A microbial sulfoquinovose monooxygenase pathway that enables sulfosugar assimilation

Abstract

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...

Sulfoglycolysis: catabolic pathways for metabolism of sulfoquinovose

“…5). 28 A. tumefaciens grows on SQ but the only observable carbon metabolite produced in the growth media is bicarbonate, while growth correlates with release of sulfite, suggestive of complete degradation of SQ. Comparative proteomics revealed the upregulated proteins from growth on SQ derive from the gene cluster smoABCDEFGHI (Atu3277-3285).…”

“…SRDI565 shared the putative TauE-type SL exporter with SQ1 but it instead possessed an ABC solute importer cassette involving a putative SQ binding protein, and ABC-type permease components, also identified in the sulfo-SMO pathway. 28 This suggests that the SQ importation machinery can be interchanged between different sulfoglycolytic gene clusters.…”

“…9a). 28 SQGro binds SmoF in a cleft between domains. Binding of SQGro causes a 31° hinge motion of its two domains resulting in complete enclosure of the ligand.…”

“…The genes encoding flavin reductase SmoA and monooxygenase SmoC are present within sulfo-SMO gene clusters in multiple organisms including Agrobacterium sp., Rhizobium oryzae, and Aureimonas flava suggestive that SmoA and SmoC comprise a two-component system that effects the desulfurization and oxidation of SQ. 28 Recombinantly-expressed A.…”

“…5), which produces glucose and sulfite and is the only pathway in a single organism that results in cleavage of the sulfur-carbon bond of SQ to allow complete utilization of all six of its carbons. 28…”