Chain initiation in the leinamycin-producing hybrid nonribosomal peptide/polyketide synthetase from Streptomyces atroolivaceus S-140. Discrete, monofunctional adenylation enzyme and peptidyl carrier protein that directly load D-alanine

J Biol Chem. 2007 Jul 13;282(28):20273-82. doi: 10.1074/jbc.M702814200. Epub 2007 May 14.

Abstract

Nonribosomal peptide natural products are biosynthesized from amino acid precursors by nonribosomal peptide synthetases (NRPSs), which are organized into modules. For a typical NRPS initiation module, an adenylation (A) domain activates an amino acid and installs it onto a peptidyl carrier protein (PCP) domain as a thioester; an elongation module, which has a condensation (C) domain located between every consecutive pair of A and PCP domains, catalyzes the formation of the peptide bond between the upstream aminoacyl/peptidyl-S-PCP and the free amino group of the downstream aminoacyl-S-PCP. D-amino acid constituents in peptide natural products usually arise from the L-enantiomers through the action of integral epimerization (E) domains of an NRPS. The biosynthetic gene cluster for leinamycin, a hybrid nonribosomal peptide/polyketide containing a D-alanine moiety, does not encode a typical NRPS initiation module with the expected A-PCP-E domains; instead, it has only an A protein (LnmQ) and a PCP (LnmP), both of which are encoded by separate genes. Here we show the results of biochemical experiments as follows: (i) we demonstrate that LnmQ directly activates D-alanine as D-alaninyl-AMP and installs it onto LnmP to generate a D-alaninyl-S-PCP intermediate; (ii) we confirm that aminoacylation of LnmP by LnmQ in trans is the result of specific communication between the separate A and PCP proteins; and (iii) we reveal that leinamycin production can be improved by supplementation of exogenous D-alanine in the fermentation broth of Streptomyces atroolivaceous S-140. These findings unveil an unprecedented NRPS initiation module structure that is characterized by a discrete D-alanine-specific A protein and a PCP.

Publication types

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

MeSH terms

  • Alanine / genetics
  • Alanine / metabolism
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Genes, Bacterial / physiology
  • Lactams / metabolism*
  • Macrolides / metabolism*
  • Multigene Family / physiology
  • Peptide Biosynthesis, Nucleic Acid-Independent / physiology*
  • Peptide Synthases / genetics
  • Peptide Synthases / metabolism*
  • Polyketide Synthases / genetics
  • Polyketide Synthases / metabolism*
  • Protein Structure, Tertiary / physiology
  • Streptomyces / enzymology*
  • Streptomyces / genetics
  • Thiazoles / metabolism*
  • Thiones / metabolism*

Substances

  • Bacterial Proteins
  • Carrier Proteins
  • Lactams
  • Macrolides
  • Thiazoles
  • Thiones
  • leinamycin
  • Polyketide Synthases
  • Peptide Synthases
  • Alanine