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Chemosensory pathways, motility and development in Myxococcus xanthus

Key Points

  • Myxococcus xanthus is a Gram-negative bacterium that grows by microbial predation or by degradation of complex macromolecules. When starved, M. xanthus cells aggregate and form spore-filled fruiting bodies.

  • M. xanthus cells have two very different gliding motility systems. Social (S-) motility, powered by type IV pili, moves cells in groups, whereas adventurous (A-) motility, powered by uncharacterized motors that use adhesion complexes, moves isolated cells.

  • M. xanthus contains an extremely large genome that encodes eight clusters of chemotaxis-like genes that define eight two-component chemosensory pathways, most of which have dedicated functions.

  • The Frz (Che1) chemosensory pathway was the first to be characterized. It controls the reversal frequency of cells, which is important for cellular reorientation, and is required for directed movements during colony swarming and fruiting-body formation. During fruiting-body formation, FrzCD, a cytoplasmic receptor, becomes highly methylated, which might indicate that it responds to a developmental signal.

  • Extracellular polysaccharide serves as a receptor for pilus adhesion and stimulates pilus retraction. The Dif (Che2) chemosensory pathway controls the production of extracellular polysaccharide and also functions in cellular recognition and chemotaxis towards lipids.

  • The Che3 chemosensory system does not control motility, but instead controls gene expression during development. Mutants in the che3 system express developmental genes inappropriately and form fruiting bodies on rich media.

  • The Che4–8 chemosensory systems control varied and complex functions, many of which remain uncharacterized.

  • Multiple chemosensory systems are found in many other bacterial species and are not unique to the myxobacteria. The key advantage that is provided by chemosensory systems is temporal regulation of a given output in response to a persistent stimulus, as these systems show adaptation. One interesting question is: how do these multiple chemosensory systems remain insulated from each other so that crosstalk is controlled?

Abstract

The complex life cycle of Myxococcus xanthus includes predation, swarming, fruiting-body formation and sporulation. The genome of M. xanthus is large and comprises an estimated 7,400 open reading frames, of which approximately 605 code for regulatory genes. These include eight clusters of chemotaxis-like genes that define eight chemosensory pathways, most of which have dedicated functions. Although many of these chemosensory pathways have a role in controlling motility, at least two of these pathways control gene expression during development.

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Figure 1: Life cycle of Myxococcus xanthus.
Figure 2: Myxococcus cells: movement and developmental stages.
Figure 3: Myxococcus xanthus motility systems.
Figure 4: Multiple chemosensory gene clusters in Myxococcus xanthus.
Figure 5: Model for the regulation of directional control in Myxococcus xanthus.

References

  1. Kaiser, D. Signaling in myxobacteria. Annu. Rev. Microbiol. 58, 75–98 (2004).

    Article  CAS  PubMed  Google Scholar 

  2. Kaiser, D. A microbial genetic journey. Annu. Rev. Microbiol. 60, 1–25 (2006).

    Article  CAS  PubMed  Google Scholar 

  3. Kaiser, D. Coupling cell movement to multicellular development in myxobacteria. Nature Rev. Microbiol. 1, 45–54 (2003).

    Article  CAS  Google Scholar 

  4. Shimkets, L. J. Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu. Rev. Microbiol. 53, 525–549 (1999).

    Article  CAS  PubMed  Google Scholar 

  5. Reichenbach, H. The ecology of the myxobacteria. Environmen. Microbiol. 1, 15–21 (1999).

    Article  CAS  Google Scholar 

  6. Baker, M. D., Wolanin, P. M. & Stock, J. B. Signal transduction in bacterial chemotaxis. Bioessays 28, 9–22 (2006).

    Article  CAS  PubMed  Google Scholar 

  7. McBride, M. J. Bacterial gliding motility: multiple mechanisms for cell movement over surfaces. Annu. Rev. Microbiol. 55, 49–75 (2001).

    Article  CAS  PubMed  Google Scholar 

  8. Rosenberg, E., Keller, K. H. & Dworkin, M. Cell density-dependent growth of Myxococcus xanthus on casein. J. Bacteriol. 129, 770–777 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Goldman, B. S. et al. Evolution of sensory complexity recorded in a myxobacterial genome. Proc. Natl Acad. Sci. USA 103, 15200–15205 (2006).

    Article  CAS  PubMed  Google Scholar 

  10. McBride, M. J. & Zusman, D. R. Behavioral analysis of single cells of Myxococcus xanthus in response to prey cells of Escherichia coli. FEMS Microbiol. Lett. 137, 227–231 (1996).

    Article  CAS  PubMed  Google Scholar 

  11. Berleman, J. E., Chumley, T., Cheung, P. & Kirby, J. R. Rippling is a predatory behavior in Myxococcus xanthus. J. Bacteriol. 188, 5888–5895 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Igoshin, O. A., Mogilner, A., Welch, R. D., Kaiser, D. & Oster, G. Pattern formation and traveling waves in myxobacteria: theory and modeling. Proc. Natl Acad. Sci. USA 98, 14913–14918 (2001).

    Article  CAS  PubMed  Google Scholar 

  13. Sager, B. & Kaiser, D. Intercellular C-signaling and the traveling waves of Myxococcus. Genes Dev. 8, 2793–2804 (1994).

    Article  CAS  PubMed  Google Scholar 

  14. Sliusarenko, O., Neu, J., Zusman, D. R. & Oster, G. Accordion waves in Myxococcus xanthus. Proc. Natl Acad. Sci. USA 103, 1534–1539 (2006).

    Article  CAS  PubMed  Google Scholar 

  15. O'Connor, K. A. & Zusman, D. R. Behavior of peripheral rods and their role in the life cycle of Myxococcus xanthus. J. Bacteriol. 173, 3342–3355 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wireman, J. W. & Dworkin, M. Developmentally induced autolysis during fruiting body formation by Myxococcus xanthus. J. Bacteriol. 129, 798–802 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Berleman, J. E. & Kirby, J. R. multicellular development in Myxococcus xanthus is stimulated by predator–prey interactions. J. Bacteriol. 189, 5675–5682 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hodgkin, J. & Kaiser, D. Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc. Natl Acad. Sci. USA 74, 2938–2942 (1977).

    Article  CAS  PubMed  Google Scholar 

  19. Hodgkin, J. & Kaiser, D. Genetics of gliding motility in Myxococcus xanthus (myxobacteriales) — two gene systems control movement. Mol. Gen. Genet. 171, 177–191 (1979). This is a seminal paper that showed that there are two motility systems in M. xanthus.

    Article  Google Scholar 

  20. Stephens, K., Hartzell, P. & Kaiser, D. Gliding motility in Myxococcus xanthus: mgl locus, RNA, and predicted protein products. J. Bacteriol. 171, 819–830 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hartzell, P. L. Complementation of sporulation and motility defects in a prokaryote by a eukaryotic GTPase. Proc. Natl Acad. Sci. USA 94, 9881–9886 (1997).

    Article  CAS  PubMed  Google Scholar 

  22. Barnes, G., Louie, K. A. & Botstein, D. Yeast proteins associated with microtubules in vitro and in vivo. Mol. Biol. Cell 3, 29–47 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Yang, R. et al. AglZ is a filament-forming coiled-coil protein required for adventurous gliding motility of Myxococcus xanthus. J. Bacteriol. 186, 6168–6178 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ward, M. J., Lew, H. & Zusman, D. R. Social motility in Myxococcus xanthus requires FrzS, a protein with an extensive coiled-coil domain. Mol. Microbiol. 37, 1357–1371 (2000).

    Article  CAS  PubMed  Google Scholar 

  25. Lancero, H. et al. Characterization of a Myxococcus xanthus mutant that is defective for adventurous motility and social motility. Microbiology 150, 4085–4093 (2004).

    Article  CAS  PubMed  Google Scholar 

  26. Zusman, D. R. “Frizzy” mutants: a new class of aggregation-defective developmental mutants of Myxococcus xanthus. J. Bacteriol. 150, 1430–1437 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 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. USA 82, 8767–8770 (1985). This paper showed that the Frz system controls the frequency of cell reversals.

    Article  CAS  PubMed  Google Scholar 

  28. 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. USA 86, 424–428 (1989). This paper showed that the frz genes encode chemosensory homologues.

    Article  CAS  PubMed  Google Scholar 

  29. Ward, M. J. & Zusman, D. R. Motility in Myxococcus xanthus and its role in developmental aggregation. Curr. Opin. Microbiol. 2, 624–629 (1999).

    Article  CAS  PubMed  Google Scholar 

  30. Inclan, Y. F., Vlamakis, H. C. & Zusman, D. R. FrzZ, a dual CheY-like response regulator, functions as an output for the Frz chemosensory pathway of Myxococcus xanthus. Mol. Microbiol. 65, 90–102 (2007).

    Article  CAS  PubMed  Google Scholar 

  31. Fraser, J. S. et al. An atypical receiver domain controls the dynamic polar localization of the Myxococcus xanthus social motility protein FrzS. Mol. Microbiol. 65, 319–332 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Mignot, T., Merlie, J. P. Jr & Zusman, D. R. Two localization motifs mediate polar residence of FrzS during cell movement and reversals of Myxococcus xanthus. Mol. Microbiol. 65, 363–372 (2007).

    Article  CAS  PubMed  Google Scholar 

  33. Dworkin, M. & Eide, D. Myxococcus xanthus does not respond chemotactically to moderate concentration gradients. J. Bacteriol. 154, 437–442 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Shi, W., Kohler, T. & Zusman, D. R. Chemotaxis plays a role in the social behaviour of Myxococcus xanthus. Mol. Microbiol. 9, 601–611 (1993).

    Article  CAS  PubMed  Google Scholar 

  35. Kearns, D. B. & Shimkets, L. J. Lipid chemotaxis and signal transduction in Myxococcus xanthus. Trends Microbiol. 9, 126–129 (2001). This paper describes lipid chemotaxis in M. xanthus.

    Article  CAS  PubMed  Google Scholar 

  36. McBride, M. J. & Zusman, D. R. FrzCD, a methyl-accepting taxis protein from Myxococcus xanthus, shows modulated methylation during fruiting body formation. J. Bacteriol. 175, 4936–4940 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Geng, Y., Yang, Z., Downard, J., Zusman, D. & Shi, W. Methylation of FrzCD defines a discrete step in the developmental program of Myxococcus xanthus. J. Bacteriol. 180, 5765–5768 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Gorski, L., Gronewold, T. & Kaiser, D. A σ54 activator protein necessary for spore differentiation within the fruiting body of Myxococcus xanthus. J. Bacteriol. 182, 2438–2444 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Sun, H. & Shi, W. Genetic studies of mrp, a locus essential for cellular aggregation and sporulation of Myxococcus xanthus. J. Bacteriol. 183, 4786–4795 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Sun, H. & Shi, W. Analyses of mrp genes during Myxococcus xanthus development. J. Bacteriol. 183, 6733–6739 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Boysen, A., Ellehauge, E., Julien, B. & Sogaard-Andersen, L. The DevT protein stimulates synthesis of FruA, a signal transduction protein required for fruiting body morphogenesis in Myxococcus xanthus. J. Bacteriol. 184, 1540–1546 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Ellehauge, E., Norregaard-Madsen, M. & Sogaard-Andersen, L. The FruA signal transduction protein provides a checkpoint for the temporal co-ordination of intercellular signals in Myxococcus xanthus development. Mol. Microbiol. 30, 807–817 (1998).

    Article  CAS  PubMed  Google Scholar 

  43. Sogaard-Andersen, L. et al. Coupling gene expression and multicellular morphogenesis during fruiting body formation in Myxococcus xanthus. Mol. Microbiol. 48, 1–8 (2003).

    Article  CAS  PubMed  Google Scholar 

  44. Rasmussen, A. A., Porter, S. L., Armitage, J. P. & Sogaard-Andersen, L. Coupling of multicellular morphogenesis and cellular differentiation by an unusual hybrid histidine protein kinase in Myxococcus xanthus. Mol. Microbiol. 56, 1358–1372 (2005).

    Article  CAS  PubMed  Google Scholar 

  45. Yang, Z., Geng, Y., Xu, D., Kaplan, H. B. & Shi, W. A new set of chemotaxis homologues is essential for Myxococcus xanthus social motility. Mol. Microbiol. 30, 1123–1130 (1998). This was the first paper to describe the Dif chemosensory system.

    Article  CAS  PubMed  Google Scholar 

  46. Li, Y. et al. Extracellular polysaccharides mediate pilus retraction during social motility of Myxococcus xanthus. Proc. Natl Acad. Sci. USA 100, 5443–5448 (2003).

    Article  CAS  PubMed  Google Scholar 

  47. Yang, Z. & Li, Z. Demonstration of interactions among Myxococcus xanthus Dif chemotaxis-like proteins by the yeast two-hybrid system. Arch. Microbiol. 183, 243–252 (2005).

    Article  CAS  PubMed  Google Scholar 

  48. Bellenger, K., Ma, X., Shi, W. & Yang, Z. A CheW homologue is required for Myxococcus xanthus fruiting body development, social gliding motility, and fibril biogenesis. J. Bacteriol. 184, 5654–5660 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Yang, Z. et al. Myxococcus xanthus dif genes are required for biogenesis of cell surface fibrils essential for social gliding motility. J Bacteriol. 182, 5793–5798 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Black, W. P. & Yang, Z. Myxococcus xanthus chemotaxis homologs DifD and DifG negatively regulate fibril polysaccharide production. J. Bacteriol. 186, 1001–1008 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Bonner, P. J. et al. The Dif chemosensory pathway is directly involved in phosphatidylethanolamine sensory transduction in Myxococcus xanthus. Mol. Microbiol. 57, 1499–1508 (2005).

    Article  CAS  PubMed  Google Scholar 

  52. Black, W. P., Xu, Q. & Yang, Z. Type IV pili function upstream of the Dif chemotaxis pathway in Myxococcus xanthus EPS regulation. Mol. Microbiol. 61, 447–456 (2006).

    Article  CAS  PubMed  Google Scholar 

  53. Xu, Q., Black, W. P., Ward, S. M. & Yang, Z. Nitrate-dependent activation of the Dif signaling pathway of Myxococcus xanthus mediated by a NarX–DifA interspecies chimera. J. Bacteriol. 187, 6410–6418 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Bonner, P. J. & Shimkets, L. J. Phospholipid directed motility of surface-motile bacteria. Mol. Microbiol. 61, 1101–1109 (2006).

    Article  CAS  PubMed  Google Scholar 

  55. Kearns, D. B., Bonner, P. J., Smith, D. R. & Shimkets, L. J. An extracellular matrix-associated zinc metalloprotease is required for dilauroyl phosphatidylethanolamine chemotactic excitation in Myxococcus xanthus. J. Bacteriol. 184, 1678–1684 (2002). This paper showed that the Che3 system controls gene expression during development.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Kearns, D. B., Campbell, B. D. & Shimkets, L. J. Myxococcus xanthus fibril appendages are essential for excitation by a phospholipid attractant. Proc. Natl Acad. Sci. USA 97, 11505–11510 (2000).

    Article  CAS  PubMed  Google Scholar 

  57. Kirby, J. R. & Zusman, D. R. Chemosensory regulation of developmental gene expression in Myxococcus xanthus. Proc. Natl Acad. Sci. USA 100, 2008–2013 (2003).

    Article  CAS  PubMed  Google Scholar 

  58. Vlamakis, H. C., Kirby, J. R. & Zusman, D. R. The Che4 pathway of Myxococcus xanthus regulates type IV pilus-mediated motility. Mol. Microbiol. 52, 1799–1811 (2004).

    Article  CAS  PubMed  Google Scholar 

  59. Lee, K. & Shimkets, L. J. Suppression of a signaling defect during Myxococcus xanthus development. J. Bacteriol. 178, 977–984 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Berleman, J. E. & Bauer, C. E. A Che-like signal transduction cascade involved in controlling flagella biosynthesis in Rhodospirillum centenum. Mol. Microbiol. 55, 1390–1402 (2005).

    Article  CAS  PubMed  Google Scholar 

  61. Hickman, J. W., Tifrea, D. F. & Harwood, C. S. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl Acad. Sci. USA 102, 14422–14427 (2005).

    Article  CAS  PubMed  Google Scholar 

  62. Whitchurch, C. B. et al. Characterization of a complex chemosensory signal transduction system which controls twitching motility in Pseudomonas aeruginosa. Mol. Microbiol. 52, 873–893 (2004).

    Article  CAS  PubMed  Google Scholar 

  63. D'Argenio, D. A., Gallagher, L. A., Berg, C. A. & Manoil, C. Drosophila as a model host for Pseudomonas aeruginosa infection. J. Bacteriol. 183, 1466–1471 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Guo D, W. Y., Kaplan HB. Identification and characterization of genes required for early Myxococcus xanthus developmental gene expression. J. Bacteriol. 182, 4564–4571 (2000).

    Article  PubMed  PubMed Central  Google Scholar 

  65. Alley, M. R., Gomes, S. L., Alexander, W. & Shapiro, L. Genetic analysis of a temporally transcribed chemotaxis gene cluster in Caulobacter crescentus. Genetics 129, 333–341 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Maddock, J. R. & Shapiro, L. Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259, 1717–1723 (1993).

    Article  CAS  PubMed  Google Scholar 

  67. Bray, D., Levin, M. D. & Morton-Firth, C. J. Receptor clustering as a cellular mechanism to control sensitivity. Nature 393, 85–88 (1998).

    Article  CAS  PubMed  Google Scholar 

  68. Parkinson, J. S., Ames, P. & Studdert, C. A. Collaborative signaling by bacterial chemoreceptors. Curr. Opin. Microbiol. 8, 116–121 (2005).

    Article  CAS  PubMed  Google Scholar 

  69. Segall, J. E., Block, S. M. & Berg, H. C. Temporal comparisons in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 83, 8987–8991 (1986).

    Article  CAS  PubMed  Google Scholar 

  70. Wadhams, G. H. et al. TlpC, a novel chemotaxis protein in Rhodobacter sphaeroides, localizes to a discrete region in the cytoplasm. Mol. Microbiol. 46, 1211–1221 (2002).

    Article  CAS  PubMed  Google Scholar 

  71. Weinberg, R. A. & Zusman, D. R. Evidence that the Myxococcus xanthus frz genes are developmentally regulated. J. Bacteriol. 171, 6174–6186 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Jakobsen, J. S. et al. σ54 enhancer binding proteins and Myxococcus xanthus fruiting body development. J. Bacteriol. 186, 4361–4368 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Sun, H., Zusman, D. R. & Shi, W. Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr. Biol. 10, 1143–1146 (2000).

    Article  CAS  PubMed  Google Scholar 

  74. Wall, D. & Kaiser, D. Type IV pili and cell motility. Mol. Microbiol. 32, 1–10 (1999).

    Article  CAS  PubMed  Google Scholar 

  75. Arnold, J. W. & Shimkets, L. J. Inhibition of cell–cell interactions in Myxococcus xanthus by congo red. J. Bacteriol. 170, 5765–5770 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Bowden, M. G. & Kaplan, H. B. The Myxococcus xanthus lipopolysaccharide O-antigen is required for social motility and multicellular development. Mol. Microbiol. 30, 275–284 (1998).

    Article  CAS  PubMed  Google Scholar 

  77. Jahn, E. Beitrage zur Botanischen Protistologie (Gebruder Borntraeger, Leipzig, 1924).

    Google Scholar 

  78. Wolgemuth, C., Hoiczyk, E., Kaiser, D. & Oster, G. How myxobacteria glide. Curr. Biol. 12, 369–377 (2002).

    Article  CAS  PubMed  Google Scholar 

  79. Sliusarenko, O., Zusman, D. R. & Oster, G. The motors powering A-motility in Myxococcus xanthus are distributed along the cell body. J. Bacteriol. 17 Aug 2007 (doi: 10.1128/JB.00923-07).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Sun, H., Yang, Z. & Shi, W. Effect of cellular filamentation on adventurous and social gliding motility of Myxococcus xanthus. Proc. Natl Acad. Sci. USA 96, 15178–15183 (1999).

    Article  CAS  PubMed  Google Scholar 

  81. Mignot, T. The elusive engine in Myxococcus xanthus gliding motility. Cell. Mol. Life Sci. 25 July 2007 (doi: 10.1007/s00018-007-7176-x).

    Article  CAS  PubMed  Google Scholar 

  82. Mignot, T., Shaevitz, J. W., Hartzell, P. L. & Zusman, D. R. Evidence that focal adhesion complexes power bacterial gliding motility. Science 315, 853–856 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Graumann, P. Cytoskeletal elements in bacteria. Annu. Rev. Microbiol. (in the press).

  84. Shi, W. & Zusman, D. R. The two motility systems of Myxococcus xanthus show different selective advantages on various surfaces. Proc. Natl Acad. Sci. USA 90, 3378–3382 (1993).

    Article  CAS  PubMed  Google Scholar 

  85. Wozniak, M. A., Modzelewska, K., Kwong, L. & Keely, P. J. Focal adhesion regulation of cell behavior. Biochim. Biophys. Acta 1692, 103–119 (2004).

    Article  CAS  PubMed  Google Scholar 

  86. Baum, J., Papenfuss, A. T., Baum, B., Speed, T. P. & Cowman, A. F. Regulation of apicomplexan actin-based motility. Nature Rev. Microbiol. 4, 621–628 (2006).

    Article  CAS  Google Scholar 

  87. Wadhams, G. H. & Armitage, J. P. Making sense of it all: bacterial chemotaxis. Nature Rev. Mol. Cell Biol. 5, 1024–1037 (2004).

    Article  CAS  Google Scholar 

  88. Wolanin, P. M. et al. Self-assembly of receptor/signaling complexes in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 103, 14313–14318 (2006).

    Article  CAS  PubMed  Google Scholar 

  89. Welch, M., Oosawa, K., Aizawa, S. & Eisenbach, M. Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. Proc. Natl Acad. Sci. USA 90, 8787–8791 (1993).

    Article  CAS  PubMed  Google Scholar 

  90. Okumura, H., Nishiyama, S., Sasaki, A., Homma, M. & Kawagishi, I. Chemotactic adaptation is altered by changes in the carboxy-terminal sequence conserved among the major methyl-accepting chemoreceptors. J. Bacteriol. 180, 1862–1868 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Ninfa, E. G., Stock, A., Mowbray, S. & Stock, J. Reconstitution of the bacterial chemotaxis signal transduction system from purified components. J. Biol. Chem. 266, 9764–9770 (1991).

    CAS  PubMed  Google Scholar 

  92. Levit, M. N. & Stock, J. B. Receptor methylation controls the magnitude of stimulus-response coupling in bacterial chemotaxis. J. Biol. Chem. 277, 36760–36765 (2002).

    Article  CAS  PubMed  Google Scholar 

  93. Armitage, J. P. & Schmitt, R. Bacterial chemotaxis: Rhodobacter sphaeroides and Sinorhizobium meliloti — variations on a theme? Microbiology 143, 3671–3682 (1997).

    Article  CAS  PubMed  Google Scholar 

  94. Mignot, T., Merlie, J. P. Jr & Zusman, D. R. Two localization motifs mediate polar residence of FrzS during cell movement and reversals of Myxococcus xanthus. Mol. Microbiol. 65, 363–372 (2007).

    Article  CAS  PubMed  Google Scholar 

  95. Gross, L. Antisocial behavior in cooperative bacteria. PLoS Biol. 3, 1847–1848 (2005).

    CAS  Google Scholar 

  96. Foster, K. R. Sociobiology: the Phoenix effect. Nature 441, 291–292 (2006).

    Article  CAS  PubMed  Google Scholar 

  97. Zusman, D. R. & O'Connor, K. A. Development in Myxococcus xanthus involves aggregation and sporulation as well as non-aggregation and non-sporulation. Sem. Dev. Biol. 2, 37–45 (1991).

    Google Scholar 

  98. Zhulin, I. B. The superfamily of chemotaxis transducers: from physiology to genomics and back. Adv. Microb. Physiol. 45, 157–198 (2001).

    Article  CAS  PubMed  Google Scholar 

  99. Alam, M. & Oesterhelt, D. Morphology, function and isolation of halobacterial flagella. J. Mol. Biol. 176, 459–475 (1984).

    Article  CAS  PubMed  Google Scholar 

  100. Meier, V. M., Muschler, P. & Scharf, B. E. Functional analysis of nine putative chemoreceptor proteins in Sinorhizobium meliloti. J. Bacteriol. 189, 1816–1826 (2007).

    Article  CAS  PubMed  Google Scholar 

  101. Ng, W. V. et al. Genome sequence of Halobacterium species NRC-1. Proc. Natl Acad. Sci. USA 97, 12176–12181 (2000).

    Article  CAS  PubMed  Google Scholar 

  102. Pittman, M. S., Goodwin, M. & Kelly, D. J. Chemotaxis in the human gastric pathogen Helicobacter pylori: different roles for CheW and the three CheV paralogues, and evidence for CheV2 phosphorylation. Microbiology 147, 2493–2504 (2001).

    Article  CAS  PubMed  Google Scholar 

  103. Croxen, M. A., Sisson, G., Melano, R. & Hoffman, P. S. The Helicobacter pylori chemotaxis receptor TlpB (HP0103) is required for pH taxis and for colonization of the gastric mucosa. J. Bacteriol. 188, 2656–2665 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Foynes, S. et al. Helicobacter pylori possesses two CheY response regulators and a histidine kinase sensor, CheA, which are essential for chemotaxis and colonization of the gastric mucosa. Infect. Immun. 68, 2016–2023 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Kato, J., Nakamura, T., Kuroda, A. & Ohtake, H. Cloning and characterization of chemotaxis genes in Pseudomonas aeruginosa. Biosci. Biotechnol. Biochem. 63, 155–161 (1999).

    Article  CAS  PubMed  Google Scholar 

  106. Jiang, Z. Y. & Bauer, C. E. Analysis of a chemotaxis operon from Rhodospirillum centenum. J. Bacteriol. 179, 5712–5719 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Jiang, Z. Y., Gest, H. & Bauer, C. E. Chemosensory and photosensory perception in purple photosynthetic bacteria utilize common signal transduction components. J. Bacteriol. 179, 5720–5727 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Attmannspacher, U., Scharf, B. & Schmitt, R. Control of speed modulation (chemokinesis) in the unidirectional rotary motor of Sinorhizobium meliloti. Mol. Microbiol. 56, 708–718 (2005).

    Article  CAS  PubMed  Google Scholar 

  109. Bhaya, D. Light matters: phototaxis and signal transduction in unicellular cyanobacteria. Mol. Microbiol. 53, 745–754 (2004).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We are grateful to members of the Zusman laboratory, past and present, for many helpful discussions. Our research is supported by grants from the National Institutes of Health GM20509 and GM64463 to D.R.Z., GM071601 to Z.Y. and AI59682 to J.R.K. A.E.S was supported by a predoctoral fellowship from the National Science Foundation.

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Correspondence to David R. Zusman or John R. Kirby.

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DATABASES

Genome Project

Myxococcus xanthus

Rhodobacter sphaeroides

Salmonella typhimurium

Streptomyces coelicolor

FURTHER INFORMATION

David R. Zusman's homepage

John R. Kirby's homepage

Myxopedia

Glossary

Development

A programmed change in gene expression and morphology. In Myxococcus xanthus, this process is triggered by starvation and results in cellular aggregation, fruiting-body formation and sporulation.

Rippling

Coordinated rhythmic movement of cells.

Cell reversal

When a cell changes its direction along its long axis so that the leading cell pole becomes the lagging cell pole.

Mound

An early stage of development during which cells aggregate before sporulation.

Fruiting body

The final stage of Myxococcus xanthus development during which cells form a large aggregate and develop into environmentally resistant spores.

Peripheral rod

A cell that maintains its rod shape and does not form a spore during development.

DZ2

A wild-type laboratory strain of Myxococcus xanthus. It was obtained from the Berkeley microbiology laboratory culture collection in 1973. It is thought to be the parent strain of FB, DK101, DZF1 and DK1622.

FB

A strain of Myxococcus xanthus that has been selected for its ability to form single colonies.

DK1622

A 'wild-type' laboratory strain of Myxococcus xanthus. It was derived by restoring full social motility to strain FB, which is thought to have originated by mutagenesis from strain DZ2. Strain DK1622 contains a 250-kb deletion of unknown function.

S-motility

Movement of cells in groups that involves extension and retraction of the type IV pili.

CheW

An adaptor protein that links CheA to methyl-accepting chemotaxis protein receptors in bacterial chemotaxis.

CheA

A histidine kinase that is involved in bacterial chemotaxis and that phosphorylates a cognate response regulator such as CheY. Chemosensory pathways can usually be identified by a specific CheA.

Frz pathway

A Myxococcus xanthus chemotaxis pathway that controls cellular reversal frequency.

Chemotaxis

Directed movement towards attractants or away from repellents.

Adaptation

A process whereby cells can adjust to the levels of an attractant or repellent. In bacteria this involves the methylation and/or demethylation of receptors or the dephosphorylation of response regulators. Adaptation allows bacteria to sense small changes in stimuli.

Methyl-accepting chemotaxis protein

A protein that is involved in bacterial chemotaxis and that senses attractants and repellents.

Slime

Polysaccharide that contains material secreted by Myxococcus xanthus.

Extracellular polysaccharides

Extracellular polysaccharides that stimulate the retraction of the type IV pili of Myxococcus xanthus.

Dif pathway

A Myxococcus xanthus chemosensory pathway that controls the production of extracellular polysaccharide and lipid chemotaxis. This pathway is essential for social motility.

CheY

A receiver-domain protein that is phosphorylated by CheA on an Asp residue. Phosphorylated CheY interacts with the output functions of the chemosensory system, which signals stimulation. In Escherichia coli, this results in reversal of the flagellar motor rotation.

CheR

A methyltransferase that methylates methyl-accepting chemotaxis protein receptors in response to stimuli. It is involved in adaptation in bacterial chemotaxis.

CheB

A methylesterase that removes methyl groups from receptors and is involved in adaptation. In Escherichia coli, CheB is phosphorylated, and thereby activated, by phosphorylated CheA.

Che3 pathway

A Myxococcus xanthus chemosensory pathway that controls the expression of many developmental genes.

Che4 pathway

A Myxococcus xanthus chemosensory pathway that regulates social motility.

Type IV pili

Long flexible appendages that are found at the poles of cells and can power motility.

Myxospore

A spherical, environmentally resistant and metabolically inactive Myxococcus xanthus cell.

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Zusman, D., Scott, A., Yang, Z. et al. Chemosensory pathways, motility and development in Myxococcus xanthus. Nat Rev Microbiol 5, 862–872 (2007). https://doi.org/10.1038/nrmicro1770

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