Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1996 Jul;178(13):3785–3790. doi: 10.1128/jb.178.13.3785-3790.1996

Changes in patterns of ADP-ribosylated proteins during differentiation of Streptomyces coelicolor A3(2) and its development mutants.

J Shima 1, A Penyige 1, K Ochi 1
PMCID: PMC232637  PMID: 8682781

Abstract

Mutants resistant to 3-aminobenzamide, a known inhibitor of ADP-ribosyltransferase, were obtained from Streptomyces coelicolor A3(2). One (strain 27) was analyzed in detail. Mutant 27 had a reduced ADP-ribosyl-transferase activity, exhibited substantial changes from the wild type in ADP-ribosylated protein profile during cell aging, and was defective in producing aerial mycelium and antibiotics. A 92-kDa ADP-ribosylated protein disappeared at the onset of differentiation in the parent strain but was present in mutant 27. Four ADP-ribosylated proteins (39, 41, 43, and 46 kDa) appeared at the onset of differentiation in the parent strain but were missing in mutant 27. Failure to ADP-ribosylate these four proteins was detected when the parent strain was grown in the presence of subinhibitory amounts of 3-aminobenzamide. Genetic analysis showed that the mutation, named brgA, conferring resistance to 3-aminobenzamide, cosegregated with the altered phenotypes (i.e., defects in ADP-ribosylation and aerial mycelium formation) and was mapped to a new locus near uraA. The brgA mutants were nonconditionally deficient in producing aerial mycelium and antibiotics, as determined by using various media, and had a morphological and physiological phenotype quite different from that of a bldG mutant carrying a mutation which was previously mapped near uraA. Among the known bld mutants, bldA, bldD, and bldG mutants exhibited a ADP-ribosylated protein profile similar to that of the wild type, while like mutant 27, bldB, bldC, and bldH mutants failed to ADP-ribosylate certain proteins.

Full Text

The Full Text of this article is available as a PDF (602.9 KB).

Selected References

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

  1. Champness W. C. New loci required for Streptomyces coelicolor morphological and physiological differentiation. J Bacteriol. 1988 Mar;170(3):1168–1174. doi: 10.1128/jb.170.3.1168-1174.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Eastman D., Dworkin M. Endogenous ADP-ribosylation during development of the prokaryote Myxococcus xanthus. Microbiology. 1994 Nov;140(Pt 11):3167–3176. doi: 10.1099/13500872-140-11-3167. [DOI] [PubMed] [Google Scholar]
  3. Edmonds C., Griffin G. E., Johnstone A. P. Demonstration and partial characterization of ADP-ribosylation in Pseudomonas maltophilia. Biochem J. 1989 Jul 1;261(1):113–118. doi: 10.1042/bj2610113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Fernández-Moreno M. A., Martín-Triana A. J., Martínez E., Niemi J., Kieser H. M., Hopwood D. A., Malpartida F. abaA, a new pleiotropic regulatory locus for antibiotic production in Streptomyces coelicolor. J Bacteriol. 1992 May;174(9):2958–2967. doi: 10.1128/jb.174.9.2958-2967.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Hartmann A., Fu H., Burris R. H. Regulation of nitrogenase activity by ammonium chloride in Azospirillum spp. J Bacteriol. 1986 Mar;165(3):864–870. doi: 10.1128/jb.165.3.864-870.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Itoh M., Penyige A., Okamoto S., Ochi K. Proteins that interact with GTP in Streptomyces griseus and its possible implication in morphogenesis. FEMS Microbiol Lett. 1996 Jan 15;135(2-3):311–316. doi: 10.1111/j.1574-6968.1996.tb08006.x. [DOI] [PubMed] [Google Scholar]
  7. Merrick M. J. A morphological and genetic mapping study of bald colony mutants of Streptomyces coelicolor. J Gen Microbiol. 1976 Oct;96(2):299–315. doi: 10.1099/00221287-96-2-299. [DOI] [PubMed] [Google Scholar]
  8. Obaya A. J., Guijarro J. Specific in vitro guanylylation of a 43-kilodalton membrane-associated protein of Streptomyces coelicolor. J Bacteriol. 1993 May;175(10):3220–3223. doi: 10.1128/jb.175.10.3220-3223.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ochi K. A relaxed (rel) mutant of Streptomyces coelicolor A3(2) with a missing ribosomal protein lacks the ability to accumulate ppGpp, A-factor and prodigiosin. J Gen Microbiol. 1990 Dec;136(12):2405–2412. doi: 10.1099/00221287-136-12-2405. [DOI] [PubMed] [Google Scholar]
  10. Ochi K. Metabolic initiation of differentiation and secondary metabolism by Streptomyces griseus: significance of the stringent response (ppGpp) and GTP content in relation to A factor. J Bacteriol. 1987 Aug;169(8):3608–3616. doi: 10.1128/jb.169.8.3608-3616.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ochi K., Penyige A., Barabas G. The possible role of ADP-ribosylation in sporulation and streptomycin production by Streptomyces griseus. J Gen Microbiol. 1992 Aug;138(Pt 8):1745–1750. doi: 10.1099/00221287-138-8-1745. [DOI] [PubMed] [Google Scholar]
  12. Ochi K. Streptomyces relC mutants with an altered ribosomal protein ST-L11 and genetic analysis of a Streptomyces griseus relC mutant. J Bacteriol. 1990 Jul;172(7):4008–4016. doi: 10.1128/jb.172.7.4008-4016.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Penyige A., Barabás G., Szabó I., Ensign J. C. ADP-ribosylation of membrane proteins of Streptomyces griseus strain 52-1. FEMS Microbiol Lett. 1990 Jun 1;57(3):293–297. doi: 10.1016/0378-1097(90)90083-3. [DOI] [PubMed] [Google Scholar]
  14. Spangler B. D. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol Rev. 1992 Dec;56(4):622–647. doi: 10.1128/mr.56.4.622-647.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ueda K., Hayaishi O. ADP-ribosylation. Annu Rev Biochem. 1985;54:73–100. doi: 10.1146/annurev.bi.54.070185.000445. [DOI] [PubMed] [Google Scholar]

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

RESOURCES