Tandem sulfofucolytic-sulfolactate sulfolyase pathway for catabolism of the rare sulfosugar sulfofucose

Abstract

The rare sulfosugar sulfofucose (6-deoxy-6-sulfo-D-galactose) is catabolized by Paracoccus wurundjeri sp. nov. strain Merri via a novel tandem pathway that couples sulfofucolytic and sulfolactate sulfolyase reactions. We isolated P. wurundjeri from soil and demonstrated its ability to utilize sulfofucose as the sole carbon source, leading to complete degradation of sulfofucose and release of sulfite. Proteomics and metabolomics analysis revealed a sulfofucolytic variant of the Entner–Doudoroff (ED) pathway, wherein sulfofucose is converted to sulfolactaldehyde through oxidation, lactone hydrolysis, dehydration, and retro-aldol steps. The sulfolactaldehyde is subsequently degraded to pyruvate and sulfite via a downstream biomineralization pathway involving sulfolactate as an intermediate. In vitro reconstitution of the key enzymatic steps validated the pathway, identifying four enzymes: SfcH (dehydrogenase), SfcD (lactonase), SfcF (dehydratase), and SfcE (aldolase), that collectively convert sulfofucose to sulfolactaldehyde and pyruvate. Our findings provide insight into microbial utilization of rare sulfosugars and expand the known metabolic versatility of the genus Paracoccus. IMPORTANCE Sulfosugars, such as sulfoquinovose, are integral to the global sulfur cycle, but the metabolism of rarer sulfosugars, like sulfofucose, remains poorly understood. This study identifies a unique bacterial catabolic pathway for sulfofucose degradation, comprising a sulfofucolytic ED pathway, followed by biomineralization to sulfite. The identification of this tandem pathway highlights the metabolic flexibility of bacteria to adapt carbohydrate catabolic pathways for processing structurally similar sulfosugars. This work sheds light on the ecological role of sulfofucose metabolism and broadens our understanding of bacterial sulfur metabolism and biogeochemical sulfur cycling, and offers potential biotechnological applications.