Role of crotonyl coenzyme A reductase in determining the ratio of polyketides monensin A and monensin B produced by Streptomyces cinnamonensis

J Bacteriol. 1999 Nov;181(21):6806-13. doi: 10.1128/JB.181.21.6806-6813.1999.

Abstract

The ccr gene, encoding crotonyl coenzyme A (CoA) reductase (CCR), was cloned from Streptomyces cinnamonensis C730.1 and shown to encode a protein with 90% amino acid sequence identity to the CCRs of Streptomyces collinus and Streptomyces coelicolor. A ccr-disrupted mutant, S. cinnamonensis L1, was constructed by inserting the hyg resistance gene into a unique BglII site within the ccr coding region. By use of the ermE* promoter, the S. collinus ccr gene was expressed from plasmids in S. cinnamonensis C730. 1/pHL18 and L1/pHL18. CCR activity in mutant L1 was shown to decrease by more than 90% in both yeast extract-malt extract (YEME) medium and a complex fermentation medium, compared to that in wild-type C730.1. Compared to C730.1, mutants C730.1/pHL18 and L1/pHL18 exhibited a huge increase in CCR activity (14- and 13-fold, respectively) in YEME medium and a moderate increase (3.7- and 2. 7-fold, respectively) in the complex fermentation medium. In the complex fermentation medium, S. cinnamonensis L1 produced monensins A and B in a ratio of 12:88, dramatically lower than the 50:50 ratio observed for both C730.1 and C730.1/pHL18. Plasmid (pHL18)-based expression of the S. collinus ccr gene in mutant L1 increased the monensin A/monensin B ratio to 42:58. Labeling experiments with [1, 2-(13)C(2)]acetate demonstrated the same levels of intact incorporation of this material into the butyrate-derived portion of monensin A in both C730.1 and mutant C730.1/pLH18 but a markedly decreased level of such incorporation in mutant L1. The addition of crotonic acid at 15 mM led to significant increases in the monensin A/monensin B ratio in C730.1 and C730.1/pHL18 but had no effect in S. cinnamonensis L1. These results demonstrate that CCR plays a significant role in providing butyryl-CoA for monensin A biosynthesis and is present in wild-type S. cinnamonensis C730.1 at a level sufficient that the availability of the appropriate substrate (crotonyl-CoA) is limiting.

Publication types

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

MeSH terms

  • Acetates / metabolism
  • Acyl Coenzyme A / metabolism
  • Acyl-CoA Dehydrogenases
  • Butyrates / metabolism
  • Cloning, Molecular*
  • Crotonates / metabolism
  • Fatty Acids / analysis
  • Gene Deletion
  • Genes, Bacterial*
  • Magnetic Resonance Spectroscopy
  • Molecular Sequence Data
  • Monensin / analogs & derivatives*
  • Monensin / biosynthesis*
  • Oxidoreductases / genetics
  • Oxidoreductases / metabolism*
  • Sequence Analysis, DNA
  • Streptomyces / enzymology*
  • Streptomyces / genetics

Substances

  • Acetates
  • Acyl Coenzyme A
  • Butyrates
  • Crotonates
  • Fatty Acids
  • butyryl-coenzyme A
  • monensin B
  • Monensin
  • Oxidoreductases
  • Acyl-CoA Dehydrogenases
  • acyl-CoA dehydrogenase (NADP+)

Associated data

  • GENBANK/AF178673