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Volume 153, Issue 5

ScbA from A3(2) has homology to fatty acid synthases and is able to synthesize -butyrolactones Free

Abstract

-Butyrolactones play an important role in the regulation of antibiotic production and differentiation in . However the biosynthetic pathway for these small molecules has not yet been determined, and synthesis has not been reported. The function of the AfsA family of proteins, originally proposed to catalyse -butyrolactone synthesis, has been in debate. To clarify the function of the AfsA family, and to understand the synthesis of the -butyrolactones, we performed analysis of this protein family. AfsA proteins consist of two divergent domains, each of which has similarity to the fatty acid synthesis enzymes FabA and FabZ. The two predicted active sites in ScbA, which is the AfsA orthologue found in , were mutated, and -butyrolactone biosynthesis was abolished in all four constructed mutants, strongly suggesting that ScbA has enzymic activity.

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  • Published Online:
Keyword(s): SCB, Streptomyces coelicolor butyrolactones and VB, virginiae butanolide
SGM
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2007-05-01
2024-04-19
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References

  1. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
     [Google Scholar]
  2. Ando N., Matsumori N., Sakuda S., Beppu T., Horinouchi S. 1997; Involvement of AfsA in A-factor biosynthesis as a key enzyme. J Antibiot 50:847–852 [CrossRef]
     [Google Scholar]
  3. Bentley S. D., Chater K. F., Cerdeno-Tarraga A. M., Challis G. L., Thomson N. R., James K. D., Harris D. E., Quail M. A., Kieser H. other authors 2002; Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2. Nature 417:141–147 [CrossRef]
     [Google Scholar]
  4. Bierman M., Logan R., O'Brien K., Seno E. T., Rao R. N., Schoner B. E. 1992; Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116:43–49 [CrossRef]
     [Google Scholar]
  5. Brock D. J., Kass L. R., Bloch K. 1967; β -hydroxydecanoyl thioester dehydrase. II. Mode of action. J Biol Chem 242:4432–4440
     [Google Scholar]
  6. Camilli A., Bassler B. L. 2006; Bacterial small-molecule signaling pathways. Science 311:1113–1116 [CrossRef]
     [Google Scholar]
  7. Chiu J., March P. E., Lee R., Tillett D. 2004; Site-directed, ligase-independent mutagenesis (slim): a single-tube methodology approaching 100 % efficiency in 4 h. Nucleic Acids Res 32:e174 [CrossRef]
     [Google Scholar]
  8. Chung C. T., Niemela S. L., Miller R. H. 1989; One-step preparation of competent Escherichia coli : transformation and storage of bacterial cells in the same solution. Proc Natl Acad Sci U S A 86:2172–2175 [CrossRef]
     [Google Scholar]
  9. Flett F., Mersinias V., Smith C. P. 1997; High efficiency intergeneric conjugal transfer of plasmid DNA from Escherichia coli to methyl DNA-restricting streptomycetes. FEMS Microbiol Lett 155:223–229 [CrossRef]
     [Google Scholar]
  10. Gesheva V., Rachev R., Bojkova S. 1997; Fatty acid composition of Streptomyces hygroscopicus strains producing antibiotics. Lett Appl Microbiol 24:109–112 [CrossRef]
     [Google Scholar]
  11. Hara O., Beppu T. 1982; Mutants blocked in streptomycin production in Streptomyces griseus – the role of A-factor. J Antibiot 35:349–358
     [Google Scholar]
  12. Heath R. J., Rock C. O. 1996; Roles of the FabA and FabZ β -hydroxyacyl-acyl carrier protein dehydratases in Escherichia coli fatty acid biosynthesis. J Biol Chem 271:27795–27801 [CrossRef]
     [Google Scholar]
  13. Horinouchi S., Nishiyama M., Suzuki H., Kumada Y., Beppu T. 1985; The cloned Streptomyces bikiniensis ( griseus ) A-factor determinant. J Antibiot 36:636–641
     [Google Scholar]
  14. Ikeda H., Ishikawa J., Hanamoto A., Shinose M., Kikuchi H., Shiba T., Sakaki Y., Hattori M., Omura S. 2003; Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21:526–531 [CrossRef]
     [Google Scholar]
  15. Kato J. Y., Funa N., Watanabe H., Ohnishi Y., Horinouchi S. 2007; Biosynthesis of γ-butyrolactone autoregulators that switch on secondary metabolism and morphological development in Streptomyces. Proc Natl Acad Sci U S A 104:2378–2383 [CrossRef]
     [Google Scholar]
  16. Kawachi R., Akashi T., Kamitani Y., Sy A., Wangchaisoonthorn U., Nihira T., Yamada Y. 2000; Identification of an a AfsA homologue (BarX) from Streptomyces virginiae as a pleiotropic regulator controlling autoregulator biosynthesis, virginiamycin biosynthesis and virginiamycin M1 resistance. Mol Microbiol 36:302–313 [CrossRef]
     [Google Scholar]
  17. Khokhlov A. S., Tovarova I. I., Borisova L. N., Pliner S. A., Shevchenko L. A., Schevchenko L. N., Kornitskaia EIa., Ivkina N. S., Rapoport I. A. 1967; The A-factor, responsible for streptomycin biosynthesis by mutant strains of Actinomyces streptomycini. Dokl Akad Nauk SSSR 177:232–235
     [Google Scholar]
  18. Kieser T., Bibb M. J., Buttner M. J., Chater K. F., Hopwood D. A. 2000 Practical Streptomyces Genetics Norwich: John Innes Foundation;
     [Google Scholar]
  19. Kimber M. S., Martin F., Lu Y., Houston S., Vedadi M., Dharamsi A., Fiebig K. M., Schmid M., Rock C. O. 2004; The structure of (3 R )-hydroxyacyl-acylcarrier protein dehydratase (FabZ) from Pseudomonas aeruginosa. J Biol Chem 2793:52593–52602
     [Google Scholar]
  20. Kostrewa D., Winkler F. K., Folkers G., Scapozza L., Perozzo R. 2005; The crystal structure of PfFabZ, the unique β -hydroxyacyl-ACP dehydratase involved in fatty acid biosynthesis of Plasmodium falciparum. Protein Sci 14:1570–1580
     [Google Scholar]
  21. Leblond P., Fischer G., Francou F. X., Berger F., Decaris B., Guérineau M. 1996; The unstable region of Streptomyces ambofaciens includes 210 kb terminal inverted repeats flanking the extremities of the linear chromosomal DNA. Mol Microbiol 19:261–271 [CrossRef]
     [Google Scholar]
  22. Leesong M., Henderson B. S., Gillig J. R., Schwab J. M., Smith J. L. 1996; Structure of a dehydratase-isomerase from the bacterial pathway for biosynthesis of unsaturated fatty acids: two catalytic activities in one active site. Structure 4:253–264 [CrossRef]
     [Google Scholar]
  23. MacNeil D. J., Occi J. L., Gewain K. M., MacNeil T., Gibbons P. H., Ruby C. L., Danid S. J. 1992; Complex organization of the Streptomyces avermitilis genes encoding the avermectin polyketide synthetase. Gene 155:119–125
     [Google Scholar]
  24. Marrakchi H., Choi K. H., Rock C. O. 2002; A new mechanism for anaerobic unsaturated fatty acid formation in Streptococcus pneumoniae. J Biol Chem 277:44809–44816 [CrossRef]
     [Google Scholar]
  25. Murzin A. G., Brenner S. E., Hubbard T., Chothia C. 1995; scop: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247:536–540
     [Google Scholar]
  26. Paget M. S. B., Chamberlin L., Atrih A., Foster S. J., Buttner M. J. 1999; Evidence that the extracytoplasmic function sigma factor σ E is required for normal cell wall structure in Streptomyces coelicolor A3(2. J Bacteriol 181:204–211
     [Google Scholar]
  27. Sakuda S., Higashi A., Nihira T., Yamada Y. 1990; Biosynthesis of virginiae butanolide A. J Am Chem Soc 112:898–899 [CrossRef]
     [Google Scholar]
  28. Sakuda S., Higashi A., Tanaka S., Nihira T., Yamada Y. 1992; Biosynthesis of virginiae butanolide A, a butyrolactone autoregulator from Streptomyces. J Am Chem Soc 114:663–668 [CrossRef]
     [Google Scholar]
  29. Sakuda S., Tanaka S., Mizuno K., Sukcharoen O., Nihira T., Yamada Y. 1993; Biosynthetic studies on virginiae butanolide A, a butyrolactone autoregulator from Streptomyces . Part 2. Preparation of possible biosynthetic intermediates and conversion experiments in a cell-free system. J Chem Soc Perkin Trans 1:2309–2315
     [Google Scholar]
  30. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  31. Shikura N., Yamamura J., Nihira T. 2002; barS1 , a gene for biosynthesis of a γ -butyrolactone autoregulator, a microbial signalling molecule eliciting antibiotic production in Streptomyces species. J Bacteriol 184:5151–5157 [CrossRef]
     [Google Scholar]
  32. Söding J., Biegert A., Lupas A. N. 2005; The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244–248 [CrossRef]
     [Google Scholar]
  33. Sonnhammer E. L., Eddy S. R., Birney E., Bateman A., Durbin R. 1998; Pfam: multiple sequence alignments and HMM-profiles of protein domains. Nucleic Acids Res 26:320–322 [CrossRef]
     [Google Scholar]
  34. Strauch E., Takano E., Baylis H. A., Bibb M. J. 1991; The stringent response in Streptomyces coelicolor A3(2. Mol Microbiol 5:289–298 [CrossRef]
     [Google Scholar]
  35. Takano E. 2006; γ -Butyrolactones: Streptomyces signaling molecules regulating antibiotic production and differentiation. Curr Opin Microbiol 9:287–294 [CrossRef]
     [Google Scholar]
  36. Takano E., Chakaraburtty R., Nihira T., Yamada Y., Bibb M. J. 2001; A complex role for the γ -butyrolactone SCB1 in regulating antibiotic production in Streptomyces coelicolor A3(2. Mol Microbiol 41:1015–1028
     [Google Scholar]
  37. Takano E., Kinoshita H., Mersinias V., Bucca G., Hotchkiss G., Nihira T., Smith C. P., Bibb M., Wohlleben W., Chater K. 2005; A bacterial hormone (the SCB1) directly controls the expression of a pathway-specific regulatory gene in the cryptic type I polyketide biosynthetic gene cluster of Streptomyces coelicolor. Mol Microbiol 56:465–479 [CrossRef]
     [Google Scholar]
  38. Vendeville A., Winzer K., Heurlier K., Tang C. M., Hardie K. R. 2005; Making ‘sense’ of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nature Rev Microbiol 3:383–396 [CrossRef]
     [Google Scholar]
  39. Venturi V. 2006; Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev 30:274–291 [CrossRef]
     [Google Scholar]
  40. Yamada Y. 1999; Autoregulatory factors and regulation of antibiotic production in Streptomyces . In Microbial Signalling and CommunicationSociety for General Microbiology Symposium no. 57 pp 177–196 Edited by England R. R., Hobbs G., Bainton N. J., Roberts D. McL. Cambridge: Cambridge University Press;
     [Google Scholar]
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ScbA from Streptomyces coelicolor A3(2) has homology to fatty acid synthases and is able to synthesize γ-butyrolactones
Microbiology 153, 1394 (2007); https://doi.org/10.1099/mic.0.2006/004432-0
/content/journal/micro/10.1099/mic.0.2006/004432-0
/content/journal/micro/10.1099/mic.0.2006/004432-0
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