Polyketide synthase chemistry does not direct biosynthetic divergence between 9- and 10-membered enediynes

Proc Natl Acad Sci U S A. 2010 Jun 22;107(25):11331-5. doi: 10.1073/pnas.1003442107. Epub 2010 Jun 7.

Abstract

Enediynes are potent antitumor antibiotics that are classified as 9- or 10-membered according to the size of the enediyne core structure. However, almost nothing is known about enediyne core biosynthesis, and the determinants of 9- versus 10-membered enediyne core biosynthetic divergence remain elusive. Previous work identified enediyne-specific polyketide synthases (PKSEs) that can be phylogenetically distinguished as being involved in 9- versus 10-membered enediyne biosynthesis, suggesting that biosynthetic divergence might originate from differing PKSE chemistries. Recent in vitro studies have identified several compounds produced by the PKSE and associated thioesterase (TE), but condition-dependent product profiles make it difficult to ascertain a true catalytic difference between 9- and 10-membered PKSE-TE systems. Here we report that PKSE chemistry does not direct 9- versus 10-membered enediyne core biosynthetic divergence as revealed by comparing the products from three 9-membered and two 10-membered PKSE-TE systems under identical conditions using robust in vivo assays. Three independent experiments support a common catalytic function for 9- and 10-membered PKSEs by the production of a heptaene metabolite from: (i) all five cognate PKSE-TE pairs in Escherichia coli; (ii) the C-1027 and calicheamicin cognate PKSE-TEs in Streptomyces lividans K4-114; and (iii) selected native producers of both 9- and 10-membered enediynes. Furthermore, PKSEs and TEs from different 9- and 10-membered enediyne biosynthetic machineries are freely interchangeable, revealing that 9- versus 10-membered enediyne core biosynthetic divergence occurs beyond the PKSE-TE level. These findings establish a starting point for determining the origins of this biosynthetic divergence.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aminoglycosides / chemistry
  • Aminoglycosides / pharmacology
  • Biochemistry / methods
  • Chromatography, High Pressure Liquid
  • Enediynes / chemistry*
  • Enediynes / pharmacology
  • Escherichia coli / enzymology
  • Escherichia coli Proteins / chemistry
  • Gene Expression Regulation, Bacterial
  • Lysophospholipase / chemistry
  • Models, Chemical
  • Models, Genetic
  • Multigene Family
  • Periplasmic Proteins / chemistry
  • Polyketide Synthases / chemistry*
  • Sequence Analysis, DNA
  • Streptomyces lividans / enzymology
  • Ultraviolet Rays

Substances

  • Aminoglycosides
  • Enediynes
  • Escherichia coli Proteins
  • Periplasmic Proteins
  • C 1027
  • Polyketide Synthases
  • Lysophospholipase
  • tesA protein, E coli