Analysis of the biosynthetic gene cluster for the polyether antibiotic monensin in Streptomyces cinnamonensis and evidence for the role of monB and monC genes in oxidative cyclization

Mol Microbiol. 2003 Sep;49(5):1179-90. doi: 10.1046/j.1365-2958.2003.03571.x.

Abstract

The analysis of a candidate biosynthetic gene cluster (97 kbp) for the polyether ionophore monensin from Streptomyces cinnamonensis has revealed a modular polyketide synthase composed of eight separate multienzyme subunits housing a total of 12 extension modules, and flanked by numerous other genes for which a plausible function in monensin biosynthesis can be ascribed. Deletion of essentially all these clustered genes specifically abolished monensin production, while overexpression in S. cinnamonensis of the putative pathway-specific regulatory gene monR led to a fivefold increase in monensin production. Experimental support is presented for a recently-proposed mechanism, for oxidative cyclization of a linear polyketide intermediate, involving four enzymes, the products of monBI, monBII, monCI and monCII. In frame deletion of either of the individual genes monCII (encoding a putative cyclase) or monBII (encoding a putative novel isomerase) specifically abolished monensin production. Also, heterologous expression of monCI, encoding a flavin-linked epoxidase, in S. coelicolor was shown to significantly increase the ability of S. coelicolor to epoxidize linalool, a model substrate for the presumed linear polyketide intermediate in monensin biosynthesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Base Sequence
  • Cyclization
  • DNA, Bacterial / chemistry
  • DNA, Bacterial / isolation & purification
  • Drug Resistance, Bacterial / genetics
  • Epoxide Hydrolases / genetics
  • Epoxide Hydrolases / metabolism
  • Fatty Acid Synthases / genetics
  • Fatty Acid Synthases / metabolism
  • Gene Deletion
  • Gene Expression Regulation, Bacterial
  • Gene Order
  • Genes, Bacterial
  • Genes, Regulator
  • Methyltransferases / genetics
  • Methyltransferases / metabolism
  • Mixed Function Oxygenases / genetics
  • Mixed Function Oxygenases / metabolism
  • Molecular Sequence Data
  • Monensin / analogs & derivatives*
  • Monensin / biosynthesis*
  • Multienzyme Complexes / genetics
  • Multienzyme Complexes / metabolism
  • Oxidation-Reduction
  • Oxidoreductases / genetics
  • Oxidoreductases / metabolism
  • Steroid Isomerases / genetics
  • Steroid Isomerases / metabolism
  • Streptomyces / enzymology*
  • Streptomyces / genetics*
  • Streptomyces / metabolism
  • Thiolester Hydrolases / genetics
  • Thiolester Hydrolases / metabolism

Substances

  • DNA, Bacterial
  • Multienzyme Complexes
  • monensin B
  • Monensin
  • Mixed Function Oxygenases
  • Oxidoreductases
  • epoxidase
  • Methyltransferases
  • Fatty Acid Synthases
  • Thiolester Hydrolases
  • thioesterase II
  • Epoxide Hydrolases
  • Steroid Isomerases
  • steroid delta-isomerase

Associated data

  • GENBANK/AF440781