From genetic diversity to metabolic unity: studies on the biosynthesis of aurafurones and aurafuron-like structures in myxobacteria and streptomycetes

J Mol Biol. 2007 Nov 16;374(1):24-38. doi: 10.1016/j.jmb.2007.09.015. Epub 2007 Sep 11.

Abstract

The myxobacterial polyketide secondary metabolites aurafuron A and B were identified by genome mining in the myxobacterial strain Stigmatella aurantiaca DW4/3-1. The compounds contain an unusual furanone moiety and resemble metabolites isolated from soil-dwelling and marine actinobacteria, a fungus and mollusks. We describe here the cloning and functional analysis of the aurafuron biosynthetic gene cluster, including site-directed mutagenesis and feeding studies using labeled precursors. The polyketide core of the aurafurones is assembled by a modular polyketide synthase (PKS). As with many such systems described from myxobacteria, the aurafuron PKS exhibits a number of unusual features, including the apparent iterative use of a module, redundant modules and domains, a trans acting dehydratase and the absence of a terminal thioesterase domain. Four oxidoreductases are encoded within the gene locus, some of which likely participate in formation of the furanone moiety via a Baeyer-Villiger type oxidation. Indeed, inactivation of a gene encoding a cytochrome P(450) monooxygenase completely abolished production of both compounds. We also compare the complete gene locus to biosynthetic gene clusters from two Streptomyces sp., which produce close structural analogues of the aurafurones. A portion of the post-PKS biosynthetic machinery is strikingly similar in all three cases, in contrast to the PKS genes, which are highly divergent. Phylogenetic analysis of the ketosynthase domains further indicates that the PKSs have developed independently (polyphyletically) during evolution. These findings point to a currently unknown but important biological function of aurafuron-like compounds for the producing organisms.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cytochrome P-450 Enzyme Inhibitors
  • Cytochrome P-450 Enzyme System / metabolism
  • Furans / metabolism*
  • Genetic Variation*
  • Molecular Sequence Data
  • Multigene Family
  • Myxococcales / genetics*
  • Myxococcales / growth & development
  • Myxococcales / metabolism
  • Phylogeny
  • Polyketide Synthases / metabolism
  • Streptomyces / genetics*
  • Streptomyces / growth & development
  • Streptomyces / metabolism

Substances

  • Cytochrome P-450 Enzyme Inhibitors
  • Furans
  • aurafuron A
  • aurafuron B
  • Polyketide Synthases
  • Cytochrome P-450 Enzyme System

Associated data

  • GENBANK/AM850130