Skip to content
1887

Abstract

, a Gram-negative soil bacterium, undergoes multicellular development when nutrients become limiting. Aggregation, which is part of the developmental process, requires the surface motility of this organism. One component of motility, the social (S) gliding motility, enables the movement of cells in close physical proximity. Previous studies demonstrated that the cell surface-associated exopolysaccharide (EPS) is essential for S motility and that the Dif proteins form a chemotaxis-like pathway that regulates EPS production in . DifA, a homologue of methyl-accepting chemotaxis proteins (MCPs) in the Dif system, is required for EPS production, S motility and development. In this study, a spontaneous extragenic suppressor of a deletion was isolated in order to identify additional regulators of EPS production. The suppressor mutation was found to be a single base pair insertion in at the chemotaxis gene cluster. Further examination indicated that mutations in may lead to the interaction of Mcp7 with DifC (CheW-like) and DifE (CheA-like) to reconstruct a functional pathway to regulate EPS production in the absence of DifA. In addition, the mutation was found to partially suppress a mutation in EPS production in a background. Further deletion of from the double mutant resulted in a triple mutant that produced wild-type levels of EPS, implying that DifA (MCP-like) and Mcp7 compete for interactions with DifC and DifE in the modulation of EPS production.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.031070-0
2009-11-01
2025-02-12
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/11/3599.html?itemId=/content/journal/micro/10.1099/mic.0.031070-0&mimeType=html&fmt=ahah

References

  1. Armitage J. P., Holland I. B., Jenal U., Kenny B. 2005; “Neural networks” in bacteria: making connections. J Bacteriol 187:26–36
    [Google Scholar]
  2. Arshinoff B. I., Suen G., Just E. M., Merchant S. M., Kibbe W. A., Chisholm R. L., Welch R. D. 2007; Xanthusbase: adapting wikipedia principles to a model organism database. Nucleic Acids Res 35:D422–D426
    [Google Scholar]
  3. Beck E., Ludwig G., Auerswald E. A., Reiss B., Schaller H. 1982; Nucleotide sequence and exact localization of the neomycin phosphotransferase gene from transposon Tn 5 . Gene 19:327–336
    [Google Scholar]
  4. Bellenger K., Ma X., Shi W., Yang Z. 2002; A CheW homologue is required for Myxococcus xanthus fruiting body development, social gliding motility, and fibril biogenesis. J Bacteriol 184:5654–5660
    [Google Scholar]
  5. Black W. P., Yang Z. 2004; Myxococcus xanthus chemotaxis homologs DifD and DifG negatively regulate fibril polysaccharide production. J Bacteriol 186:1001–1008
    [Google Scholar]
  6. Black W. P., Xu Q., Yang Z. 2006; Type IV pili function upstream of the Dif chemotaxis pathway in Myxococcus xanthus EPS regulation. Mol Microbiol 61:447–456
    [Google Scholar]
  7. Bonner P. J., Xu Q., Black W. P., Li Z., Yang Z., Shimkets L. J. 2005; The Dif chemosensory pathway is directly involved in phosphatidylethanolamine sensory transduction in Myxococcus xanthus . Mol Microbiol 57:1499–1508
    [Google Scholar]
  8. Bonner P. J., Black W. P., Yang Z., Shimkets L. J. 2006; FibA and PilA act cooperatively during fruiting body formation of Myxococcus xanthus . Mol Microbiol 61:1283–1293
    [Google Scholar]
  9. Bourret R. B., Stock A. M. 2002; Molecular information processing: lessons from bacterial chemotaxis. J Biol Chem 277:9625–9628
    [Google Scholar]
  10. Bren A., Eisenbach M. 2000; How signals are heard during bacterial chemotaxis: protein–protein interactions in sensory signal propagation. J Bacteriol 182:6865–6873
    [Google Scholar]
  11. Campos J. M., Zusman D. R. 1975; Regulation of development in Myxococcus xanthus: effect of 3′: 5′-cyclic AMP, ADP, and nutrition. Proc Natl Acad Sci U S A 72:518–522
    [Google Scholar]
  12. Dana J. R., Shimkets L. J. 1993; Regulation of cohesion-dependent cell interactions in Myxococcus xanthus . J Bacteriol 175:3636–3647
    [Google Scholar]
  13. Goldman B. S., Nierman W. C., Kaiser D., Slater S. C., Durkin A. S., Eisen J. A., Ronning C. M., Barbazuk W. B., Blanchard M. other authors 2006; Evolution of sensory complexity recorded in a myxobacterial genome. Proc Natl Acad Sci U S A 103:15200–15205
    [Google Scholar]
  14. Hagen D. C., Bretscher A. P., Kaiser D. 1978; Synergism between morphogenetic mutants of Myxococcus xanthus . Dev Biol 64:284–296
    [Google Scholar]
  15. Hodgkin J., Kaiser D. 1979a; Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): genes controlling movement of single cells. Mol Gen Genet 171:167–176
    [Google Scholar]
  16. Hodgkin J., Kaiser D. 1979b; Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): two gene systems control movement. Mol Gen Genet 171:177–191
    [Google Scholar]
  17. Julien B., Kaiser A. D., Garza A. 2000; Spatial control of cell differentiation in Myxococcus xanthus . Proc Natl Acad Sci U S A 97:9098–9103
    [Google Scholar]
  18. Kaiser D. 1979; Social gliding is correlated with the presence of pili in Myxococcus xanthus . Proc Natl Acad Sci U S A 76:5952–5956
    [Google Scholar]
  19. Kaiser D. 2003; Coupling cell movement to multicellular development in myxobacteria. Nat Rev Microbiol 1:45–54
    [Google Scholar]
  20. Kashefi K., Hartzell P. L. 1995; Genetic suppression and phenotypic masking of a Myxococcus xanthus frzF defect. Mol Microbiol 15:483–494
    [Google Scholar]
  21. Kearns D. B., Shimkets L. J. 2001; Lipid chemotaxis and signal transduction in Myxococcus xanthus . Trends Microbiol 9:126–129
    [Google Scholar]
  22. Kirby J. R., Berleman J. E., Muller S., Li D., Scott J. C., Wilson J. M. 2008; Chemosensory signal transduction systems in Myxococcus xanthus . In Myxobacteria: Multicellularity and Differentiation pp 135–147 Edited by Whitworth D. E. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  23. Lancero H., Brofft J. E., Downard J., Birren B. W., Nusbaum C., Naylor J., Shi W., Shimkets L. J. 2002; Mapping of Myxococcus xanthus social motility dsp mutations to the dif genes. J Bacteriol 184:1462–1465
    [Google Scholar]
  24. Li Y., Sun H., Ma X., Lu A., Lux R., Zusman D., Shi W. 2003; Extracellular polysaccharides mediate pilus retraction during social motility of Myxococcus xanthus . Proc Natl Acad Sci U S A 100:5443–5448
    [Google Scholar]
  25. Lu A., Cho K., Black W. P., Duan X. Y., Lux R., Yang Z., Kaplan H. B., Zusman D. R., Shi W. 2005; Exopolysaccharide biosynthesis genes required for social motility in Myxococcus xanthus . Mol Microbiol 55:206–220
    [Google Scholar]
  26. Magrini V., Creighton C., Youderian P. 1999; Site-specific recombination of temperate Myxococcus xanthus phage Mx8: genetic elements required for integration. J Bacteriol 181:4050–4061
    [Google Scholar]
  27. Merz A. J., So M., Sheetz M. P. 2000; Pilus retraction powers bacterial twitching motility. Nature 407:98–102
    [Google Scholar]
  28. Mignot T. 2007; The elusive engine in Myxococcus xanthus gliding motility. Cell Mol Life Sci 64:2733–2745
    [Google Scholar]
  29. Mignot T., Shaevitz J. W., Hartzell P. L., Zusman D. R. 2007; Evidence that focal adhesion complexes power bacterial gliding motility. Science 315:853–856
    [Google Scholar]
  30. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  31. Palsdottir H., Remis J. P., Schaudinn C., O'Toole E., Lux R., Shi W., McDonald K. L., Costerton J. W., Auer M. 2009; Three-dimensional macromolecular organization of cryofixed Myxococcus xanthus biofilms as revealed by electron microscope tomography. J Bacteriol 191:2077–2082
    [Google Scholar]
  32. Ramaswamy S., Dworkin M., Downard J. 1997; Identification and characterization of Myxococcus xanthus mutants deficient in calcofluor white binding. J Bacteriol 179:2863–2871
    [Google Scholar]
  33. Rubin E. J., Akerley B. J., Novik V. N., Lampe D. J., Husson R. N., Mekalanos J. J. 1999; In vivo transposition of mariner-based elements in enteric bacteria and mycobacteria. Proc Natl Acad Sci U S A 96:1645–1650
    [Google Scholar]
  34. Semmler A. B., Whitchurch C. B., Mattick J. S. 1999; A re-examination of twitching motility in Pseudomonas aeruginosa . Microbiology 145:2863–2873
    [Google Scholar]
  35. Shi W., Zusman D. R. 1993; The two motility systems of Myxococcus xanthus show different selective advantages on various surfaces. Proc Natl Acad Sci U S A 90:3378–3382
    [Google Scholar]
  36. Shimkets L. J. 1986a; Role of cell cohesion in Myxococcus xanthus fruiting body formation. J Bacteriol 166:842–848
    [Google Scholar]
  37. Shimkets L. J. 1986b; Correlation of energy-dependent cell cohesion with social motility in Myxococcus xanthus . J Bacteriol 166:837–841
    [Google Scholar]
  38. Shimkets L. J. 1989; The role of the cell surface in social and adventurous behaviour of myxobacteria. Mol Microbiol 3:1295–1299
    [Google Scholar]
  39. Shimkets L. J. 1999; Intercellular signaling during fruiting-body development of Myxococcus xanthus . Annu Rev Microbiol 53:525–549
    [Google Scholar]
  40. Skerker J. M., Berg H. C. 2001; Direct observation of extension and retraction of type IV pili. Proc Natl Acad Sci U S A 98:6901–6904
    [Google Scholar]
  41. Sun H., Zusman D. R., Shi W. 2000; Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr Biol 10:1143–1146
    [Google Scholar]
  42. Ueki T., Inouye S., Inouye M. 1996; Positive-negative KG cassettes for construction of multi-gene deletions using a single drug marker. Gene 183:153–157
    [Google Scholar]
  43. Vlamakis H. C., Kirby J. R., Zusman D. R. 2004; The Che4 pathway of Myxococcus xanthus regulates type IV pilus-mediated motility. Mol Microbiol 52:1799–1811
    [Google Scholar]
  44. Wall D., Wu S. S., Kaiser D. 1998; Contact stimulation of Tgl and type IV pili in Myxococcus xanthus . J Bacteriol 180:759–761
    [Google Scholar]
  45. Wall D., Kolenbrander P. E., Kaiser D. 1999; The Myxococcus xanthus pilQ ( sglA) gene encodes a secretin homolog required for type IV pilus biogenesis, social motility, and development. J Bacteriol 181:24–33
    [Google Scholar]
  46. Ward M. J., Zusman D. R. 1999; Motility in Myxococcus xanthus and its role in developmental aggregation. Curr Opin Microbiol 2:624–629
    [Google Scholar]
  47. Whitworth D. E. 2008 Myxobacteria: Multicellularity and Differentiation Washington, DC: American Society for Microbiology;
    [Google Scholar]
  48. Wolgemuth C., Hoiczyk E., Kaiser D., Oster G. 2002; How myxobacteria glide. Curr Biol 12:369–377
    [Google Scholar]
  49. Wu S. S., Kaiser D. 1995; Genetic and functional evidence that Type IV pili are required for social gliding motility in Myxococcus xanthus . Mol Microbiol 18:547–558
    [Google Scholar]
  50. Wu S. S., Wu J., Kaiser D. 1997; The Myxococcus xanthus pilT locus is required for social gliding motility although pili are still produced. Mol Microbiol 23:109–121
    [Google Scholar]
  51. Wu S. S., Wu J., Cheng Y. L., Kaiser D. 1998; The pilH gene encodes an ABC transporter homologue required for type IV pilus biogenesis and social gliding motility in Myxococcus xanthus . Mol Microbiol 29:1249–1261
    [Google Scholar]
  52. Xu Q., Black W. P., Ward S. M., Yang Z. 2005; Nitrate-dependent activation of the Dif signaling pathway of Myxococcus xanthus mediated by a NarX–DifA interspecies chimera. J Bacteriol 187:6410–6418
    [Google Scholar]
  53. Xu Q., Black W. P., Cadieux C. L., Yang Z. 2008; Independence and interdependence of Dif and Frz chemosensory pathways in Myxococcus xanthus chemotaxis. Mol Microbiol 69:714–723
    [Google Scholar]
  54. Yang Z., Li Z. 2005; Demonstration of interactions among Myxococcus xanthus Dif chemotaxis-like proteins by the yeast two-hybrid system. Arch Microbiol 183:243–252
    [Google Scholar]
  55. Yang Z., Geng Y., Xu D., Kaplan H. B., Shi W. 1998; A new set of chemotaxis homologues is essential for Myxococcus xanthus social motility. Mol Microbiol 30:1123–1130
    [Google Scholar]
  56. Yang Z., Ma X., Tong L., Kaplan H. B., Shimkets L. J., Shi W. 2000; Myxococcus xanthus dif genes are required for biogenesis of cell surface fibrils essential for social gliding motility. J Bacteriol 182:5793–5798
    [Google Scholar]
  57. Youderian P., Hartzell P. L. 2006; Transposon insertions of magellan-4 that impair social gliding motility in Myxococcus xanthus . Genetics 172:1397–1410
    [Google Scholar]
  58. Youderian P., Burke N., White D. J., Hartzell P. L. 2003; Identification of genes required for adventurous gliding motility in Myxococcus xanthus with the transposable element mariner . Mol Microbiol 49:555–570
    [Google Scholar]
  59. Yu R., Kaiser D. 2007; Gliding motility and polarized slime secretion. Mol Microbiol 63:454–467
    [Google Scholar]
  60. Zusman D. R., Scott A. E., Yang Z., Kirby J. R. 2007; Chemosensory pathways, motility and development in Myxococcus xanthus . Nat Rev Microbiol 5:862–872
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.031070-0
Loading
/content/journal/micro/10.1099/mic.0.031070-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF
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