Molecular Basis of Sulfosugar Selectivity in Sulfoglycolysis

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

Petricevic

et al. 2022

Self Cite

Catabolism of sulfoquinovose (SQ; 6-deoxy-6-sulfoglucose), the ubiquitous sulfosugar produced by photosynthetic organisms, is an important component of the biogeochemical carbon and sulfur cycles. Here, we describe a 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 are imported into the cell by an ATP-binding cassette transporter system with an associated SQ binding protein. A sulfoquinovosidase hydrolyzes the SQ glycoside and the liberated SQ is acted on by a flavin mononucleotide-dependent sulfoquinovose monooxygenase, in concert with an NADH-dependent flavin reductase, to release sulfite and 6-oxo-glucose. An NAD(P)H-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 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 because it enables the complete utilization of all carbons within SQ by a single organism with concomitant production of inorganic sulfite.

Section: Discussionmentioning

confidence: 99%

Oxidative desulfurization pathway for complete catabolism of sulfoquinovose by bacteria

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

Petricevic

et al. 2022

Self Cite

“…Through structural analysis we identified key residues involved in sulfosugar recognition and processing, in order to provide greater confidence to bioinformatic analyses of putative smo gene clusters: an approach that has proven valuable for the identification of tier 1 sulfoglycolytic pathways (8,22,23). This includes the Thr220-Gly166-Ser43-H2O(His13-Gln46) cluster of SmoF for the recognition of SQGro, the Arg283-Tryp286-H2O(Tyr491) triad of SmoI for the recognition of SQGro; and the Trp206-Arg236-His238-Tyr341-His343 constellation of SmoC for the recognition of SQ.…”

Section: Discussionmentioning

confidence: 99%

Oxidative desulfurization pathway for complete catabolism of sulfoquinovose by bacteria

Petricevic

et al. 2021

Preprint

Self 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.

“…The structural studies highlight key residues in the sulfosugar processing enzymes that have evolved to bind this distinguishing group: an Arg283-Tryp286-H2O(Tyr491) triad for recognition of the sulfonate in the SQase; a Thr220-Gly166-Ser43-H2O(His13-Gln46) cluster for recognition of the sulfonate in the SQGro binding protein; and a proposed binding pocket of Trp206-Arg236-His238-Tyr341-His343 for recognition of sulfonate in the SQ monooxygenase. Well-defined sulfonate binding pockets have been highlighted for the enzymes of the sulfo-EMP pathway 8,21,22 and are useful sequence signatures for bioinformatic studies and assignment of the pathways in unstudied organisms.…”

Section: Discussionmentioning

confidence: 99%

A microbial sulfoquinovose monooxygenase pathway that enables sulfosugar assimilation

Williams

et al. 2021

Preprint

Self 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...