In vitro reconstitution of the myxochelin biosynthetic machinery of Stigmatella aurantiaca Sg a15: Biochemical characterization of a reductive release mechanism from nonribosomal peptide synthetases

Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11136-41. doi: 10.1073/pnas.201167098. Epub 2001 Sep 18.

Abstract

Microorganisms produce iron-chelating compounds to sequester the iron essential for growth from the environment. Many of these compounds are biosynthesized by nonribosomal peptide synthetases, some in cooperation with polyketide synthases. Myxochelins are produced by the myxobacterium Stigmatella aurantiaca Sg a15, and the corresponding gene cluster was cloned recently. We have undertaken to express heterologously the myxochelin biosynthetic machinery in Escherichia coli. To activate the involved proteins posttranslationally, they were coexpressed with the phosphopantetheinyltransferase MtaA from the myxothiazol biosynthetic gene cluster. Phosphopantetheinylation of the carrier proteins could be verified by protein mass analysis. Six active domains in proteins MxcE, MxcF, and MxcG are capable of assembling myxochelin from ATP, NAD(P)H, lysine, and 2,3-dihydroxybenzoic acid in vitro. This fact demonstrates that the condensation domain of MxcG performs two condensation reactions, creating the aryl-capped alpha-amide and the aryl-capped gamma-amide of the molecule. A previously unknown type of reductive release is performed by the reduction domain of MxcG, which alternatively uses NADPH and NADH to set free the peptidyl-carrier protein-bound thioester as an aldehyde and further reduces it to the alcohol structure that can be found in myxochelin A. This type of reductive release seems to be a general mechanism in polyketide and nonribosomal peptide biosynthesis, because several systems with C-terminal similarity to the reductase domain of MxcG can be found in the databases. Alternatively, the aldehyde can be transaminated, giving rise to a terminal amine.

MeSH terms

  • Amino Acid Sequence
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Catechols
  • Cloning, Molecular
  • DNA-Binding Proteins / chemistry
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Escherichia coli
  • Hydrolases / chemistry
  • Hydrolases / genetics
  • Lysine / analogs & derivatives*
  • Lysine / biosynthesis*
  • Molecular Sequence Data
  • Molecular Structure
  • Multigene Family
  • Nucleotidyltransferases / chemistry
  • Nucleotidyltransferases / genetics
  • Oxidation-Reduction
  • Peptide Synthases / genetics*
  • Peptide Synthases / metabolism*
  • Protein Processing, Post-Translational
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Stigmatella aurantiaca / enzymology
  • Stigmatella aurantiaca / genetics
  • Stigmatella aurantiaca / metabolism*

Substances

  • Bacterial Proteins
  • Catechols
  • DNA-Binding Proteins
  • MxcE protein, Methylobacterium organophilum
  • Recombinant Proteins
  • myxochelin B
  • myxochelin A
  • MxcG protein, Stigmatella aurantiaca
  • Nucleotidyltransferases
  • Hydrolases
  • MxcF protein, Stigmatella aurantiaca
  • Peptide Synthases
  • Lysine