Skip to main content
SpringerLink
Log in

Structure, function, and biosynthesis of thiazole/oxazole-modified microcins

  • Reveiws
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

A great variety of prokaryotic ribosomally synthesized and posttranslationally modified peptides (RiPPs) were predicted and identified experimentally owing to recent advances in large-scale genome sequencing and data analysis. Thiazole/oxazole-modified microcins (TOMMs) are a group of RiPPs that have characteristic thiazole and oxazole heterocycles derived from cysteine and serine residues. The review summarizes the available data on the classification, structure, and biosynthesis of TOMMs and discusses their biological activity and potential use in medicine.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

LAP:

linear azol(in)e-containing peptide

RiPP:

ribosomally synthesized and posttranslationally modified peptide

TOMM:

thiazole/oxazole-modified microcin

SLS:

streptolysin S

References

  1. Arnison P.G., Bibb M.J., Bierbaum G., Bowers A.A., Bugni T.S., Bulaj G., Camarero J.A., Campopiano D.J., Challis G.L., Clardy J., Cotter P.D., Craik D.J., Dawson M., Dittmann E., Donadio S., Dorrestein P.C., Entian K.D., Fischbach M.A., Garavelli J.S., Goransson U., Gruber C.W., Haft D.H., Hemscheidt T.K., Hertweck C., Hill C., Horswill A.R., Jaspars M., Kelly W.L., Klinman J.P., Kuipers O.P., Link A.J., Liu W., Marahiel M.A., Mitchell D.A., Moll G.N., Moore B.S., Muller R., Nair S.K., Nes I.F., Norris G.E., Olivera B.M., Onaka H., Patchett M.L., Piel J., Reaney M.J., Rebuffat S., Ross R.P., Sahl H.G., Schmidt E.W., Selsted M.E., Severinov K., Shen B., Sivonen K., Smith L., Stein T., Sussmuth R.D., Tagg J.R., Tang G.L., Truman A.W., Vederas J.C., Walsh C.T., Walton J.D., Wenzel S.C., Willey J.M., van der Donk W.A. 2013. Ribosomally synthesized and post-translationally modified peptide natural products: Overview and recommendations for a universal nomenclature. Nature Prod. Rep. 30, 108–160.

    CAS  Google Scholar 

  2. Lee S.W., Mitchell D.A., Markley A.L., Hensler M.E., Gonzalez D., Wohlrab A., Dorrestein P.C., Nizet V., Dixon J.E. 2008. Discovery of a widely distributed toxin biosynthetic gene cluster. Proc. Natl. Acad. Sci. U. S. A. 105, 5879–5884.

    CAS  PubMed Central  PubMed  Google Scholar 

  3. Oman T.J., van der Donk W.A. 2010. Follow the leader: The use of leader peptides to guide natural product biosynthesis. Nature Chem. Biol. 6, 9–18.

    CAS  Google Scholar 

  4. Zhang W., Li Y., Qian G., Wang Y., Chen H., Li Y.Z., Liu F., Shen Y., Du L. 2011. Identification and characterization of the anti-methicillin-resistant Staphylococcus aureus WAP-8294A2 biosynthetic gene cluster from Lysobacter enzymogenes OH11. Antimicrob. Agents Chemother. 55, 5581–5589.

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Gruber C.W., Cemazar M., Anderson M.A., Craik D.J. 2007. Insecticidal plant cyclotides and related cystine knot toxins. Toxicon. 49, 561–675.

    CAS  PubMed  Google Scholar 

  6. Kaas Q., Westermann J.C., Craik D.J. 2010. Conopeptide characterization and classifications: An analysis using ConoServer. Toxicon. 55, 1491–1509.

    CAS  PubMed  Google Scholar 

  7. Chatterjee C., Miller L.M., Leung Y.L., Xie L., Yi M., Kelleher N.L., van der Donk W.A. 2005. Lacticin 481 synthetase phosphorylates its substrate during antibiotic production. J. Am. Chem. Soc. 127, 15332–15333.

    CAS  PubMed  Google Scholar 

  8. Kelly W.L., Pan L., Li C. 2009. Thiostrepton biosynthesis: Prototype for a new family of bacteriocins. J. Am. Chem. Soc. 131, 4327–4334.

    CAS  PubMed  Google Scholar 

  9. Onaka H., Nakaho M., Hayashi K., Igarashi Y., Furumai T. 2005. Cloning and characterization of the goadsporin biosynthetic gene cluster from Streptomyces sp. TP-A0584. Microbiology. 151, 3923–3933.

    CAS  PubMed  Google Scholar 

  10. Melby J.O., Nard N.J., Mitchell D.A. 2011. Thiazole/oxazole-modified microcins: Complex natural products from ribosomal templates. Curr. Opin. Chem. Biol. 15, 369–378.

    CAS  PubMed  Google Scholar 

  11. Lee J., McIntosh J., Hathaway B.J., Schmidt E.W. 2009. Using marine natural products to discover a protease that catalyzes peptide macrocyclization of diverse substrates. J. Am. Chem. Soc. 131, 2122–2124.

    CAS  PubMed Central  PubMed  Google Scholar 

  12. Li Y.M., Milne J.C., Madison L.L., Kolter R., Walsh C.T. 1996. From peptide precursors to oxazole and thiazolecontaining peptide antibiotics: Microcin B17 synthase. Science. 274, 1188–1193.

    CAS  PubMed  Google Scholar 

  13. Milne J.C., Roy R.S., Eliot A.C., Kelleher N.L., Wokhlu A., Nickels B., Walsh C.T. 1999. Cofactor requirements and reconstitution of microcin B17 synthetase: A multienzyme complex that catalyzes the formation of oxazoles and thiazoles in the antibiotic microcin B17. Biochemistry. 38, 4768–4781.

    CAS  PubMed  Google Scholar 

  14. Dunbar K.L., Melby J.O., Mitchell D.A. 2012. YcaO domains use ATP to activate amide backbones during peptide cyclodehydrations. Nature Chem. Biol. 8, 569–575.

    CAS  Google Scholar 

  15. Haft D.H., Basu M.K., Mitchell D.A. 2010. Expansion of ribosomally produced natural products: A nitrile hydratase- and Nif11-related precursor family. BMC Biol. 8, 70.

    PubMed Central  PubMed  Google Scholar 

  16. Velasquez J.E., van der Donk W.A. 2011. Genome mining for ribosomally synthesized natural products. Curr. Opin. Chem. Biol. 15, 11–21.

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Yorgey P., Lee J., Kordel J., Vivas E., Warner P., Jebaratnam D., Kolter R. 1994. Posttranslational modifications in microcin B17 define an additional class of DNA gyrase inhibitor. Proc. Natl. Acad. Sci. U. S. A. 91, 4519–4523.

    CAS  PubMed Central  PubMed  Google Scholar 

  18. Garrido M.C., Herrero M., Kolter R., Moreno F. 1988. The export of the DNA replication inhibitor Microcin B17 provides immunity for the host cell. EMBO J. 7, 1853–1862.

    CAS  PubMed  Google Scholar 

  19. Sinha Roy R., Kelleher N.L., Milne J.C., Walsh C.T. 1999. In vivo processing and antibiotic activity of microcin B17 analogs with varying ring content and altered bisheterocyclic sites. Chem. Biol. 6, 305–318.

    CAS  PubMed  Google Scholar 

  20. Zamble D.B., McClure C.P., Penner-Hahn J.E., Walsh C.T. 2000. The McbB component of microcin B17 synthetase is a zinc metalloprotein. Biochemistry. 39, 16190–16199.

    CAS  PubMed  Google Scholar 

  21. Ghilarov D., Serebryakova M., Shkundina I., Severinov K. 2011. A major portion of DNA gyrase inhibitor microcin B17 undergoes an N,O-peptidyl shift during synthesis. J. Biol. Chem. 286, 26308–26318.

    CAS  PubMed  Google Scholar 

  22. Allali N., Afif H., Couturier M., van Melderen L. 2002. The highly conserved TldD and TldE proteins of Escherichia coli are involved in microcin B17 processing and in CcdA degradation. J. Bacteriol. 184, 3224–3231.

    CAS  PubMed Central  PubMed  Google Scholar 

  23. Heddle J.G., Blance S.J., Zamble D.B., Hollfelder F., Miller D.A., Wentzell L.M., Walsh C.T., Maxwell A. 2001. The antibiotic microcin B17 is a DNA gyrase poison: Characterisation of the mode of inhibition. J. Mol. Biol. 307, 1223–1234.

    CAS  PubMed  Google Scholar 

  24. Pierrat O.A., Maxwell A. 2003. The action of the bacterial toxin microcin B17. Insight into the cleavagereligation reaction of DNA gyrase. J. Biol. Chem. 278, 35016–35023.

    CAS  Google Scholar 

  25. Pierrat O.A., Maxwell A. 2005. Evidence for the role of DNA strand passage in the mechanism of action of microcin B17 on DNA gyrase. Biochemistry. 44, 4204–4215.

    CAS  PubMed  Google Scholar 

  26. Metelev M., Serebryakova M., Ghilarov D., Zhao Y., Severinov K. 2013. Microcin-B-like compounds produced by Pseudomonas syringae: Structure and species-specificity of antibacterial action. J. Bacteriol. 195(18), 4129–4137. doi 10.1128/JB.00665-13

    CAS  PubMed  Google Scholar 

  27. Severinov K., Semenova E., Kazakov A., Kazakov T., Gelfand M.S. 2007. Low-molecular-weight posttranslationally modified microcins. Mol. Microbiol. 65, 1380–1394.

    CAS  PubMed  Google Scholar 

  28. Cunningham M.W. 2000. Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev. 13, 470–511.

    CAS  PubMed Central  PubMed  Google Scholar 

  29. Todd E.W. 1938. The differentiation of two distinct serological varieties of streptolysin, streptolysin O and streptolysin S. J. Pathol. Bacteriol. 47, 423–445. doi 10.1002/path.1700470307

    CAS  Google Scholar 

  30. Molloy E.M., Cotter P.D., Hill C., Mitchell D.A., Ross R.P. 2011. Streptolysin S-like virulence factors: The continuing sagA. Nature Rev. Microbiol. 9, 670–681.

    CAS  Google Scholar 

  31. Betschel S.D., Borgia S.M., Barg N.L., Low D.E., De Azavedo J.C. 1998. Reduced virulence of group A streptococcal Tn916 mutants that do not produce streptolysin S. Infect. Immun. 66, 1671–1679.

    CAS  PubMed Central  PubMed  Google Scholar 

  32. Datta V., Myskowski S.M., Kwinn L.A., Chiem D.N., Varki N., Kansal R.G., Kotb M., Nizet V. 2005. Mutational analysis of the group A streptococcal operon encoding streptolysin S and its virulence role in invasive infection. Mol. Microbiol. 56, 681–695.

    CAS  PubMed  Google Scholar 

  33. Gonzalez D.J., Lee S.W., Hensler M.E., Markley A.L., Dahesh S., Mitchell D.A., Bandeira N., Nizet V., Dixon J.E., Dorrestein P.C. 2010. Clostridiolysin S, a post-translationally modified biotoxin from Clostridium botulinum. J. Biol. Chem. 285, 28220–28228.

    CAS  PubMed  Google Scholar 

  34. Chen X.H., Koumoutsi A., Scholz R., Eisenreich A., Schneider K., Heinemeyer I., Morgenstern B., Voss B., Hess W.R., Reva O., Junge H., Voigt B., Jungblut P.R., Vater J., Sussmuth R., Liesegang H., Strittmatter A., Gottschalk G., Borriss R. 2007. Comparative analysis of the complete genome sequence of the plant growthpromoting bacterium Bacillus amyloliquefaciens FZB42. Nature Biotechnol. 25, 1007–1014.

    CAS  Google Scholar 

  35. Scholz R., Molohon K.J., Nachtigall J., Vater J., Markley A.L., Sussmuth R.D., Mitchell D.A., Borriss R. 2011. Plantazolicin, a novel microcin B17/streptolysin S-like natural product from Bacillus amyloliquefaciens FZB42. J. Bacteriol. 193, 215–224.

    CAS  PubMed Central  PubMed  Google Scholar 

  36. Kalyon B., Helaly S.E., Scholz R., Nachtigall J., Vater J., Borriss R., Sussmuth R.D. 2011. Plantazolicin A and B: Structure elucidation of ribosomally synthesized thiazole/oxazole peptides from Bacillus amyloliquefaciens FZB42. Org. Lett. 13, 2996–2999.

    CAS  PubMed  Google Scholar 

  37. Molohon K.J., Melby J.O., Lee J., Evans B.S., Dunbar K.L., Bumpus S.B., Kelleher N.L., Mitchell D.A. 2011. Structure determination and interception of biosynthetic intermediates for the plantazolicin class of highly discriminating antibiotics. ACS Chem. Biol. 6, 1307–1313.

    CAS  PubMed Central  PubMed  Google Scholar 

  38. Onaka H., Tabata H., Igarashi Y., Sato Y., Furumai T. 2001. Goadsporin, a chemical substance which promotes secondary metabolism and morphogenesis in streptomycetes: 1. Purification and characterization. J. Antibiot. (Tokyo). 54, 1036–1044.

    CAS  Google Scholar 

  39. Onaka H. 2009. Biosynthesis of indolocarbazole and goadsporin, two different heterocyclic antibiotics produced by actinomycetes. Biosci. Biotechnol. Biochem. 73, 2149–2155.

    CAS  PubMed  Google Scholar 

  40. Donia M.S., Ravel J., Schmidt E.W. 2008. A global assembly line for cyanobactins. Nature Chem. Biol. 4, 341–343.

    CAS  Google Scholar 

  41. Schmidt E.W., Donia M.S. 2009. Chapter 23. Cyanobactin ribosomally synthesized peptides: A case of deep metagenome mining. Methods Enzymol. 458, 575–596.

    CAS  PubMed Central  PubMed  Google Scholar 

  42. Schmidt E.W., Nelson J.T., Rasko D.A., Sudek S., Eisen J.A., Haygood M.G., Ravel J. 2005. Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc. Natl. Acad. Sci. U. S. A. 102, 7315–7320.

    CAS  PubMed Central  PubMed  Google Scholar 

  43. Agarwal V., Pierce E., McIntosh J., Schmidt E.W., Nair S.K. 2012. Structures of cyanobactin maturation enzymes define a family of transamidating proteases. Chem. Biol. 19, 1411–1422.

    CAS  PubMed  Google Scholar 

  44. Jian X.H., Pan H.X., Ning T.T., Shi Y.Y., Chen Y.S., Li Y., Zeng X.W., Xu J., Tang G.L. 2012. Analysis of YM-216391 biosynthetic gene cluster and improvement of the cyclopeptide production in a heterologous host. ACS Chem. Biol. 7, 646–651.

    CAS  PubMed  Google Scholar 

  45. Sivonen K., Leikoski N., Fewer D.P., Jokela J. 2010. Cyanobactins: Ribosomal cyclic peptides produced by cyanobacteria. Appl. Microbiol. Biotechnol. 86, 1213–1225.

    CAS  PubMed Central  PubMed  Google Scholar 

  46. Ishida K., Matsuda H., Murakami M., Yamaguchi K. 1997. Kawaguchipeptin B, an antibacterial cyclic undecapeptide from the cyanobacterium Microcystis aeruginosa. J. Nature Prod. 60, 724–726.

    CAS  Google Scholar 

  47. Williams A.B., Jacobs R.S. 1993. A marine natural product, patellamide D, reverses multidrug resistance in a human leukemic cell line. Cancer Lett. 71, 97–102.

    CAS  PubMed  Google Scholar 

  48. Salvatella X., Caba J.M., Albericio F., Giralt E. 2003. Solution structure of the antitumor candidate trunkamide A by 2D NMR and restrained simulated annealing methods. J. Org. Chem. 68, 211–215.

    CAS  PubMed  Google Scholar 

  49. Leikoski N., Fewer D.P., Jokela J., Alakoski P., Wahlsten M., Sivonen K. 2012. Analysis of an inactive cyanobactin biosynthetic gene cluster leads to discovery of new natural products from strains of the genus Microcystis. PLoS ONE. 7, e43002.

    CAS  PubMed Central  PubMed  Google Scholar 

  50. Donia M.S., Schmidt E.W. 2011. Linking chemistry and genetics in the growing cyanobactin natural products family. Chem. Biol. 18, 508–519.

    CAS  PubMed Central  PubMed  Google Scholar 

  51. McIntosh J.A., Donia M.S., Nair S.K., Schmidt E.W. 2011. Enzymatic basis of ribosomal peptide prenylation in cyanobacteria. J. Am. Chem. Soc. 133, 13698–13705.

    CAS  PubMed Central  PubMed  Google Scholar 

  52. Leikoski N., Fewer D.P., Jokela J., Wahlsten M., Rouhiainen L., Sivonen K. 2010. Highly diverse cyanobactins in strains of the genus Anabaena. Appl. Environ. Microbiol. 76, 701–709.

    CAS  PubMed Central  PubMed  Google Scholar 

  53. Donia M.S., Hathaway B.J., Sudek S., Haygood M.G., Rosovitz M.J., Ravel J., Schmidt E.W. 2006. Natural combinatorial peptide libraries in cyanobacterial symbionts of marine ascidians. Nature Chem. Biol. 2, 729–735.

    CAS  Google Scholar 

  54. McIntosh J.A., Robertson C.R., Agarwal V., Nair S.K., Bulaj G.W., Schmidt E.W. 2010. Circular logic: Nonribosomal peptide-like macrocyclization with a ribosomal peptide catalyst. J. Am. Chem. Soc. 132, 15499–15501.

    CAS  PubMed Central  PubMed  Google Scholar 

  55. McIntosh J.A., Schmidt E.W. 2010. Marine molecular machines: Heterocyclization in cyanobactin biosynthesis. ChemBioChem. 11, 1413–1421.

    CAS  PubMed Central  PubMed  Google Scholar 

  56. McIntosh J.A., Donia M.S., Schmidt E.W. 2010. Insights into heterocyclization from two highly similar enzymes. J. Am. Chem. Soc. 132, 4089–4091.

    CAS  PubMed Central  PubMed  Google Scholar 

  57. Sudek S., Haygood M.G., Youssef D.T., Schmidt E.W. 2006. Structure of trichamide, a cyclic peptide from the bloom-forming cyanobacterium Trichodesmium erythraeum, predicted from the genome sequence. Appl. Environ. Microbiol. 72, 4382–4387.

    CAS  PubMed Central  PubMed  Google Scholar 

  58. Fu X., Do T., Schmitz F.J., Andrusevich V., Engel M.H. 1998. New cyclic peptides from the ascidian Lissoclinum patella. J. Nat. Prod. 61, 1547–1551.

    CAS  PubMed  Google Scholar 

  59. Bagley M.C., Dale J.W., Merritt E.A., Xiong X. 2005. Thiopeptide antibiotics. Chem. Rev. 105, 685–714.

    CAS  PubMed  Google Scholar 

  60. Carnio M.C., Holtzel A., Rudolf M., Henle T., Jung G., Scherer S. 2000. The macrocyclic peptide antibiotic micrococcin P(1) is secreted by the food-borne bacterium Staphylococcus equorum WS 2733 and inhibits Listeria monocytogenes on soft cheese. Appl. Environ. Microbiol. 66, 2378–2384.

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Fuller A.T. 1955. A new antibiotic of bacterial origin. Nature. 175, 722.

    CAS  PubMed  Google Scholar 

  62. Su T.L. 1948. Micrococcin, an antibacterial substance formed by a strain of Micrococcus. Br. J. Exp. Pathol. 29, 473–781.

    CAS  PubMed Central  PubMed  Google Scholar 

  63. Dutcher J.D., Vandeputte J. 1955. Thiostrepton, a new antibiotic: 2. Isolation and chemical characterization. Antibiot. Annu. 3, 560–561.

    Google Scholar 

  64. Liao R., Duan L., Lei C., Pan H., Ding Y., Zhang Q., Chen D., Shen B., Yu Y., Liu W. 2009. Thiopeptide biosynthesis featuring ribosomally synthesized precursor peptides and conserved posttranslational modifications. Chem. Biol. 16, 141–147.

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Heffron S.E., Jurnak F. 2000. Structure of an EF-Tu complex with a thiazolyl peptide antibiotic determined at 2.35 — bition of EF-Tu. Biochemistry. 39, 37–45.

    CAS  PubMed  Google Scholar 

  66. Parmeggiani A., Krab I.M., Okamura S., Nielsen R.C., Nyborg J., Nissen P. 2006. Structural basis of the action of pulvomycin and GE2270A on elongation factor Tu. Biochemistry. 45, 6846–6857.

    CAS  PubMed  Google Scholar 

  67. Hensens O.D., Albers-Schönberg G. 1978. Total structure of the peptide antibiotic components of thiopeptin by 1H and 13C NMR spectroscopy. Tetrahedron Lett. 19, 3649–3652.

    Google Scholar 

  68. Puar M.S., Ganguly A.K., Afonso A., Brambilla R., Mangiaracina P., Sarre O., MacFarlane R.D. 1981. Sch 18640, a new thiostrepton-type antibiotic. J. Am. Chem. Soc. 103, 5231–5233.

    CAS  Google Scholar 

  69. Nishimura H., Kimura T., Tawara K., Sasaki K., Nakajima K., Shimaoka N., Okamoto S., Shimohira M., Isono J. 1957. Aburamycin, a new antibiotic. J. Antibiot. (Tokyo). 10, 205–212.

    CAS  PubMed  Google Scholar 

  70. Puar M.S., Chan T.M., Hegde V., Patel M., Bartner P., Ng K.J., Pramanik B.N., MacFarlane R.D. 1998. Sch 40832, a novel thiostrepton from Micromonospora carbonacea. J. Antibiot. (Tokyo). 51, 221–224.

    CAS  Google Scholar 

  71. Benazet F., Cartier M., Florent J., Godard C., Jung G., Lunel J., Mancy D., Pascal C., Renaut J., Tarridec P., Theilleux J., Tissier R., Dubost M., Ninet L. 1980. Nosiheptide, a sulfur-containing peptide antibiotic isolated from Streptomyces actuosus 40037. Experientia. 36, 414–416.

    CAS  PubMed  Google Scholar 

  72. Lentzen G., Klinck R., Matassova N., Aboul-ela F., Murchie A.I. 2003. Structural basis for contrasting activities of ribosome binding thiazole antibiotics. Chem. Biol. 10, 769–778.

    CAS  PubMed  Google Scholar 

  73. Porse B.T., Cundliffe E., Garrett R.A. 1999. The antibiotic micrococcin acts on protein L11 at the ribosomal GTPase centre. J. Mol. Biol. 287, 33–45.

    CAS  PubMed  Google Scholar 

  74. Baumann S., Schoof S., Bolten M., Haering C., Takagi M., Shin-ya K., Arndt H.D. 2010. Molecular determinants of microbial resistance to thiopeptide antibiotics. J. Am. Chem. Soc. 132, 6973–6981.

    CAS  PubMed  Google Scholar 

  75. Rodnina M.V., Savelsbergh A., Matassova N.B., Katunin V.I., Semenkov Y.P., Wintermeyer W. 1999. Thiostrepton inhibits the turnover but not the GTPase of elongation factor G on the ribosome. Proc. Natl. Acad. Sci. U. S. A. 96, 9586–9590.

    CAS  PubMed Central  PubMed  Google Scholar 

  76. Harms J.M., Wilson D.N., Schluenzen F., Connell S.R., Stachelhaus T., Zaborowska Z., Spahn C.M., Fucini P. 2008. Translational regulation via L11: Molecular switches on the ribosome turned on and off by thiostrepton and micrococcin. Mol. Cell. 30, 26–38.

    CAS  PubMed  Google Scholar 

  77. Anborgh P.H., Parmeggiani A. 1991. New antibiotic that acts specifically on the GTP-bound form of elongation factor Tu. EMBO J. 10, 779–784.

    CAS  PubMed  Google Scholar 

  78. Mizuhara N., Kuroda M., Ogita A., Tanaka T., Usuki Y., Fujita K. 2011. Antifungal thiopeptide cyclothiazomycin B1 exhibits growth inhibition accompanying morphological changes via binding to fungal cell wall chitin. Bioorg. Med. Chem. 19, 5300–5310.

    CAS  PubMed  Google Scholar 

  79. Aoki M., Ohtsuka T., Yamada M., Ohba Y., Yoshizaki H., Yasuno H., Sano T., Watanabe J., Yokose K., Seto H. 1991. Cyclothiazomycin, a novel polythiazole-containing peptide with renin inhibitory activity. Taxonomy, fermentation, isolation and physico-chemical characterization. J. Antibiot. (Tokyo). 44, 582–588.

    CAS  Google Scholar 

  80. Morris R.P., Leeds J.A., Naegeli H.U., Oberer L., Memmert K., Weber E., LaMarche M.J., Parker C.N., Burrer N., Esterow S., Hein A.E., Schmitt E.K., Krastel P. 2009. Ribosomally synthesized thiopeptide antibiotics targeting elongation factor Tu. J. Am. Chem. Soc. 131, 5946–5955.

    CAS  PubMed  Google Scholar 

  81. Yu Y., Duan L., Zhang Q., Liao R., Ding Y., Pan H., Wendt-Pienkowski E., Tang G., Shen B., Liu W. 2009. Nosiheptide biosynthesis featuring a unique indole side ring formation on the characteristic thiopeptide framework. ACS Chem. Biol. 4, 855–864.

    CAS  PubMed Central  PubMed  Google Scholar 

  82. Wieland Brown L.C., Acker M.G., Clardy J., Walsh C.T., Fischbach M.A. 2009. Thirteen posttranslational modifications convert a 14-residue peptide into the antibiotic thiocillin. Proc. Natl. Acad. Sci. U. S. A. 106, 2549–2553.

    CAS  PubMed Central  PubMed  Google Scholar 

  83. Wang J., Yu Y., Tang K., Liu W., He X., Huang X., Deng Z. 2010. Identification and analysis of the biosynthetic gene cluster encoding the thiopeptide antibiotic cyclothiazomycin in Streptomyces hygroscopicus 10–22. Appl. Environ. Microbiol. 76, 2335–2344.

    CAS  PubMed Central  PubMed  Google Scholar 

  84. Bowers A.A., Walsh C.T., Acker M.G. 2010. Genetic interception and structural characterization of thiopeptide cyclization precursors from Bacillus cereus. J. Am. Chem. Soc. 132, 12182–12184.

    CAS  PubMed Central  PubMed  Google Scholar 

  85. Young T.S., Walsh C.T. 2011. Identification of the thiazolyl peptide GE37468 gene cluster from Streptomyces ATCC 55365 and heterologous expression in Streptomyces lividans. Proc. Natl. Acad. Sci. U. S. A. 108, 13053–13058.

    CAS  PubMed Central  PubMed  Google Scholar 

  86. Takahashi Y., Naganawa H., Takita T., Umezawa H., Nakamura S. 1976. The revised structure of bottromycin A2. J. Antibiot. (Tokyo). 29, 1120–1123.

    CAS  Google Scholar 

  87. Schipper D. 1983. The revised structure of bottromycin A2. J. Antibiot. (Tokyo). 36, 1076–1077.

    CAS  PubMed  Google Scholar 

  88. Shimamura H., Gouda H., Nagai K., Hirose T., Ichioka M., Furuya Y., Kobayashi Y., Hirono S., Sunazuka T., Omura S. 2009. Structure determination and total synthesis of bottromycin A2: A potent antibiotic against MRSA and VRE. Angew. Chem. Int. Ed. Engl. 48, 914–917.

    CAS  PubMed  Google Scholar 

  89. Gouda H., Kobayashi Y., Yamada T., Ideguchi T., Sugawara A., Hirose T., Omura S., Sunazuka T., Hirono S. 2012. Three-dimensional solution structure of bottromycin A2: A potent antibiotic active against methicillin-resistant Staphylococcus aureus and vancomycinresistant enterococci. Chem. Pharm. Bull. (Tokyo). 60, 169–171.

    CAS  PubMed  Google Scholar 

  90. Waisvisz J.M., van der Hoeven M.G., Nijenhuis B.t. 1957. The structure of the sulfur-containing moiety of bottromycin. J. Am. Chem. Soc. 79, 4524–4527.

    CAS  Google Scholar 

  91. Tokuyama H., Yokoshima S., Yamashita T., Fukuyama T. 1998. A novel ketone synthesis by a palladium-catalyzed reaction of thiol esters and organozinc reagents. Tetrahedron Lett. 39, 3189–3192.

    CAS  Google Scholar 

  92. Kobayashi Y., Ichioka M., Hirose T., Nagai K., Matsumoto A., Matsui H., Hanaki H., Masuma R., Takahashi Y., Omura S., Sunazuka T. 2010. Bottromycin derivatives: Efficient chemical modifications of the ester moiety and evaluation of anti-MRSA and anti-VRE activities. Bioorg. Med. Chem. Lett. 20, 6116–6120.

    CAS  PubMed  Google Scholar 

  93. Otaka T., Kaji A. 1976. Mode of action of bottromycin A2. Release of aminoacyl- or peptidyl-tRNA from ribosomes. J. Biol. Chem. 251, 2299–2306.

    CAS  PubMed  Google Scholar 

  94. Otaka T., Kaji A. 1981. Mode of action of bottromycin A2: Effect on peptide bond formation. FEBS Lett. 123, 173–176.

    CAS  PubMed  Google Scholar 

  95. Otaka T., Kaji A. 1983. Mode of action of bottromycin A2: Effect of bottromycin A2 on polysomes. FEBS Lett. 153, 53–59.

    CAS  PubMed  Google Scholar 

  96. Huo L., Rachid S., Stadler M., Wenzel S.C., Muller R. 2012. Synthetic biotechnology to study and engineer ribosomal bottromycin biosynthesis. Chem. Biol. 19, 1278–1287.

    CAS  PubMed  Google Scholar 

  97. Crone W.J.K., Leeper F.J., Truman A.W. 2012. Identification and characterisation of the gene cluster for the anti-MRSA antibiotic bottromycin: expanding the biosynthetic diversity of ribosomal peptides. Chemical Sci. 3, 3516–3521.

    CAS  Google Scholar 

  98. Gomez-Escribano J.P., Song L., Bibb M.J., Challis G.L. 2012. Posttranslational β-methylation and macrolactamidination in the biosynthesis of the bottromycin complex of ribosomal peptide antibiotics. Chemical Sci. 3, 3522–3525.

    CAS  Google Scholar 

  99. Hou Y., Tianero M.D., Kwan J.C., Wyche T.P., Michel C.R., Ellis G.A., Vazquez-Rivera E., Braun D.R., Rose W.E., Schmidt E.W., Bugni T.S. 2012. Structure and biosynthesis of the antibiotic bottromycin D. Org Lett. 14, 5050–5053.

    CAS  PubMed Central  PubMed  Google Scholar 

  100. Tanaka N., Nishimura T., Nakamura S., Umezawa H. 1966. Biological studies on bottromycin A and its hydrazide. J. Antibiot. (Tokyo). 19, 149–154.

    CAS  Google Scholar 

  101. Inoue M., Shinohara N., Tanabe S., Takahashi T., Okura K., Itoh H., Mizoguchi Y., Iida M., Lee N., Matsuoka S. 2010. Total synthesis of the large nonribosomal peptide polytheonamide B. Nature Chem. 2, 280–285.

    CAS  Google Scholar 

  102. McIntosh J.A., Donia M.S., Schmidt E.W. 2009. Ribosomal peptide natural products: Bridging the ribosomal and nonribosomal worlds. Nature Prod. Rep. 26, 537–559.

    CAS  Google Scholar 

  103. Wang H., Fewer D.P., Sivonen K. 2011. Genome mining demonstrates the widespread occurrence of gene clusters encoding bacteriocins in cyanobacteria. PLoS ONE. 6, e22384.

    CAS  PubMed Central  PubMed  Google Scholar 

  104. Kersten R.D., Yang Y.L., Xu Y., Cimermancic P., Nam S.J., Fenical W., Fischbach M.A., Moore B.S., Dorrestein P.C. 2011. A mass spectrometry-guided genome mining approach for natural product peptidogenomics. Nature Chem. Biol. 7, 794–802.

    CAS  Google Scholar 

  105. Freeman M.F., Gurgui C., Helf M.J., Morinaka B.I., Uria A.R., Oldham N.J., Sahl H.G., Matsunaga S., Piel J. 2012. Metagenome mining reveals polytheonamides as posttranslationally modified ribosomal peptides. Science. 338, 387–390.

    CAS  PubMed  Google Scholar 

  106. Deane C.D., Melby J.O., Molohon K.J., Susarrey A.R., Mitchell D.A. 2013. Engineering unnatural variants of plantazolicin through codon reprogramming. ACS Chem. Biol. 8(9), 1998–2008. doi 10.1021/cb4003392

    CAS  PubMed  Google Scholar 

  107. Lee J., Hao Y., Blair P.M., Melby J.O., Agarwal V., Burkhart B.J., Nair S.K., Mitchell D.A. 2013. Structural and functional insight into an unexpectedly selective N-methyltransferase involved in plantazolicin biosynthesis. Proc. Natl. Acad. Sci. U. S. A. 110, 12954–12959.

    CAS  PubMed Central  PubMed  Google Scholar 

  108. Dunbar K.L., Mitchell D.A. 2013. Insights into the mechanism of peptide cyclodehydrations achieved through the chemoenzymatic generation of amide derivatives. J. Am. Chem. Soc. 135, 8692–8701.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Gene Biology, Russian Academy of Sciences, Moscow, 119334, Russia

    M. V. Metelev & D. A. Ghilarov

Authors
  1. M. V. Metelev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. A. Ghilarov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. V. Metelev.

Additional information

Original Russian Text © M.V. Metelev, D.A. Ghilarov, 2014, published in Molekulyarnaya Biologiya, 2014, Vol. 48, No. 1, pp. 36–54.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Metelev, M.V., Ghilarov, D.A. Structure, function, and biosynthesis of thiazole/oxazole-modified microcins. Mol Biol 48, 29–45 (2014). https://doi.org/10.1134/S0026893314010105

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893314010105

Keywords

Search

Navigation