Crossref journal-article
Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences (341)
Abstract

Lantibiotics are ribosomally synthesized, posttranslationally modified peptide antibiotics. The biosynthetic gene cluster for microbisporicin, a potent lantibiotic produced by the actinomycete Microbispora corallina containing chlorinated tryptophan and dihydroxyproline residues, was identified by genome scanning and isolated from an M. corallina cosmid library. Heterologous expression in Nonomuraea sp. ATCC 39727 confirmed that all of the genes required for microbisporicin biosynthesis were present in the cluster. Deletion, in M. corallina, of the gene ( mibA ) predicted to encode the prepropeptide abolished microbisporicin production. Further deletion analysis revealed insights into the biosynthesis of this unusual and potentially clinically useful lantibiotic, shedding light on mechanisms of regulation and self-resistance. In particular, we report an example of the involvement of a tryptophan halogenase in the modification of a ribosomally synthesized peptide and the pathway-specific regulation of an antibiotic biosynthetic gene cluster by an extracytoplasmic function σ factor–anti-σ factor complex.

Bibliography

Foulston, L. C., & Bibb, M. J. (2010). Microbisporicin gene cluster reveals unusual features of lantibiotic biosynthesis in actinomycetes. Proceedings of the National Academy of Sciences, 107(30), 13461–13466.

Authors 2
  1. Lucy C. Foulston (first)
  2. Mervyn J. Bibb (additional)
References 32 Referenced 125
  1. C Chatterjee, M Paul, L Xie, WA van der Donk, Biosynthesis and mode of action of lantibiotics. Chem Rev 105, 633–684 (2005). (10.1021/cr030105v) / Chem Rev / Biosynthesis and mode of action of lantibiotics by Chatterjee C (2005)
  2. Y Nakajima, V Kitpreechavanich, K Suzuki, T Kudo, Microbispora corallina sp. nov., a new species of the genus Microbispora isolated from Thai soil. Int J Syst Bacteriol 49, 1761–1767 (1999). (10.1099/00207713-49-4-1761) / Int J Syst Bacteriol / Microbispora corallina sp. nov., a new species of the genus Microbispora isolated from Thai soil by Nakajima Y (1999)
  3. MD Lee US Patent 6 551 591. 2003). (10.1016/S1351-4180(03)00931-0)
  4. F Castiglione, et al., Determining the structure and mode of action of microbisporicin, a potent lantibiotic active against multiresistant pathogens. Chem Biol 15, 22–31 (2008). (10.1016/j.chembiol.2007.11.009) / Chem Biol / Determining the structure and mode of action of microbisporicin, a potent lantibiotic active against multiresistant pathogens by Castiglione F (2008)
  5. A Lazzarini et al. WO/2005/014628 (February 17 2005). 2005).
  6. S Boakes, J Cortés, AN Appleyard, BA Rudd, MJ Dawson, Organization of the genes encoding the biosynthesis of actagardine and engineering of a variant generation system. Mol Microbiol 72, 1126–1136 (2009). (10.1111/j.1365-2958.2009.06708.x) / Mol Microbiol / Organization of the genes encoding the biosynthesis of actagardine and engineering of a variant generation system by Boakes S (2009)
  7. DA Widdick, et al., Cloning and engineering of the cinnamycin biosynthetic gene cluster from Streptomyces cinnamoneus cinnamoneus DSM 40005. Proc Natl Acad Sci USA 100, 4316–4321 (2003). (10.1073/pnas.0230516100) / Proc Natl Acad Sci USA / Cloning and engineering of the cinnamycin biosynthetic gene cluster from Streptomyces cinnamoneus cinnamoneus DSM 40005 by Widdick DA (2003)
  8. S Zehner, et al., A regioselective tryptophan 5-halogenase is involved in pyrroindomycin biosynthesis in Streptomyces rugosporus LL-42D005. Chem Biol 12, 445–452 (2005). (10.1016/j.chembiol.2005.02.005) / Chem Biol / A regioselective tryptophan 5-halogenase is involved in pyrroindomycin biosynthesis in Streptomyces rugosporus LL-42D005 by Zehner S (2005)
  9. K Rutherford, et al., Artemis: Sequence visualization and annotation. Bioinformatics 16, 944–945 (2000). (10.1093/bioinformatics/16.10.944) / Bioinformatics / Artemis: Sequence visualization and annotation by Rutherford K (2000)
  10. JR van der Meer, et al., Influence of amino acid substitutions in the nisin leader peptide on biosynthesis and secretion of nisin by Lactococcus lactis. J Biol Chem 269, 3555–3562 (1994). (10.1016/S0021-9258(17)41899-0) / J Biol Chem / Influence of amino acid substitutions in the nisin leader peptide on biosynthesis and secretion of nisin by Lactococcus lactis by van der Meer JR (1994)
  11. O McAuliffe, T O'Keeffe, C Hill, RP Ross, Regulation of immunity to the two-component lantibiotic, lacticin 3147, by the transcriptional repressor LtnR. Mol Microbiol 39, 982–993 (2001). (10.1046/j.1365-2958.2001.02290.x) / Mol Microbiol / Regulation of immunity to the two-component lantibiotic, lacticin 3147, by the transcriptional repressor LtnR by McAuliffe O (2001)
  12. LA Draper, RP Ross, C Hill, PD Cotter, Lantibiotic immunity. Curr Protein Pept Sci 9, 39–49 (2008). (10.2174/138920308783565750) / Curr Protein Pept Sci / Lantibiotic immunity by Draper LA (2008)
  13. C Dong, et al., Tryptophan 7-halogenase (PrnA) structure suggests a mechanism for regioselective chlorination. Science 309, 2216–2219 (2005). (10.1126/science.1116510) / Science / Tryptophan 7-halogenase (PrnA) structure suggests a mechanism for regioselective chlorination by Dong C (2005)
  14. IC Sutcliffe, DJ Harrington, Pattern searches for the identification of putative lipoprotein genes in Gram-positive bacterial genomes. Microbiology 148, 2065–2077 (2002). (10.1099/00221287-148-7-2065) / Microbiology / Pattern searches for the identification of putative lipoprotein genes in Gram-positive bacterial genomes by Sutcliffe IC (2002)
  15. AM van Wageningen, et al., Sequencing and analysis of genes involved in the biosynthesis of a vancomycin group antibiotic. Chem Biol 5, 155–162 (1998). (10.1016/S1074-5521(98)90060-6) / Chem Biol / Sequencing and analysis of genes involved in the biosynthesis of a vancomycin group antibiotic by van Wageningen AM (1998)
  16. C Tibazarwa, S Wuertz, M Mergeay, L Wyns, D van Der Lelie, Regulation of the cnr cobalt and nickel resistance determinant of Ralstonia eutropha (Alcaligenes eutrophus) CH34. J Bacteriol 182, 1399–1409 (2000). (10.1128/JB.182.5.1399-1409.2000) / J Bacteriol / Regulation of the cnr cobalt and nickel resistance determinant of Ralstonia eutropha (Alcaligenes eutrophus) CH34 by Tibazarwa C (2000)
  17. L Kall, A Krogh, EL Sonnhammer, Advantages of combined transmembrane topology and signal peptide prediction—the Phobius web server. Nucleic Acids Res 35, W429–W432 (2007). (10.1093/nar/gkm256) / Nucleic Acids Res / Advantages of combined transmembrane topology and signal peptide prediction—the Phobius web server by Kall L (2007)
  18. K Yanai, T Murakami, M Bibb, Amplification of the entire kanamycin biosynthetic gene cluster during empirical strain improvement of Streptomyces kanamyceticus. Proc Natl Acad Sci USA 103, 9661–9666 (2006). (10.1073/pnas.0603251103) / Proc Natl Acad Sci USA / Amplification of the entire kanamycin biosynthetic gene cluster during empirical strain improvement of Streptomyces kanamyceticus by Yanai K (2006)
  19. B Gust, GL Challis, K Fowler, T Kieser, KF Chater, PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci USA 100, 1541–1546 (2003). (10.1073/pnas.0337542100) / Proc Natl Acad Sci USA / PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin by Gust B (2003)
  20. M Sosio, S Stinchi, F Beltrametti, A Lazzarini, S Donadio, The gene cluster for the biosynthesis of the glycopeptide antibiotic A40926 by nonomuraea species. Chem Biol 10, 541–549 (2003). (10.1016/S1074-5521(03)00120-0) / Chem Biol / The gene cluster for the biosynthesis of the glycopeptide antibiotic A40926 by nonomuraea species by Sosio M (2003)
  21. GL Marcone, et al., Novel mechanism of glycopeptide resistance in the A40926 producer Nonomuraea sp. ATCC 39727. Antimicrob Agents Chemother 54, 2465–2472 (2010). (10.1128/AAC.00106-10) / Antimicrob Agents Chemother / Novel mechanism of glycopeptide resistance in the A40926 producer Nonomuraea sp. ATCC 39727 by Marcone GL (2010)
  22. TL Bailey, C Elkan, Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2, 28–36 (1994). / Proc Int Conf Intell Syst Mol Biol / Fitting a mixture model by expectation maximization to discover motifs in biopolymers by Bailey TL (1994)
  23. A Staroń, et al., The third pillar of bacterial signal transduction: Classification of the extracytoplasmic function (ECF) sigma factor protein family. Mol Microbiol 74, 557–581 (2009). (10.1111/j.1365-2958.2009.06870.x) / Mol Microbiol / The third pillar of bacterial signal transduction: Classification of the extracytoplasmic function (ECF) sigma factor protein family by Staroń A (2009)
  24. CT Walsh, et al., Tailoring enzymes that modify nonribosomal peptides during and after chain elongation on NRPS assembly lines. Curr Opin Chem Biol 5, 525–534 (2001). (10.1016/S1367-5931(00)00235-0) / Curr Opin Chem Biol / Tailoring enzymes that modify nonribosomal peptides during and after chain elongation on NRPS assembly lines by Walsh CT (2001)
  25. K Altena, A Guder, C Cramer, G Bierbaum, Biosynthesis of the lantibiotic mersacidin: Organization of a type B lantibiotic gene cluster. Appl Environ Microbiol 66, 2565–2571 (2000). (10.1128/AEM.66.6.2565-2571.2000) / Appl Environ Microbiol / Biosynthesis of the lantibiotic mersacidin: Organization of a type B lantibiotic gene cluster by Altena K (2000)
  26. LE Cooper, AL McClerren, A Chary, WA van der Donk, Structure-activity relationship studies of the two-component lantibiotic haloduracin. Chem Biol 15, 1035–1045 (2008). (10.1016/j.chembiol.2008.07.020) / Chem Biol / Structure-activity relationship studies of the two-component lantibiotic haloduracin by Cooper LE (2008)
  27. MSB Paget, H-J Hong, MJ Bibb, MJ Buttner, The ECF sigma factors of Streptomyces coelicolor A3(2). Signals, Switches, Regulons and Cascades: Control of Bacterial Gene Expression, eds DA Hodgson, CM Thomas (Cambridge Univ Press, Cambridge, UK), pp. 105–125 (2002). / Signals, Switches, Regulons and Cascades: Control of Bacterial Gene Expression by Paget MSB (2002)
  28. Y Luo, JD Helmann, Extracytoplasmic function sigma factors with overlapping promoter specificity regulate sublancin production in Bacillus subtilis. J Bacteriol 191, 4951–4958 (2009). (10.1128/JB.00549-09) / J Bacteriol / Extracytoplasmic function sigma factors with overlapping promoter specificity regulate sublancin production in Bacillus subtilis by Luo Y (2009)
  29. GL Marcone, L Carrano, F Marinelli, F Beltrametti, Protoplast preparation and reversion to the normal filamentous growth in antibiotic-producing uncommon actinomycetes. J Antibiot (Tokyo) 63, 83–88 (2010). (10.1038/ja.2009.127) / J Antibiot (Tokyo) / Protoplast preparation and reversion to the normal filamentous growth in antibiotic-producing uncommon actinomycetes by Marcone GL (2010)
  30. T Kieser, MJ Bibb, MJ Buttner, KF Chater, DA Hopwood Practical Streptomyces Genetics (John Innes Foundation, Norwich, UK, 2000). / Practical Streptomyces Genetics by Kieser T (2000)
  31. J Sambrook, EF Fritch, T Maniatis Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Lab Press, 3rd Ed, Cold Spring Harbor, NY, 2001). / Molecular Cloning: A Laboratory Manual by Sambrook J (2001)
  32. SF Altschul, W Gish, W Miller, EW Myers, DJ Lipman, Basic local alignment search tool. J Mol Biol 215, 403–410 (1990). (10.1016/S0022-2836(05)80360-2) / J Mol Biol / Basic local alignment search tool by Altschul SF (1990)
Dates
Type When
Created 15 years, 1 month ago (July 13, 2010, 9:46 p.m.)
Deposited 3 years, 2 months ago (June 7, 2022, 2:58 a.m.)
Indexed 3 months ago (June 3, 2025, 11:15 a.m.)
Issued 15 years, 1 month ago (July 13, 2010)
Published 15 years, 1 month ago (July 13, 2010)
Published Online 15 years, 1 month ago (July 13, 2010)
Published Print 15 years, 1 month ago (July 27, 2010)
Funders 0

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@article{Foulston_2010, title={Microbisporicin gene cluster reveals unusual features of lantibiotic biosynthesis in actinomycetes}, volume={107}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.1008285107}, DOI={10.1073/pnas.1008285107}, number={30}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Foulston, Lucy C. and Bibb, Mervyn J.}, year={2010}, month=jul, pages={13461–13466} }