The complete {lambda}-carrageenan depolymerization cascade from a marine Pseudoalteromonad revealed by structural analysis of the enzymes.

Abstract

Carrageenans are a complex group of polysaccharides derived from the cell walls of red macroalgae. They are an abundant, yet recalcitrant nutrient source for most marine heterotrophic bacteria. Some member species of the Pseudoalteromonas genus are effective at metabolizing carrageenan. However, the enzymatic pathway for {lambda}-carrageenan, one of the most sulfated naturally occurring polysaccharides, remains unknown. Using detailed structural analysis by X-ray crystallography we reveal the sophisticated and cyclic enzymatic cascade deployed by Pseudoalteromonas distincta (strain U2A) to utilize {lambda}-carrageenan. The cascade incorporates ten glycoside hydrolases and five sulfatases that are specific for {lambda}-carrageenan and cooperate to completely deconstruct this polysaccharide, thus yielding galactose monosaccharides for subsequent energy production. The detailed molecular understanding of {lambda}-carrageenan depolymerisation provided includes structural evidence for a lesser described sulfatase catalytic mechanism and elucidation of a distinct catabolic cascade that is unique from previously described carrageenan metabolic pathways. This insight also holds potential for the application of enzymatic logic in the generation of high value products from abundant natural biopolymers, such as carrageenans.