1887

Microbiology Society logo

Volume 152, Issue 10

Glycerol, ethylene glycol and propanediol elicit pimaricin biosynthesis in the PI-factor-defective strain 287 and increase polyene production in several wild-type actinomycetes Free

Abstract

Production of pimaricin by ATCC 27448 is elicited by the PI-factor, an autoinducer secreted by the producer strain during the rapid growth phase. Exogenous PI-factor restored pimaricin production in a mutant strain 287 defective in PI-factor biosynthesis. During purification of the PI-factor, a second pimaricin-inducing fraction different from PI-factor was isolated from the culture broth of wild-type ATCC 27448. After purification by HPLC and analysis by MS and NMR, this active fraction was shown to contain glycerol and lactic acid. Pure glycerol restored pimaricin production in liquid cultures of the autoinducer-defective 287 mutant. A similar effect was exerted by ethylene glycol, 1,2-propanediol and 1,3-propanediol but not by higher polyalcohols or by glycerol acetate or glycerol lactate esters. Glycerol stimulated (30–270 %) the production of six different polyene macrolide antibiotics by their respective producer strains. Addition of glycerol to the inducer-defective 287 strain restored pimaricin production but did not result in extracellular or intracellular accumulation of PI-factor. Exogenously added PI-factor was internalized by the cells in the presence of glycerol, and a mixture of both PI-factor and glycerol produced a slightly higher inducing effect on pimaricin production than PI-factor alone. In summary, glycerol, ethylene glycol and propanediol exert a bypass of the PI-factor inducing effect on pimaricin biosynthesis.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28953-0
2006-10-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/10/3147.html?itemId=/content/journal/micro/10.1099/mic.0.28953-0&mimeType=html&fmt=ahah

References

  1. Antón N, Mendes M. V, Aparicio J. F, Martín J. F. 2004; Identification of PimR as a positive regulator of pimaricin biosynthesis in Streptomyces natalensis . J Bacteriol 186:2567–2575 [CrossRef]
     [Google Scholar]
  2. Aparicio J. F, Colina A, Ceballos E, Martín J. F. 1999; The biosynthetic gene cluster for the 26-membered ring polyene macrolide pimaricin. A new polyketide synthase organization encoded by two subclusters separated by functionalization genes. J Biol Chem 274:10133–10139 [CrossRef]
     [Google Scholar]
  3. Aparicio J. F, Fouces R, Mendes M. V, Olivera N, Martín J. F. 2000; A complex multienzyme system encoded by five polyketide synthase genes is involved in the biosynthesis of the 26-membered polyene macrolide pimaricin in Streptomyces natalensis . Chem Biol 7:895–905 [CrossRef]
     [Google Scholar]
  4. Aparicio J. F, Caffrey P, Gil J. A, Zotchev Z. A. 2003; Polyene antibiotic biosynthesis gene clusters. Appl Microbiol Biotechnol 61:179–188 [CrossRef]
     [Google Scholar]
  5. Aparicio J. F, Mendes M. V, Recio E, Antón N, Martín J. F. 2004; Polyene macrolide antibiotic biosynthesis. Curr Med Chem 11:1645–1656
     [Google Scholar]
  6. Berdy J. 2005; Bioactive microbial metabolites. A personal view. J Antibiot 58:1–26 [CrossRef]
     [Google Scholar]
  7. Borodina I, Eliasson A, Nielsen J, Schöller C. 2005; Metabolic network analysis of Streptomyces tenebrarius , a Streptomyces species with an active Entner–Doudoroff pathway. Appl Environ Microbiol 71:2294–2302 [CrossRef]
     [Google Scholar]
  8. Brautaset T, Sekurova O. N, Sletta H, Ellingsen T. E, Strøm A. R, Valla S, Zotchev S. B. 2000; Biosynthesis of the polyene antifungal antibiotic nystatin in Streptomyces noursei ATCC 11455: analysis of the gene cluster and deduction of the biosynthetic pathway. Chem Biol 7:395–403 [CrossRef]
     [Google Scholar]
  9. Caffrey P, Lynch S, Flood E, Finnan S, Oliynyk M. 2001; Amphotericin biosynthesis in Streptomyces nodosus : deductions from analysis of polyketide synthase and late genes. Chem Biol 8:713–723 [CrossRef]
     [Google Scholar]
  10. Dworkin M, Gibson S. M. 1964; A system for studying microbial morphogenesis: rapid formation of microcysts in Myxococcus xanthus . Science 146:243–244 [CrossRef]
     [Google Scholar]
  11. Federle M. J, Bassler B. L. 2003; Interspecies communication in bacteria. J Clin Invest 112:1291–1299 [CrossRef]
     [Google Scholar]
  12. Fray R. G. 2002; Altering plant–microbe interaction through artificially manipulating bacterial quorum sensing. Ann Botany 89:245–253 [CrossRef]
     [Google Scholar]
  13. Horinouchi S, Beppu T. 1992; Autoregulatory factors and communication in actinomycetes. Annu Rev Microbiol 46:377–398 [CrossRef]
     [Google Scholar]
  14. Jonsbu E, McIntyre M, Nielsen J. 2002; The influence of carbon sources and morphology on nystatin production by Streptomyces noursei . J Biotechnol 95:133–144 [CrossRef]
     [Google Scholar]
  15. Kaiser D, Losick R. 1993; How and why bacteria talk to each other. Cell 73:873–885 [CrossRef]
     [Google Scholar]
  16. Kaiser D, Onken U, Sattler I, Zeeck A. 1994; Influence of increased dissolved oxygen concentration on the formation of secondary metabolites by manumycin-producing Streptomyces parvulus . Appl Microbiol Biotechnol 41:309–312 [CrossRef]
     [Google Scholar]
  17. Killeen K. P, Nelson D. R. 1988; Acceleration of starvation- and glycerol-induced myxospore formation by prior heat shock in Myxococcus xanthus . J Bacteriol 170:5200–5207
     [Google Scholar]
  18. Klose K. E. 2006; Increased chatter: cyclic dipeptides as molecules of chemical communication in Vibrio spp. J Bacteriol 188:2025–2026 [CrossRef]
     [Google Scholar]
  19. Lee K. M, Lee C. K, Park H. R, Kitani S, Nihira T, Hwang Y. I. 2005; Cloning and in vivo functional analysis by disruption of a gene encoding the gamma-butyrolactone autoregulator receptor from Streptomyces natalensis . Arch Microbiol 184:249–257 [CrossRef]
     [Google Scholar]
  20. Martín J. F. 1977; Biosynthesis of polyene macrolide antibiotics. Annu Rev Microbiol 31:13–38 [CrossRef]
     [Google Scholar]
  21. Martín J. F, Gutiérrez S., Aparicio J. F. 2000; Secondary metabolites. In Encyclopedia of Microbiology vol. 4, 2nd edn. pp  213–236 Edited by Lederberg J. San Diego, CA: Academic Press;
     [Google Scholar]
  22. Mendes M. V, Recio E, Fouces R, Luiten R, Aparicio J. F, Martín J. F. 2001; Engineered biosynthesis of novel polyenes: a pimaricin derivative produced by targeted gene disruption in Streptomyces natalensis . Chem Biol 8:635–644 [CrossRef]
     [Google Scholar]
  23. Mendes M. V, Aparicio J. F, Antón N, Martín J. F. 2005; Characterization of the polyene macrolide P450 epoxidase from Streptomyces natalensis that converts de-epoxypimaricin into pimaricin. Biochem J 386:57–62 [CrossRef]
     [Google Scholar]
  24. Moraleda-Muñoz A, Carrero-Lérida J, Extremera A. L, Arias J. M, Muñoz-Dorado J. 2001; Glycerol 3-phosphate inhibits swarming and aggregation of Myxococcus xanthus . J Bacteriol 183:6135–6139 [CrossRef]
     [Google Scholar]
  25. Nodwell J. R, Losick R. 1998; Purification of an extracellular signaling molecule involved in production of aerial mycelium by Streptomyces coelicolor . J Bacteriol 180:1334–1337
     [Google Scholar]
  26. Omura S, Tanaka H. 1984 In Macrolide Antibiotics: Chemistry, Biology and Practice pp  351–404 Edited by Omura S. New York: Academic Press;
     [Google Scholar]
  27. Recio E, Colinas A, Rumbero A, Aparicio J. F, Martín J. F. 2004; PI factor, a novel type quorum-sensing inducer, elicits pimaricin production in Streptomyces natalensis . J Biol Chem 279:41586–41593 [CrossRef]
     [Google Scholar]
  28. Robson N. D, Cox A. R, McGowan S. J, Bycroft B. W, Salmond G. P. 1997; Bacterial N -acyl-homoserine-lactone-dependent signalling and its potential biotechnological applications. Trends Biotechnol 15:458–464 [CrossRef]
     [Google Scholar]
  29. Taga M. E, Semmelhack J. L, Bassler B. L. 2001; The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium . Mol Microbiol 42:777–793
     [Google Scholar]
  30. Vining L. C. 1992; Secondary metabolism, inventive evolution and biochemical diversity – a review. Gene 115:135–140 [CrossRef]
     [Google Scholar]
  31. Wilker W, Leibfritz D, Kerssebaum R, Bermell W. 1993; Gradient selection in reverse heteronuclear correlation spectroscopy. Magn Reson Chem 31:287 [CrossRef]
     [Google Scholar]
  32. Xavier K. B, Bassler B. L. 2005; Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli . J Bacteriol 187:238–248 [CrossRef]
     [Google Scholar]
  33. Yamada Y, Nihira T. 1999; Microbial hormones and microbial chemical ecology. In Comprehensive Natural Products Chemistry vol. 8 pp  377–413 Edited by Barton S. D., Nakanishi K., Meth-Cohn O. Amsterdam & New York: Elsevier;
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28953-0
Loading
Glycerol, ethylene glycol and propanediol elicit pimaricin biosynthesis in the PI-factor-defective strain Streptomyces natalensis npi287 and increase polyene production in several wild-type actinomycetes
Microbiology 152, 3147 (2006); https://doi.org/10.1099/mic.0.28953-0
/content/journal/micro/10.1099/mic.0.28953-0
/content/journal/micro/10.1099/mic.0.28953-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error