are still produced.. Mol Microbiol 23:109–121
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-143-12-3683
Loading
A mutation that affects fibril protein, development, cohesion and gene expression in Myxococcus xanthus
Microbiology 143, 3683 (1997); https://doi.org/10.1099/00221287-143-12-3683
/content/journal/micro/10.1099/00221287-143-12-3683
/content/journal/micro/10.1099/00221287-143-12-3683
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error