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. 1991 Mar;173(5):1722–1728. doi: 10.1128/jb.173.5.1722-1728.1991

C-factor has distinct aggregation and sporulation thresholds during Myxococcus development.

S K Kim 1, D Kaiser 1
PMCID: PMC207323  PMID: 1847908

Abstract

C-factor, the protein product of the csgA gene, acts as a short-range morphogenetic signal. It is required for fruiting body development of the gram-negative bacterium Myxococcus xanthus. Aggregation, sporulation, and expression of a set of genes that are C-factor dependent, all of which fail in csgA mutant cells, are completely restored by addition of purified C-factor. We report here that, depending on its concentration, C-factor can elicit two distinct morphogenetic and transcriptional responses from csgA cells. Low levels of C-factor bring about aggregation and expression of an early C-dependent gene, whereas higher levels lead to the same effects plus expression of a late C-dependent gene and spore formation. C-factor positively regulates its own transcription. An approximately fourfold net increase in csgA transcription and C-factor levels during development was measured. We propose that autoregulation and the two distinct activity thresholds allow C-factor to act as a timer, first triggering aggregation, then sporulation, thereby producing the appropriate developmental order.

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Selected References

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  1. Driever W., Nüsslein-Volhard C. The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell. 1988 Jul 1;54(1):95–104. doi: 10.1016/0092-8674(88)90183-3. [DOI] [PubMed] [Google Scholar]
  2. Hagen D. C., Bretscher A. P., Kaiser D. Synergism between morphogenetic mutants of Myxococcus xanthus. Dev Biol. 1978 Jun;64(2):284–296. doi: 10.1016/0012-1606(78)90079-9. [DOI] [PubMed] [Google Scholar]
  3. Hagen T. J., Shimkets L. J. Nucleotide sequence and transcriptional products of the csg locus of Myxococcus xanthus. J Bacteriol. 1990 Jan;172(1):15–23. doi: 10.1128/jb.172.1.15-23.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Inouye M., Inouye S., Zusman D. R. Gene expression during development of Myxococcus xanthus: pattern of protein synthesis. Dev Biol. 1979 Feb;68(2):579–591. doi: 10.1016/0012-1606(79)90228-8. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Kim S. K., Kaiser D. Cell motility is required for the transmission of C-factor, an intercellular signal that coordinates fruiting body morphogenesis of Myxococcus xanthus. Genes Dev. 1990 Jun;4(6):896–904. doi: 10.1101/gad.4.6.896. [DOI] [PubMed] [Google Scholar]
  7. Kim S. K., Kaiser D. Purification and properties of Myxococcus xanthus C-factor, an intercellular signaling protein. Proc Natl Acad Sci U S A. 1990 May;87(10):3635–3639. doi: 10.1073/pnas.87.10.3635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Kroos L., Kaiser D. Construction of Tn5 lac, a transposon that fuses lacZ expression to exogenous promoters, and its introduction into Myxococcus xanthus. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5816–5820. doi: 10.1073/pnas.81.18.5816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. Kroos L., Kuspa A., Kaiser D. Defects in fruiting body development caused by Tn5 lac insertions in Myxococcus xanthus. J Bacteriol. 1990 Jan;172(1):484–487. doi: 10.1128/jb.172.1.484-487.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Kuspa A., Kroos L., Kaiser D. Intercellular signaling is required for developmental gene expression in Myxococcus xanthus. Dev Biol. 1986 Sep;117(1):267–276. doi: 10.1016/0012-1606(86)90369-6. [DOI] [PubMed] [Google Scholar]
  15. LaRossa R., Kuner J., Hagen D., Manoil C., Kaiser D. Developmental cell interactions of Myxococcus xanthus: analysis of mutants. J Bacteriol. 1983 Mar;153(3):1394–1404. doi: 10.1128/jb.153.3.1394-1404.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Li S. F., Shimkets L. J. Site-specific integration and expression of a developmental promoter in Myxococcus xanthus. J Bacteriol. 1988 Dec;170(12):5552–5556. doi: 10.1128/jb.170.12.5552-5556.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Rosenberg E., Keller K. H., Dworkin M. Cell density-dependent growth of Myxococcus xanthus on casein. J Bacteriol. 1977 Feb;129(2):770–777. doi: 10.1128/jb.129.2.770-777.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Shimkets L. J., Kaiser D. Murein components rescue developmental sporulation of Myxococcus xanthus. J Bacteriol. 1982 Oct;152(1):462–470. doi: 10.1128/jb.152.1.462-470.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Smith J. C., Yaqoob M., Symes K. Purification, partial characterization and biological effects of the XTC mesoderm-inducing factor. Development. 1988 Jul;103(3):591–600. doi: 10.1242/dev.103.3.591. [DOI] [PubMed] [Google Scholar]
  22. Stephens K., Hartzell P., Kaiser D. Gliding motility in Myxococcus xanthus: mgl locus, RNA, and predicted protein products. J Bacteriol. 1989 Feb;171(2):819–830. doi: 10.1128/jb.171.2.819-830.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Thaller C., Eichele G. Identification and spatial distribution of retinoids in the developing chick limb bud. Nature. 1987 Jun 18;327(6123):625–628. doi: 10.1038/327625a0. [DOI] [PubMed] [Google Scholar]
  24. Wireman J. W., Dworkin M. Morphogenesis and developmental interactions in myxobacteria. Science. 1975 Aug 15;189(4202):516–523. doi: 10.1126/science.806967. [DOI] [PubMed] [Google Scholar]

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