Glycolytic Breakdown of Sulfoquinovose in Bacteria: a Missing Link in the Sulfur Cycle

Abstract

Sulfoquinovose (6-deoxy-6-sulfo-D-glucopyranose), formed by the hydrolysis of the plant sulfolipid, is a major component of the biological sulfur cycle. However, pathways for its catabolism are poorly delineated. We examined the hypothesis that mineralization of sulfoquinovose to inorganic sulfate is initiated by reactions of the glycolytic and/or Entner-Doudoroff pathways in bacteria. Metabolites of [U-13 C]sulfoquinovose were identified by 13 C-nuclear magnetic resonance (NMR) in strains of Klebsiella and Agrobacterium previously isolated for their ability to utilize sulfoquinovose as a sole source of carbon and energy for growth, and cell extracts were analyzed for enzymes diagnostic for the respective pathways. Klebsiella sp. strain ABR11 grew rapidly on sulfoquinovose, with major accumulations of sulfopropandiol (2,3-dihydroxypropanesulfonate) but no detectable release of sulfate. Later, when sulfoquinovose was exhausted and growth was very slow, sulfopropandiol disappeared and inorganic sulfate and small amounts of sulfolactate (2-hydroxy-3-sulfopropionate) were formed. In Agrobacterium sp. strain ABR2, growth and sulfoquinovose disappearance were again coincident, though slower than that in Klebsiella sp. Release of sulfate was still late but was faster than that in Klebsiella sp., and no metabolites were detected by 13 C-NMR. Extracts of both strains grown on sulfoquinovose contained phosphofructokinase activities that remained unchanged when fructose 6-phosphate was replaced in the assay mixture with either glucose 6-phosphate or sulfoquinovose. The results were consistent with the operation of the Embden-Meyerhoff-Parnas (glycolysis) pathway for catabolism of sulfoquinovose. Extracts of Klebsiella but not Agrobacterium also contained an NAD ؉ -dependent sulfoquinovose dehydrogenase activity, indicating that the Entner-Doudoroff pathway might also contribute to catabolism of sulfoquinovose.

Dissimilation of the C2 sulfonates

“…Phased appearance of these products could scarcely occur when one enzymic reaction releases both inorganic products simultaneously (Fig. 2b, see subsequent paragraph) and transient excretion of a sulfonate has been observed recently (Roy et al 2003). This hypothesis of transient excretion requires both an exporter and an uptake system for 3-sulfolactate.…”

“…We presume that there are exporters for several organic sulfonates (e.g. Cook and Denger 2005;Roy et al 2003) but clues to their identity are few.…”

“…The generation of, e.g. sulfolactate from sulfoquinovose, involves two sulfonated fructose derivatives and sulfolactaldehyde (Roy et al 2003), so the range of even naturally occurring C 3 -sulfonates in this figure is incomplete acetate is observed; not only the substrate, but also the sulfite from desulfonation (Figs. 3, 4) is dismuted, to sulfide and sulfate (Laue et al 1997a).…”

“…Another widespread source of 3-sulfolactate, presumably L-3-sulfolactate, is bacterial endospores (Bonsen et al 1969;. Most recently, 3-sulfolactate has been detected as a minor excretion product during the bacterial dissimilation of sulfoquinovose, a component of the plant sulfonolipid; larger amounts of 2,3-dihydroxypropanesulfonate are found as a transient intermediate during degradation (Roy et al 2003). Homotaurine (3-aminopropanesulfonate) (Alzhemed TM , Cerebril TM ) is a drug candidate for two major conditions (Alzheimer and stroke).…”

Sulfoacetate generated by Rhodopseudomonas palustris from taurine

“…1) is the major organic solute found in mammals (Huxtable 1992). The plant sulfolipid, which contains a sulfonated derivative of glucose (sulfoquinovose), is a key component of the thylakoid membrane (Benson 1963;Roy et al 2003). Sulfoquinovose can be degraded via sulfoacetate (Martelli and Benson 1964; see also Roy et al 2003), and sulfoacetate has been taken as an indicator of the degradation of the plant sulfolipid (Cook and Denger 2002;Lie et al 1998).…”