Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1996 Dec;178(23):6706–6713. doi: 10.1128/jb.178.23.6706-6713.1996

Stigmatella aurantiaca fruiting body formation is dependent on the fbfA gene encoding a polypeptide homologous to chitin synthases.

B Silakowski 1, A Pospiech 1, B Neumann 1, H U Schairer 1
PMCID: PMC178565  PMID: 8955286

Abstract

Stigmatella aurantiaca is a prokaryotic organism that undergoes a multicellular cycle of development resulting in the formation of a fruiting body. For analyzing this process, mutants defective in fruiting body formation have been induced by transposon mutagenesis using a Tn5-derived transposon. About 800 bp upstream of the transposon insertion of mutant AP182 which inactivates a gene (fbfB) involved in fruiting, a further gene (fbfA) needed for fruiting body formation was detected. Inactivation of fbfA leads to mutants which form only non-structured clumps instead of the wild-type fruiting body. The mutant phenotype of fbfA mutants can be partially suppressed by mixing the mutant cells with cells of some independent mutants defective in fruiting body formation. The fbfA gene is transcribed after 8 h of development as determined by measuring the induction of beta-galactosidase activity of a fbfA-delta(trp)-lacZ fusion gene and by Northern (RNA) analysis using an insertion encoding a stable mRNA. The predicted polypeptide FbfA shows a homology of about 30% to NodC of rhizobia, an N-acetylglucosamine-transferase which is involved in the synthesis of the sugar backbone of lipo-oligosaccharides. These induce the formation of the root nodules in the Papilionaceae. Besides the predicted molecular mass of 45.5 kDa, the hydropathy profile reveals a structural relationship to the NodC polypeptide.

Full Text

The Full Text of this article is available as a PDF (370.8 KB).

Selected References

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

  1. Barany F. Single-stranded hexameric linkers: a system for in-phase insertion mutagenesis and protein engineering. Gene. 1985;37(1-3):111–123. doi: 10.1016/0378-1119(85)90263-x. [DOI] [PubMed] [Google Scholar]
  2. Barany F. Two-codon insertion mutagenesis of plasmid genes by using single-stranded hexameric oligonucleotides. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4202–4206. doi: 10.1073/pnas.82.12.4202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brewin N. J. Development of the legume root nodule. Annu Rev Cell Biol. 1991;7:191–226. doi: 10.1146/annurev.cb.07.110191.001203. [DOI] [PubMed] [Google Scholar]
  4. Caetano-Anollés G., Crist-Estes D. K., Bauer W. D. Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J Bacteriol. 1988 Jul;170(7):3164–3169. doi: 10.1128/jb.170.7.3164-3169.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  6. DeAngelis P. L., Papaconstantinou J., Weigel P. H. Molecular cloning, identification, and sequence of the hyaluronan synthase gene from group A Streptococcus pyogenes. J Biol Chem. 1993 Sep 15;268(26):19181–19184. [PubMed] [Google Scholar]
  7. Devreotes P. Dictyostelium discoideum: a model system for cell-cell interactions in development. Science. 1989 Sep 8;245(4922):1054–1058. doi: 10.1126/science.2672337. [DOI] [PubMed] [Google Scholar]
  8. Dworkin M. Recent advances in the social and developmental biology of the myxobacteria. Microbiol Rev. 1996 Mar;60(1):70–102. doi: 10.1128/mr.60.1.70-102.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Geremia R. A., Mergaert P., Geelen D., Van Montagu M., Holsters M. The NodC protein of Azorhizobium caulinodans is an N-acetylglucosaminyltransferase. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2669–2673. doi: 10.1073/pnas.91.7.2669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Glomp I., Saulnier P., Guespin-Michel J., Schairer H. U. Transfer of IncP plasmids into Stigmatella aurantiaca leading to insertional mutants affected in spore development. Mol Gen Genet. 1988 Oct;214(2):213–217. doi: 10.1007/BF00337713. [DOI] [PubMed] [Google Scholar]
  11. Gray J. X., Rolfe B. G. Exopolysaccharide production in Rhizobium and its role in invasion. Mol Microbiol. 1990 Sep;4(9):1425–1431. doi: 10.1111/j.1365-2958.1990.tb02052.x. [DOI] [PubMed] [Google Scholar]
  12. Göttfert M. Regulation and function of rhizobial nodulation genes. FEMS Microbiol Rev. 1993 Jan;10(1-2):39–63. doi: 10.1111/j.1574-6968.1993.tb05863.x. [DOI] [PubMed] [Google Scholar]
  13. Hartzell P., Kaiser D. Function of MglA, a 22-kilodalton protein essential for gliding in Myxococcus xanthus. J Bacteriol. 1991 Dec;173(23):7615–7624. doi: 10.1128/jb.173.23.7615-7624.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Henikoff S. Unidirectional digestion with exonuclease III in DNA sequence analysis. Methods Enzymol. 1987;155:156–165. doi: 10.1016/0076-6879(87)55014-5. [DOI] [PubMed] [Google Scholar]
  15. John M., Schmidt J., Wieneke U., Kondorosi E., Kondorosi A., Schell J. Expression of the nodulation gene nod C of Rhizobium meliloti in Escherichia coli: role of the nod C gene product in nodulation. EMBO J. 1985 Oct;4(10):2425–2430. doi: 10.1002/j.1460-2075.1985.tb03951.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. John M., Schmidt J., Wieneke U., Krüssmann H. D., Schell J. Transmembrane orientation and receptor-like structure of the Rhizobium meliloti common nodulation protein NodC. EMBO J. 1988 Mar;7(3):583–588. doi: 10.1002/j.1460-2075.1988.tb02850.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Johnson D., Roth L. E., Stacey G. Immunogold localization of the NodC and NodA proteins of Rhizobium meliloti. J Bacteriol. 1989 Sep;171(9):4583–4588. doi: 10.1128/jb.171.9.4583-4588.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kaiser D. Control of multicellular development: Dictyostelium and Myxococcus. Annu Rev Genet. 1986;20:539–566. doi: 10.1146/annurev.ge.20.120186.002543. [DOI] [PubMed] [Google Scholar]
  19. Kamst E., van der Drift K. M., Thomas-Oates J. E., Lugtenberg B. J., Spaink H. P. Mass spectrometric analysis of chitin oligosaccharides produced by Rhizobium NodC protein in Escherichia coli. J Bacteriol. 1995 Nov;177(21):6282–6285. doi: 10.1128/jb.177.21.6282-6285.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kessin R. H. Genetics of early Dictyostelium discoideum development. Microbiol Rev. 1988 Mar;52(1):29–49. doi: 10.1128/mr.52.1.29-49.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Klug G., Jock S., Rothfuchs R. The rate of decay of Rhodobacter capsulatus-specific puf mRNA segments is differentially affected by RNase E activity in Escherichia coli. Gene. 1992 Nov 2;121(1):95–102. doi: 10.1016/0378-1119(92)90166-m. [DOI] [PubMed] [Google Scholar]
  23. Klug G. The role of mRNA degradation in the regulated expression of bacterial photosynthesis genes. Mol Microbiol. 1993 Jul;9(1):1–7. doi: 10.1111/j.1365-2958.1993.tb01663.x. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Munoz-Dorado J., Inouye S., Inouye M. Eukaryotic-like protein serine/threonine kinases in Myxococcus xanthus, a developmental bacterium exhibiting social behavior. J Cell Biochem. 1993 Jan;51(1):29–33. doi: 10.1002/jcb.240510107. [DOI] [PubMed] [Google Scholar]
  27. Muñoz-Dorado J., Inouye S., Inouye M. A gene encoding a protein serine/threonine kinase is required for normal development of M. xanthus, a gram-negative bacterium. Cell. 1991 Nov 29;67(5):995–1006. doi: 10.1016/0092-8674(91)90372-6. [DOI] [PubMed] [Google Scholar]
  28. Nagahashi S., Sudoh M., Ono N., Sawada R., Yamaguchi E., Uchida Y., Mio T., Takagi M., Arisawa M., Yamada-Okabe H. Characterization of chitin synthase 2 of Saccharomyces cerevisiae. Implication of two highly conserved domains as possible catalytic sites. J Biol Chem. 1995 Jun 9;270(23):13961–13967. doi: 10.1074/jbc.270.23.13961. [DOI] [PubMed] [Google Scholar]
  29. Neumann B., Pospiech A., Schairer H. U. A physical and genetic map of the Stigmatella aurantiaca DW4/3.1 chromosome. Mol Microbiol. 1993 Dec;10(5):1087–1099. doi: 10.1111/j.1365-2958.1993.tb00979.x. [DOI] [PubMed] [Google Scholar]
  30. Neumann B., Pospiech A., Schairer H. U. Rapid isolation of genomic DNA from gram-negative bacteria. Trends Genet. 1992 Oct;8(10):332–333. doi: 10.1016/0168-9525(92)90269-a. [DOI] [PubMed] [Google Scholar]
  31. Qualls G. T., Stephens K., White D. Light-stimulated morphogenesis in the fruiting myxobacterium Stigmatella aurantiaca. Science. 1978 Aug 4;201(4354):444–445. doi: 10.1126/science.96528. [DOI] [PubMed] [Google Scholar]
  32. Qualls G. T., Stephens K., White D. Morphogenetic movements and multicellular development in the fruiting Myxobacterium, Stigmatella aurantiaca. Dev Biol. 1978 Sep;66(1):270–274. doi: 10.1016/0012-1606(78)90291-9. [DOI] [PubMed] [Google Scholar]
  33. Rosa F., Sargent T. D., Rebbert M. L., Michaels G. S., Jamrich M., Grunz H., Jonas E., Winkles J. A., Dawid I. B. Accumulation and decay of DG42 gene products follow a gradient pattern during Xenopus embryogenesis. Dev Biol. 1988 Sep;129(1):114–123. doi: 10.1016/0012-1606(88)90166-2. [DOI] [PubMed] [Google Scholar]
  34. Rossen L., Johnston A. W., Downie J. A. DNA sequence of the Rhizobium leguminosarum nodulation genes nodAB and C required for root hair curling. Nucleic Acids Res. 1984 Dec 21;12(24):9497–9508. doi: 10.1093/nar/12.24.9497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ruan K. H., Kulmacz R. J., Wilson A., Wu K. K. Highly sensitive fluorimetric enzyme immunoassay for prostaglandin H synthase solubilized from cultured cells. J Immunol Methods. 1993 Jun 4;162(1):23–30. doi: 10.1016/0022-1759(93)90403-t. [DOI] [PubMed] [Google Scholar]
  36. Semino C. E., Robbins P. W. Synthesis of "Nod"-like chitin oligosaccharides by the Xenopus developmental protein DG42. Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3498–3501. doi: 10.1073/pnas.92.8.3498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Simon R., O'Connell M., Labes M., Pühler A. Plasmid vectors for the genetic analysis and manipulation of rhizobia and other gram-negative bacteria. Methods Enzymol. 1986;118:640–659. doi: 10.1016/0076-6879(86)18106-7. [DOI] [PubMed] [Google Scholar]
  39. Spaink H. P., Wijfjes A. H., van der Drift K. M., Haverkamp J., Thomas-Oates J. E., Lugtenberg B. J. Structural identification of metabolites produced by the NodB and NodC proteins of Rhizobium leguminosarum. Mol Microbiol. 1994 Sep;13(5):821–831. doi: 10.1111/j.1365-2958.1994.tb00474.x. [DOI] [PubMed] [Google Scholar]
  40. Török I., Kondorosi E., Stepkowski T., Pósfai J., Kondorosi A. Nucleotide sequence of Rhizobium meliloti nodulation genes. Nucleic Acids Res. 1984 Dec 21;12(24):9509–9524. doi: 10.1093/nar/12.24.9509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Udo H., Munoz-Dorado J., Inouye M., Inouye S. Myxococcus xanthus, a gram-negative bacterium, contains a transmembrane protein serine/threonine kinase that blocks the secretion of beta-lactamase by phosphorylation. Genes Dev. 1995 Apr 15;9(8):972–983. doi: 10.1101/gad.9.8.972. [DOI] [PubMed] [Google Scholar]
  42. Valdivieso M. H., Mol P. C., Shaw J. A., Cabib E., Durán A. CAL1, a gene required for activity of chitin synthase 3 in Saccharomyces cerevisiae. J Cell Biol. 1991 Jul;114(1):101–109. doi: 10.1083/jcb.114.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  44. de Lorenzo V., Herrero M., Jakubzik U., Timmis K. N. Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol. 1990 Nov;172(11):6568–6572. doi: 10.1128/jb.172.11.6568-6572.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. van Rhijn P., Vanderleyden J. The Rhizobium-plant symbiosis. Microbiol Rev. 1995 Mar;59(1):124–142. doi: 10.1128/mr.59.1.124-142.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES