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. 1991 Apr;173(7):2206–2211. doi: 10.1128/jb.173.7.2206-2211.1991

Low-temperature induction of Myxococcus xanthus developmental gene expression in wild-type and csgA suppressor cells.

H G Rhie 1, L J Shimkets 1
PMCID: PMC207768  PMID: 1901052

Abstract

The csgA gene encodes an extracellular protein that plays an essential role in the regulation of fruiting-body formation and sporulation of Myxococcus xanthus. The csgA suppressor allele soc-500 (formerly referred to as csp-500) was selected based on its ability to restore sporulation to csgA cells under developmental conditions at 32 degrees C. The soc-500 allele was subsequently found to induce sporulation of csgA+ or csgA cells simply by shifting the temperature of vegetatively growing cells to 15 degrees C. Low-temperature-induced sporulation of soc-500 strains occurred in the absence of two requirements for fruiting-body sporulation: low nutrient levels and a high temperature. Low temperature alone caused the expression of many developmentally regulated genes but did not support the development of wild-type cells. The soc-500 allele appears to activate genes involved with sensing nutritional stress. At low temperature on a nutritionally rich medium, soc-500 induced expression of the tps gene which is normally expressed following nutritional shiftdown. The soc-500 allele was cloned and integrated into the wild-type chromosome by site-specific recombination. It was dominant over the wild-type allele in merodiploids and is contained on a 3-kbp DraI-ClaI restriction fragment. The soc-500 transcriptional unit spans a 300-bp PstI-PstI restriction fragment, since deletion of the PstI restriction fragment inhibits both csgA suppression and low-temperature induction. These results suggest that the soc-500 mutation lies in a gene that is involved in nutrient sensing.

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Selected References

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  1. Avery L., Kaiser D. In situ transposon replacement and isolation of a spontaneous tandem genetic duplication. Mol Gen Genet. 1983;191(1):99–109. doi: 10.1007/BF00330896. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Downard J. S. Identification of the RNA products of the ops gene of Myxococcus xanthus and mapping of ops and tps RNAs. J Bacteriol. 1987 Apr;169(4):1522–1528. doi: 10.1128/jb.169.4.1522-1528.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Downard J. S., Kim S. H., Kil K. S. Localization of the cis-acting regulatory DNA sequences of the Myxococcus xanthus tps and ops genes. J Bacteriol. 1988 Oct;170(10):4931–4938. doi: 10.1128/jb.170.10.4931-4938.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Downard J. S., Kupfer D., Zusman D. R. Gene expression during development of Myxococcus xanthus. Analysis of the genes for protein S. J Mol Biol. 1984 Jun 5;175(4):469–492. doi: 10.1016/0022-2836(84)90180-3. [DOI] [PubMed] [Google Scholar]
  6. Downard J. S., Zusman D. R. Differential expression of protein S genes during Myxococcus xanthus development. J Bacteriol. 1985 Mar;161(3):1146–1155. doi: 10.1128/jb.161.3.1146-1155.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Geisselsoder J., Campos J. M., Zusman D. R. Physical characterization of bacteriophage MX4, a generalized transducing phage for Myxococcus xanthus. J Mol Biol. 1978 Feb 25;119(2):179–189. doi: 10.1016/0022-2836(78)90432-1. [DOI] [PubMed] [Google Scholar]
  8. Gill R. E., Cull M. G., Fly S. Genetic identification and cloning of a gene required for developmental cell interactions in Myxococcus xanthus. J Bacteriol. 1988 Nov;170(11):5279–5288. doi: 10.1128/jb.170.11.5279-5288.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983 Jun 5;166(4):557–580. doi: 10.1016/s0022-2836(83)80284-8. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Inouye M., Inouye S., Zusman D. R. Biosynthesis and self-assembly of protein S, a development-specific protein of Myxococcus xanthus. Proc Natl Acad Sci U S A. 1979 Jan;76(1):209–213. doi: 10.1073/pnas.76.1.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Inouye S., Franceschini T., Inouye M. Structural similarities between the development-specific protein S from a gram-negative bacterium, Myxococcus xanthus, and calmodulin. Proc Natl Acad Sci U S A. 1983 Nov;80(22):6829–6833. doi: 10.1073/pnas.80.22.6829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Inouye S., Ike Y., Inouye M. Tandem repeat of the genes for protein S, a development-specific protein of Myxococcus xanthus. J Biol Chem. 1983 Jan 10;258(1):38–40. [PubMed] [Google Scholar]
  16. Kil K. S., Brown G. L., Downard J. S. A segment of Myxococcus xanthus ops DNA functions as an upstream activation site for tps gene transcription. J Bacteriol. 1990 Jun;172(6):3081–3088. doi: 10.1128/jb.172.6.3081-3088.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. 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]
  20. 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]
  21. 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]
  22. Kuner J. M., Kaiser D. Introduction of transposon Tn5 into Myxococcus for analysis of developmental and other nonselectable mutants. Proc Natl Acad Sci U S A. 1981 Jan;78(1):425–429. doi: 10.1073/pnas.78.1.425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Rhie H. G., Shimkets L. J. Developmental bypass suppression of Myxococcus xanthus csgA mutations. J Bacteriol. 1989 Jun;171(6):3268–3276. doi: 10.1128/jb.171.6.3268-3276.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sasakawa C., Yoshikawa M. A series of Tn5 variants with various drug-resistance markers and suicide vector for transposon mutagenesis. Gene. 1987;56(2-3):283–288. doi: 10.1016/0378-1119(87)90145-4. [DOI] [PubMed] [Google Scholar]
  26. Shimkets L. J., Asher S. J. Use of recombination techniques to examine the structure of the csg locus of Myxococcus xanthus. Mol Gen Genet. 1988 Jan;211(1):63–71. doi: 10.1007/BF00338394. [DOI] [PubMed] [Google Scholar]
  27. Shimkets L. J. Control of morphogenesis in myxobacteria. Crit Rev Microbiol. 1987;14(3):195–227. doi: 10.3109/10408418709104439. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Shimkets L. J., Rafiee H. CsgA, an extracellular protein essential for Myxococcus xanthus development. J Bacteriol. 1990 Sep;172(9):5299–5306. doi: 10.1128/jb.172.9.5299-5306.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Shimkets L. J. Social and developmental biology of the myxobacteria. Microbiol Rev. 1990 Dec;54(4):473–501. doi: 10.1128/mr.54.4.473-501.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shimkets L. J. The role of the cell surface in social and adventurous behaviour of myxobacteria. Mol Microbiol. 1989 Sep;3(9):1295–1299. doi: 10.1111/j.1365-2958.1989.tb00280.x. [DOI] [PubMed] [Google Scholar]
  33. Sodergren E., Cheng Y., Avery L., Kaiser D. Recombination in the Vicinity of Insertions of Transposon Tn 5 in MYXOCOCCUS XANTHUS. Genetics. 1983 Oct;105(2):281–291. doi: 10.1093/genetics/105.2.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Stellwag E., Fink J. M., Zissler J. Physical characterization of the genome of the Myxococcus xanthus bacteriophage MX-8. Mol Gen Genet. 1985;199(1):123–132. doi: 10.1007/BF00327521. [DOI] [PubMed] [Google Scholar]
  35. Teintze M., Thomas R., Furuichi T., Inouye M., Inouye S. Two homologous genes coding for spore-specific proteins are expressed at different times during development of Myxococcus xanthus. J Bacteriol. 1985 Jul;163(1):121–125. doi: 10.1128/jb.163.1.121-125.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Youngman P., Zuber P., Perkins J. B., Sandman K., Igo M., Losick R. New ways to study developmental genes in spore-forming bacteria. Science. 1985 Apr 19;228(4697):285–291. doi: 10.1126/science.228.4697.285. [DOI] [PubMed] [Google Scholar]

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