A widespread family of oxidoreductive sulfoquinovosidases at the gateway to sulfoquinovose catabolism

The sulfosugar sulfoquinovose (SQ) is produced by photosynthetic plants, algae and cyanobacteria on a scale of 10 billion tonnes per annum. Its degradation, which is essential to allow cycling of its constituent carbon and sulfur, involves specialized glycosidases termed sulfoquinovosidases (SQases), which release SQ from sulfolipid glycoconjugates so it can enter SQ catabolism pathways. However, many SQ catabolic gene clusters lack a gene encoding a classical SQase. Here, we report the discovery of a new family of SQases that use an atypical oxidoreductive mechanism involving NAD+ as a catalytic cofactor. 3D X-ray structures of complexes with SQ and NAD+ provide insight into the catalytic mechanism, which involves transient oxidation at C3. Bioinformatic survey reveals this new family of NAD-dependent SQases occur within sulfoglycolytic and sulfolytic gene clusters that lack classical SQases, and are distributed widely including within Roseobacter clade bacteria, suggesting an important contribution to marine sulfur cycling.