Genetic characterization of enzymes involved in the priming steps of oxytetracycline biosynthesis in Streptomyces rimosus

Microbiology (Reading). 2011 Aug;157(Pt 8):2401-2409. doi: 10.1099/mic.0.048439-0. Epub 2011 May 26.

Abstract

Tetracyclines are clinically important aromatic polyketides whose biosynthesis is catalysed by bacterial type II polyketide synthases (PKSs). Tetracyclines are biosynthesized starting with an amide-containing malonamate starter unit and the resulting C-2 carboxyamide is critical for the antibiotic activities. In this work, we genetically verified that an amidotransferase, OxyD, and a thiolase, OxyP, are involved in the biosynthesis and incorporation of the starter unit. First, two mutations, R248T and D268N, were found to be present in OxyD* encoded in Streptomyces rimosus ATCC 13224, a strain that produces the acetate-primed 2-acetyl-2-decarboxyamido-oxytetracycline (ADOTC) instead of the malonamate-primed oxytetracycline (OTC). Homology modelling suggested that in particular D268N may inactivate OxyD. Complementation of S. rimosus ATCC 13224 with wild-type OxyD restored OTC biosynthesis, thereby confirming the essential role of OxyD in the synthesis of the amide starter unit. Second, using a series of knockout and complementation approaches, we demonstrated that OxyP is most likely involved in maintaining fidelity of the amide-priming process via hydrolysis of the competing acetate priming starter units. While the inactivation of OxyP does not eliminate OTC biosynthesis, the ratio of acetate-primed ADOTC to malonamate-primed OTC is significantly increased. This suggests that OxyP plays an ancillary role in OTC biosynthesis and is important for minimizing the levels of ADOTC, a shunt product that has much weaker antibiotic activities than OTC.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Anti-Bacterial Agents / biosynthesis*
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Biosynthetic Pathways*
  • Enzymes / chemistry
  • Enzymes / genetics
  • Gene Knockout Techniques
  • Genetic Complementation Test
  • Models, Biological
  • Models, Molecular
  • Mutation, Missense
  • Oxytetracycline / biosynthesis*
  • Streptomyces / genetics*
  • Streptomyces / metabolism*

Substances

  • Anti-Bacterial Agents
  • Bacterial Proteins
  • Enzymes
  • Oxytetracycline