Isolation, structural elucidation and biosynthesis of 3-hydroxy-6-dimethylallylindolin-2-one, a novel prenylated indole derivative from Actinoplanes missouriensis

J Antibiot (Tokyo). 2014 Mar;67(3):231-6. doi: 10.1038/ja.2013.116. Epub 2013 Nov 13.

Abstract

Many prenylated indole derivatives are widely distributed in nature. Recently, two Streptomyces prenyltransferases, IptA and its homolog SCO7467, were identified in the biosynthetic pathways for 6-dimethylallylindole (DMAI)-3-carbaldehyde and 5-DMAI-3-acetonitrile, respectively. Here, we isolated a novel prenylated indole derivative, 3-hydroxy-6-dimethylallylindolin (DMAIN)-2-one, based on systematic purification of metabolites from a rare actinomycete, Actinoplanes missouriensis NBRC 102363. The structure of 3-hydroxy-6-DMAIN-2-one was determined by HR-MS and NMR analyses. We found that A. missouriensis produced not only 3-hydroxy-6-DMAIN-2-one but also 6-dimethylallyltryptophan (DMAT) and 6-DMAI when grown in PYM (peptone-yeast extract-MgSO4) medium. We searched the complete genome of A. missouriensis for biosynthesis genes of these compounds and found a gene cluster composed of an iptA homolog (AMIS_22580, named iptA-Am) and a putative tryptophanase gene (AMIS_22590, named tnaA-Am). We constructed a tnaA-Am-deleted (ΔtnaA-Am) strain and found that it produced 6-DMAT but did not produce 6-DMAI or 3-hydroxy-6-DMAIN-2-one. Exogenous addition of 6-DMAI to mutant ΔtnaA-Am resulted in the production of 3-hydroxy-6-DMAIN-2-one. Furthermore, in vitro enzyme assays using recombinant proteins produced by Escherichia coli demonstrated that 6-DMAI was synthesized from tryptophan and dimethylallyl pyrophosphate in the presence of both IptA-Am and TnaA-Am, and that IptA-Am preferred tryptophan to indole as the substrate. From these results, we concluded that the iptA-Am-tnaA-Am gene cluster is responsible for the biosynthesis of 3-hydroxy-6-DMAIN-2-one. Presumably, tryptophan is converted into 6-DMAT by IptA-Am and 6-DMAT is then converted into 6-DMAI by TnaA-Am. 6-DMAI appears to be converted into 3-hydroxy-6-DMAIN-2-one by the function of some unknown oxidases in A. missouriensis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Allyl Compounds / chemistry
  • Allyl Compounds / isolation & purification*
  • Allyl Compounds / metabolism
  • Cord Factors / chemistry
  • Cord Factors / isolation & purification*
  • Dimethylallyltranstransferase / metabolism
  • Escherichia coli / metabolism
  • Genome, Bacterial
  • Indoles / chemistry
  • Indoles / isolation & purification*
  • Indoles / metabolism
  • Magnetic Resonance Spectroscopy
  • Mass Spectrometry
  • Micromonosporaceae / genetics
  • Micromonosporaceae / metabolism*
  • Multigene Family
  • Oxidoreductases / metabolism
  • Recombinant Proteins / metabolism
  • Tryptophan / metabolism

Substances

  • 6-deoxy-6-mycoloylamino-alpha,alpha-trehalose
  • Allyl Compounds
  • Cord Factors
  • Indoles
  • Recombinant Proteins
  • Tryptophan
  • Oxidoreductases
  • Dimethylallyltranstransferase