PcxL and HpxL are flavin-dependent, oxime-forming N-oxidases in phosphonocystoximic acid biosynthesis in Streptomyces

J Biol Chem. 2018 May 4;293(18):6859-6868. doi: 10.1074/jbc.RA118.001721. Epub 2018 Mar 14.

Abstract

Several oxime-containing small molecules have useful properties, including antimicrobial, insecticidal, anticancer, and immunosuppressive activities. Phosphonocystoximate and its hydroxylated congener, hydroxyphosphonocystoximate, are recently discovered oxime-containing natural products produced by Streptomyces sp. NRRL S-481 and Streptomyces regensis NRRL WC-3744, respectively. The biosynthetic pathways for these two compounds are proposed to diverge at an early step in which 2-aminoethylphosphonate (2AEPn) is converted to (S)-1-hydroxy-2-aminoethylphosphonate ((S)-1H2AEPn) in S. regensis but not in Streptomyces sp. NRRL S-481). Subsequent installation of the oxime moiety into either 2AEPn or (S)-1H2AEPn is predicted to be catalyzed by PcxL or HpxL from Streptomyces sp. NRRL S-481 and S. regensis NRRL WC-3744, respectively, whose sequence and predicted structural characteristics suggest they are unusual N-oxidases. Here, we show that recombinant PcxL and HpxL catalyze the FAD- and NADPH-dependent oxidation of 2AEPn and 1H2AEPn, producing a mixture of the respective aldoximes and nitrosylated phosphonic acid products. Measurements of catalytic efficiency indicated that PcxL has almost an equal preference for 2AEPn and (R)-1H2AEPn. 2AEPn was turned over at a 10-fold higher rate than (R)-1H2AEPn under saturating conditions, resulting in a similar but slightly lower kcat/Km We observed that (S)-1H2AEPn is a relatively poor substrate for PcxL but is clearly the preferred substrate for HpxL, consistent with the proposed biosynthetic pathway in S. regensis. HpxL also used both 2AEPn and (R)-1H2AEPn, with the latter inhibiting HpxL at high concentrations. Bioinformatic analysis indicated that PcxL and HpxL are members of a new class of oxime-forming N-oxidases that are broadly dispersed among bacteria.

Keywords: enzyme kinetics; flavin adenine dinucleotide (FAD); natural product biosynthesis; nicotinamide; oxidase; oxime; phosphonates; phosphonic acid; substrate specificity.

Publication types

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

MeSH terms

  • Amines / metabolism
  • Bacterial Proteins / metabolism*
  • Catalysis
  • Dinitrocresols / metabolism*
  • Flavin-Adenine Dinucleotide / metabolism
  • Kinetics
  • NADP / metabolism
  • Oxidation-Reduction
  • Oxidoreductases / metabolism*
  • Oximes / metabolism*
  • Phosphinic Acids / metabolism
  • Streptomyces / enzymology*
  • Substrate Specificity

Substances

  • Amines
  • Bacterial Proteins
  • Dinitrocresols
  • Oximes
  • Phosphinic Acids
  • Flavin-Adenine Dinucleotide
  • 4,6-dinitro-o-cresol
  • NADP
  • Oxidoreductases

Associated data

  • PDB/3S5W
  • PDB/4TLX