Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1986 Dec;168(3):1100–1106. doi: 10.1128/jb.168.3.1100-1106.1986

Heat shock proteins of vegetative and fruiting Myxococcus xanthus cells.

D R Nelson, K P Killeen
PMCID: PMC213608  PMID: 3096968

Abstract

The heat shock response of Myxococcus xanthus was investigated and characterized. When shifted from 28 to 40 degrees C, log-phase cells rapidly ceased growth, exhibited a 50% reduction in CFU, and initiated the synthesis of heat shock proteins (HTPs). Heat-shocked log-phase M. xanthus cells labeled with [35S]methionine were found to produce 18 major HTPs. The HTPs, analyzed by sodium dodecyl sulfate-polyacrylamide gel electrophoresis and fluorography, were characterized with regard to molecular mass, subcellular location (periplasm, membrane, or cytoplasm), and temperature required for expression. Most HTPs were expressed at 36 degrees C, the optimum growth temperature of M. xanthus. Cells preincubated at 36 degrees C for 1 h before being shifted to 40 degrees C demonstrated increased thermotolerance compared with cells shifted directly from 28 to 40 degrees C. The HTPs produced by heat-shocked starvation-induced fruiting cells and glycerol-induced sporulating cells were also analyzed and characterized. Thirteen HTPs were detected in fruiting cells shifted from 28 to 40 degrees C. Six of these HTPs were not seen in vegetative M. xanthus cells. Log-phase cells induced to sporulate by the addition of glycerol produced 17 HTPs after being shifted to 40 degrees C. These HTPs were found to be a mixture of HTPs detected in heat-shocked log-phase cells and heat-shocked fruiting cells.

Full text

PDF
1100

Images in this article

1101Image
on p.1101
1103Image
on p.1103
1104Image
on p.1104
1104Image
on p.1104

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bardwell J. C., Craig E. A. Major heat shock gene of Drosophila and the Escherichia coli heat-inducible dnaK gene are homologous. Proc Natl Acad Sci U S A. 1984 Feb;81(3):848–852. doi: 10.1073/pnas.81.3.848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Borbély G., Surányi G., Korcz A., Pálfi Z. Effect of heat shock on protein synthesis in the cyanobacterium Synechococcus sp. strain PCC 6301. J Bacteriol. 1985 Mar;161(3):1125–1130. doi: 10.1128/jb.161.3.1125-1130.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bretscher A. P., Kaiser D. Nutrition of Myxococcus xanthus, a fruiting myxobacterium. J Bacteriol. 1978 Feb;133(2):763–768. doi: 10.1128/jb.133.2.763-768.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Campos J. M., Geisselsoder J., Zusman D. R. Isolation of bacteriophage MX4, a generalized transducing phage for Myxococcus xanthus. J Mol Biol. 1978 Feb 25;119(2):167–178. doi: 10.1016/0022-2836(78)90431-x. [DOI] [PubMed] [Google Scholar]
  5. Cheng K. J., Ingram J. M., Costerton J. W. Alkaline phosphatase localization and spheroplast formation of Pseudomonas aeruginosa. Can J Microbiol. 1970 Dec;16(12):1319–1324. doi: 10.1139/m70-218. [DOI] [PubMed] [Google Scholar]
  6. DWORKIN M., GIBSON S. M. A SYSTEM FOR STUDYING MICROBIAL MORPHOGENESIS: RAPID FORMATION OF MICROCYSTS IN MYXOCOCCUS XANTHUS. Science. 1964 Oct 9;146(3641):243–244. doi: 10.1126/science.146.3641.243. [DOI] [PubMed] [Google Scholar]
  7. FRIEDEN C. Glutamic dehydrogenase. III. The order of substrate addition in the enzymatic reaction. J Biol Chem. 1959 Nov;234:2891–2896. [PubMed] [Google Scholar]
  8. Gerner E. W., Boone R., Connor W. G., Hicks J. A., Boone M. L. A transient thermotolerant survival response produced by single thermal doses in HeLa cells. Cancer Res. 1976 Mar;36(3):1035–1040. [PubMed] [Google Scholar]
  9. Gerner E. W., Schneider M. J. Induced thermal resistance in HeLa cells. Nature. 1975 Aug 7;256(5517):500–502. doi: 10.1038/256500a0. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Henle K. J., Leeper D. B. Interaction of hyperthermia and radiation in CHO cells: recovery kinetics. Radiat Res. 1976 Jun;66(3):505–518. [PubMed] [Google Scholar]
  12. 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]
  13. Janssen G. R., Wireman J. W., Dworkin M. Effect of temperature on the growth of Myxococcus xanthus. J Bacteriol. 1977 Apr;130(1):561–562. doi: 10.1128/jb.130.1.561-562.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kaiser D., Manoil C., Dworkin M. Myxobacteria: cell interactions, genetics, and development. Annu Rev Microbiol. 1979;33:595–639. doi: 10.1146/annurev.mi.33.100179.003115. [DOI] [PubMed] [Google Scholar]
  15. Kasahara M., Anraku Y. Succinate dehydrogenase of Escherichia coli membrane vesicles. Activation and properties of the enzyme. J Biochem. 1974 Nov;76(5):959–966. [PubMed] [Google Scholar]
  16. Komano T., Inouye S., Inouye M. Patterns of protein production in Myxococcus xanthus during spore formation induced by glycerol, dimethyl sulfoxide, and phenethyl alcohol. J Bacteriol. 1980 Dec;144(3):1076–1082. doi: 10.1128/jb.144.3.1076-1082.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kurtz S., Rossi J., Petko L., Lindquist S. An ancient developmental induction: heat-shock proteins induced in sporulation and oogenesis. Science. 1986 Mar 7;231(4742):1154–1157. doi: 10.1126/science.3511530. [DOI] [PubMed] [Google Scholar]
  18. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  19. MCVITTIE A., MESSIK F., ZAHLER S. A. Developmental biology of Myxococcus. J Bacteriol. 1962 Sep;84:546–551. doi: 10.1128/jb.84.3.546-551.1962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Neidhardt F. C., VanBogelen R. A., Lau E. T. Molecular cloning and expression of a gene that controls the high-temperature regulon of Escherichia coli. J Bacteriol. 1983 Feb;153(2):597–603. doi: 10.1128/jb.153.2.597-603.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Neidhardt F. C., VanBogelen R. A., Vaughn V. The genetics and regulation of heat-shock proteins. Annu Rev Genet. 1984;18:295–329. doi: 10.1146/annurev.ge.18.120184.001455. [DOI] [PubMed] [Google Scholar]
  22. Nelson D. R., Cumsky M. G., Zusman D. R. Localization of myxobacterial hemagglutinin in the periplasmic space and on the cell surface of Myxococcus xanthus during developmental aggregation. J Biol Chem. 1981 Dec 10;256(23):12589–12595. [PubMed] [Google Scholar]
  23. Nelson D. R., Zusman D. R. Evidence for long-lived mRNA during fruiting body formation in myxococcus xanthus. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1467–1471. doi: 10.1073/pnas.80.5.1467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nelson D. R., Zusman D. R. Transport and localization of protein S, a spore coat protein, during fruiting body formation by Myxococcus xanthus. J Bacteriol. 1983 May;154(2):547–553. doi: 10.1128/jb.154.2.547-553.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Plesofsky-Vig N., Brambl R. Heat shock response of Neurospora crassa: protein synthesis and induced thermotolerance. J Bacteriol. 1985 Jun;162(3):1083–1091. doi: 10.1128/jb.162.3.1083-1091.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rosenberg E., Katarski M., Gottlieb P. Deoxyribonucleic acid synthesis during exponential growth and microcyst formation in Myxococcus xanthus. J Bacteriol. 1967 Apr;93(4):1402–1408. doi: 10.1128/jb.93.4.1402-1408.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Widelitz R. B., Magun B. E., Gerner E. W. Effects of cycloheximide on thermotolerance expression, heat shock protein synthesis, and heat shock protein mRNA accumulation in rat fibroblasts. Mol Cell Biol. 1986 Apr;6(4):1088–1094. doi: 10.1128/mcb.6.4.1088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yamamori T., Yura T. Genetic control of heat-shock protein synthesis and its bearing on growth and thermal resistance in Escherichia coli K-12. Proc Natl Acad Sci U S A. 1982 Feb;79(3):860–864. doi: 10.1073/pnas.79.3.860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Zusman D. R., Krotoski D. M., Cumsky M. Chromosome replication in Myxococcus xanthus. J Bacteriol. 1978 Jan;133(1):122–129. doi: 10.1128/jb.133.1.122-129.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Zusman D., Rosenberg E. DNA cycle of Myxococcus xanthus. J Mol Biol. 1970 May 14;49(3):609–619. doi: 10.1016/0022-2836(70)90285-8. [DOI] [PubMed] [Google Scholar]
  31. Zusman D., Rosenberg E. Deoxyribonucleic acid synthesis during microcyst germination in Myxococcus xanthus. J Bacteriol. 1968 Oct;96(4):981–986. doi: 10.1128/jb.96.4.981-986.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Zylicz M., Nieradko J., Taylor K. Escherichia coli dnaJ- and dnaK-gene products: synthesis in minicells and membrane-affinity. Biochem Biophys Res Commun. 1983 Jan 14;110(1):176–180. doi: 10.1016/0006-291x(83)91276-7. [DOI] [PubMed] [Google Scholar]
  33. Zylicz M., Yamamoto T., McKittrick N., Sell S., Georgopoulos C. Purification and properties of the dnaJ replication protein of Escherichia coli. J Biol Chem. 1985 Jun 25;260(12):7591–7598. [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES