A transaldolase-dependent sulfoglycolysis pathway in Bacillus megaterium DSM 1804

Liu, Yinbo; Wei, Yifeng; Zhou, Yan; Ang, Ee Lui; Zhao, Huimin; Zhang, Yan

doi:10.1016/j.bbrc.2020.09.124

Cited by 31 publications

(43 citation statements)

References 22 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Some Proteobacteria can catabolize SQDG/SQG and SQ analogously to the Embden–Meyerhof–Parnas (EMP) and the Entner–Doudoroff (ED) glycolytic pathways, hence, either via the sulfo-EMP (e.g., commensal and pathogenic Escherichia coli ) or the sulfo-ED pathway (e.g., Pseudomonas putida ) [ 12 – 14 ]. Recently, a third pathway for SQ degradation via a novel 6-deoxy-6-sulfofructose transaldolase (SFT) was described in the aerobic Bacillus aryabhattai isolate SOS1 [ 15 ] and Bacillus megaterium DSM 1804 [ 16 ]. The intestinal strains of the Firmicutes species Enterococcus gilvus , Clostridium symbiosum , and Eubacterium rectale also expressed SFT pathway genes during anaerobic, fermentative growth with SQ [ 15 ].…”

Section: Introductionmentioning

confidence: 99%

Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut

et al. 2021

View full text Add to dashboard Cite

Responses of the microbiota to diet are highly personalized but mechanistically not well understood because many metabolic capabilities and interactions of human gut microorganisms are unknown. Here we show that sulfoquinovose (SQ), a sulfonated monosaccharide omnipresent in green vegetables, is a selective yet relevant substrate for few but ubiquitous bacteria in the human gut. In human feces and in defined co-culture, Eubacterium rectale and Bilophila wadsworthia used recently identified pathways to cooperatively catabolize SQ with 2,3-dihydroxypropane-1-sulfonate as a transient intermediate to hydrogen sulfide (H2S), a key intestinal metabolite with disparate effects on host health. SQ-degradation capability is encoded in almost half of E. rectale genomes but otherwise sparsely distributed among microbial species in the human intestine. However, re-analysis of fecal metatranscriptome datasets of four human cohorts showed that SQ degradation (mostly from E. rectale and Faecalibacterium prausnitzii) and H2S production (mostly from B. wadsworthia) pathways were expressed abundantly across various health states, demonstrating that these microbial functions are core attributes of the human gut. The discovery of green-diet-derived SQ as an exclusive microbial nutrient and an additional source of H2S in the human gut highlights the role of individual dietary compounds and organosulfur metabolism on microbial activity and has implications for precision editing of the gut microbiota by dietary and prebiotic interventions.

show abstract

Section: Introductionmentioning

confidence: 99%

Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut

et al. 2021

View full text Add to dashboard Cite

show abstract

“…To date, three tier 1 pathways have been described: the sulfoglycolytic Embden-Meyerhof-Parnas (sulfo-EMP) (3), Entner-Doudoroff (sulfo-ED) (4,5) and sulfofructose transaldolase (sulfo-SFT) pathways (6,7). Tier 2 metabolism has been described for various specialized bacteria that utilize SL or DHPS and perform 'biomineralization' to release inorganic sulfite, which under aerobic conditions is readily oxidized to sulfate (1).…”

Section: Introductionmentioning

confidence: 99%

Oxidative desulfurization pathway for complete catabolism of sulfoquinovose by bacteria

Sharma

Lingford

Petricevic

et al. 2021

Preprint

View full text Add to dashboard Cite

Catabolism of sulfoquinovose (SQ,, the ubiquitous sulfosugar produced by photosynthetic organisms, is an important component of the biogeochemical carbon and sulfur cycles.Here, we describe a new pathway for SQ degradation that involves oxidative desulfurization to release sulfite and enable utilization of the entire carbon skeleton of the sugar to support the growth of the plant pathogen Agrobacterium tumefaciens. SQ or its glycoside sulfoquinovosyl glycerol (SQGro) are imported into the cell by an ABC transporter system with an associated SQ binding protein. A sulfoquinovosidase hydrolyses the SQ glycoside and the liberated SQ is acted on by a flavin mononucleotide-dependent sulfoquinovose monooxygenase, in concert with an NADHdependent flavin reductase, to release sulfite and 6-oxo-glucose. An NADPH-dependent oxidoreductase reduces the 6-oxo-glucose to glucose, enabling entry into primary metabolic pathways. Structural and biochemical studies provide detailed insights into the recognition of key metabolites by proteins in this pathway. Bioinformatic analyses reveal that the sulfoquinovose monooxygenase (smo) pathway is distributed across Alpha-and Betaproteobacteria and is especially prevalent within the Rhizobiales order. This strategy for SQ catabolism is distinct from previously described pathways as it enables the complete utilization of all carbons within SQ by a single organism with concomitant production of inorganic sulfite. Significance StatementSulfoquinovose, a sulfosugar derivative of glucose, is produced by most photosynthetic organisms and contains up to half of all sulfur in the biosphere. Several pathways for its breakdown are known, though they provide access to only half of the carbon in sulfoquinovose and none of its sulfur. Here, we describe a fundamentally different pathway within the plant pathogen Agrobacterium tumefaciens that features oxidative desulfurization of sulfoquinovose to access all carbon and sulfur within the molecule. Biochemical and structural analyses of the pathway's key proteins provided insights how the sulfosugar is recognized and degraded. Genes encoding this sulfoquinovose monooxygenase pathway are present in many plant pathogens and symbionts, alluding to a possible role for sulfoquinovose in plant host-bacteria interactions.

show abstract

“…In the second tier SL-and DHPS-utilizing bacteria release inorganic sulfur as sulfite. Three Tier 1 pathways have been described, the sulfoglycolytic Embden-Meyerhof-Parnas (sulfo-EMP) 3 , Entner-Doudoroff (sulfo-ED) 4,5 and sulfofructose transaldolase (sulfo-SFT) pathways 6,7 . Tier 2 metabolism has been described for various specialized bacteria that utilize SL or DHPS and perform 'biomineralization', releasing sulfur as sulfite, which under aerobic conditions can readily oxidize to sulfate 1 .…”

Section: Introductionmentioning

confidence: 99%

A microbial sulfoquinovose monooxygenase pathway that enables sulfosugar assimilation

Williams

Sharma

Lingford

et al. 2021

Preprint

View full text Add to dashboard Cite

Breakdown of the sulfosugar sulfoquinovose (SQ, 6-deoxy-6-sulfoglucose), produced by photosynthetic organisms, is an important component of the biogeochemical carbon and sulfur cycles. Here, we reveal a new pathway for SQ degradation involving oxidative desulfurization to release sulfite and complete breakdown of the carbon skeleton of this sugar to support the growth of the plant pathogen Agrobacterium tumefaciens. SQ or its glycoside sulfoquinovosyl glycerol are imported by an ABC transporter system with associated SQ binding protein. A sulfoquinovosidase cleaves the SQ glycoside and a flavin mononucleotide-dependent sulfoquinovose monooxygenase acts in concert with an NADH-dependent flavin reductase to release sulfite and form 6-oxo-glucose. A short-chain dehydrogenase/reductase oxidoreductase reduces 6-oxo-glucose to glucose, allowing it to enter primary metabolism. Structural and biochemical studies provide detailed insights into the binding and recognition of key species along the reaction coordinate. This sulfoquinovose monooxygenase pathway is distributed across alphaproteobacteria and especially within the rhizobiales. This metabolic strategy...

show abstract

A transaldolase-dependent sulfoglycolysis pathway in Bacillus megaterium DSM 1804

Cited by 31 publications

References 22 publications

Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut

Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut

Oxidative desulfurization pathway for complete catabolism of sulfoquinovose by bacteria

A microbial sulfoquinovose monooxygenase pathway that enables sulfosugar assimilation

Contact Info

Product

Resources

About