Biosynthesis of Anatoxins in Cyanobacteria: Identification of the Carboxy-anatoxins as the Penultimate Biosynthetic Intermediates

J Nat Prod. 2020 Jan 24;83(1):142-151. doi: 10.1021/acs.jnatprod.9b01121. Epub 2020 Jan 3.

Abstract

Anatoxin-a, homoanatoxin-a, and dihydroanatoxin-a are potent cyanobacterial neurotoxins. They are biosynthesized in cyanobacteria from proline and acetate by a pathway involving three polyketide synthases. We report the identification of carboxy-anatoxin-a, carboxy-homoanatoxin-a, and carboxy-dihydroanatoxin-a in acidic extracts of Cuspidothrix issatschenkoi CHARLIE-1, Oscillatoria sp. PCC 6506, and Cylindrospermum stagnale PCC 7417, respectively, using liquid chromatography coupled to mass spectrometry. The structure of these carboxy derivatives was confirmed by mass spectrometry and by isotopic incorporation experiments using labeled proline and acetate. Each of these three cyanobacteria only produce one carboxy-anatoxin, suggesting that these metabolites are the product of the hydrolysis by AnaA, the type II thioesterase, of the thioesters bound to AnaG, the last polyketide synthase of the pathway. By measuring the rate of isotopic incorporation of labeled proline into carboxy-homoanatoxin-a and homoanatoxin-a produced by Oscillatoria sp. PCC 6506, we show that carboxy-homoanatoxin-a is the intracellular precursor of homoanatoxin-a, and that homoanatoxin-a is then excreted into the extracellular medium. The transformation of carboxy-homoanatoxin-a into homoanatoxin-a is a very slow two-step process, with accumulation of carboxy-homoanatoxin-a, suggesting that the decarboxylation is spontaneous and not enzymatically catalyzed. However, an unidentified and extracellular catalyst accelerates the decarboxylation when the cell extracts are prepared at neutral pH.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Toxins / chemistry*
  • Bacterial Toxins / metabolism
  • Bridged Bicyclo Compounds, Heterocyclic / chemistry*
  • Bridged Bicyclo Compounds, Heterocyclic / metabolism
  • Chromatography, Liquid
  • Cyanobacteria / chemistry*
  • Cyanobacteria / metabolism
  • Cyanobacteria Toxins
  • Molecular Structure
  • Oscillatoria / chemistry*
  • Polyketide Synthases / chemistry
  • Polyketide Synthases / metabolism*
  • Proline / chemistry*
  • Tropanes / chemistry
  • Tropanes / metabolism*

Substances

  • Bacterial Toxins
  • Bridged Bicyclo Compounds, Heterocyclic
  • Cyanobacteria Toxins
  • Tropanes
  • homoanatoxin-a
  • Polyketide Synthases
  • anatoxin a
  • Proline

Supplementary concepts

  • Cuspidothrix issatschenkoi
  • Cylindrospermum stagnale