Microbial degradation of the plant sulpholipid

Roy, A.B.; Ellis, Andrew J.; White, Graham F.; Harwood, John L.

doi:10.1042/bst0280781

Cited by 11 publications

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“…A metabolite with an identical NMR spectrum was also observed (unpublished results) as the major accumulating product during degradation of [U- 13 C]sulfoquinovose by Pseudomonas sp. strain ABR1 isolated from forest leaf mould (33). When this metabolite was recovered from the growth medium and subsequently incorporated (approximately 10 mM) in fresh basal salts medium inoculated with Klebsiella sp.…”

Section: Resultsmentioning

confidence: 99%

“…Bacteria were isolated from forest leaf mould and activated sewage sludge by enrichment culture (five rounds), as reported previously (33) O (15). Axenic strains were isolated and maintained on nutrient agar.…”

Section: Methodsmentioning

confidence: 99%

“…In addition, the Entner-Doudoroff (14) pathway operating via 6-phosphogluconate may serve as a bypass for reactions of the upper glycolytic pathway (13). In a preliminary communication (33) we reported the isolation of five bacterial strains (four from forest leaf mould and one from activated sewage sludge) that grew on sulfoquinovose as a sole source of carbon. Two of these strains achieved mineralization of sulfoquinovose to inorganic sulfate.…”

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

Roy¹,

Hewlins

Ellis³

et al. 2003

Appl Environ Microbiol

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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.

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confidence: 99%

Section: Methodsmentioning

confidence: 99%

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

Roy¹,

Hewlins

Ellis³

et al. 2003

Appl Environ Microbiol

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“…SQ is continuously degraded in all environments where SQ is produced, or it would enrich in these environments. The complete degradation of SQ to, ultimately, CO 2 , concomitant with a recycling of the bound sulfur in the form of inorganic sulfate, is dominated by microbes (e.g., by soil bacteria) (2,(5)(6)(7)(8)(9). However, a more detailed exploration of SQ-degrading microbes, of their SQ-degradation pathways, and of the enzymes and genes involved has only recently been initiated (10)(11)(12).…”

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“…Several Pseudomonas strains that can use SQ for growth have been isolated from soil (8,9), and the excretion of another C 3 -organosulfonate, SL, instead of DHPS or sulfate, has been reported (9, 10). We also isolated an SQ-utilizing member of the genus Pseudomonas, Pseudomonas putida strain SQ1, from a freshwater sediment (Lake Constance, Germany).…”

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Entner–Doudoroff pathway for sulfoquinovose degradation in Pseudomonas putida SQ1

Felux

Spiteller

Klebensberger

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

126

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Sulfoquinovose (SQ; 6-deoxy-6-sulfoglucose) is the polar head group of the plant sulfolipid SQ-diacylglycerol, and SQ comprises a major proportion of the organosulfur in nature, where it is degraded by bacteria. A first degradation pathway for SQ has been demonstrated recently, a "sulfoglycolytic" pathway, in addition to the classical glycolytic (Embden-Meyerhof) pathway in Escherichia coli K-12; half of the carbon of SQ is abstracted as dihydroxyacetonephosphate (DHAP) and used for growth, whereas a C 3 -organosulfonate, 2,3-dihydroxypropane sulfonate (DHPS), is excreted. The environmental isolate Pseudomonas putida SQ1 is also able to use SQ for growth, and excretes a different C 3 -organosulfonate, 3-sulfolactate (SL). In this study, we revealed the catabolic pathway for SQ in P. putida SQ1 through differential proteomics and transcriptional analyses, by in vitro reconstitution of the complete pathway by five heterologously produced enzymes, and by identification of all four organosulfonate intermediates. The pathway follows a reaction sequence analogous to the Entner-Doudoroff pathway for glucose-6-phosphate: It involves an NAD + -dependent SQ dehydrogenase, 6-deoxy-6-sulfogluconolactone (SGL) lactonase, 6-deoxy-6-sulfogluconate (SG) dehydratase, and 2-keto-3,6-dideoxy-6-sulfogluconate (KDSG) aldolase. The aldolase reaction yields pyruvate, which supports growth of P. putida, and 3-sulfolactaldehyde (SLA), which is oxidized to SL by an NAD(P) + -dependent SLA dehydrogenase. All five enzymes are encoded in a single gene cluster that includes, for example, genes for transport and regulation. Homologous gene clusters were found in genomes of other P. putida strains, in other gamma-Proteobacteria, and in beta-and alpha-Proteobacteria, for example, in genomes of Enterobacteria, Vibrio, and Halomonas species, and in typical soil bacteria, such as Burkholderia, Herbaspirillum, and Rhizobium.bacterial biodegradation | organosulfonate | sulfolipid | 6-deoxy-6-sulfoglucose | sulfur cycle S ulfoquinovose (SQ; 6-deoxy-6-sulfoglucose) is the polar head group of the plant sulfolipids sulfoquinovosyl diacylglycerols (SQDGs), which were discovered more than 60 y ago (1). The sulfolipids are located in the photosynthetic (thylakoid) membranes of all higher plants, mosses, ferns, and algae, as well as in most photosynthetic bacteria. They are also present in some nonphotosynthetic bacteria, and SQ is in the surface layer of some archaea (2-4). SQ is continuously degraded in all environments where SQ is produced, or it would enrich in these environments. The complete degradation of SQ to, ultimately, CO 2 , concomitant with a recycling of the bound sulfur in the form of inorganic sulfate, is dominated by microbes (e.g., by soil bacteria) (2, 5-9). However, a more detailed exploration of SQ-degrading microbes, of their SQ-degradation pathways, and of the enzymes and genes involved has only recently been initiated (10-12). The common view on SQ degradation is based on the consideration that SQ is a structural analog of glucose-6...

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Sulphoquinovosyl Diacylglycerol (SQDG) — The Sulpholipid of Higher Plants

Harwood

Okanenko

2003

Sulphur in Plants

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Microbial degradation of the plant sulpholipid

Abstract: Five bacterial strains capable of using sulphoquinovose (6-deoxy-6-sulpho-D-glucopyranose) as a sole source of carbon have been isolated and partially characterized.

Cited by 11 publications

References 0 publications

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

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

Entner–Doudoroff pathway for sulfoquinovose degradation in Pseudomonas putida SQ1

Sulphoquinovosyl Diacylglycerol (SQDG) — The Sulpholipid of Higher Plants

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