Architecture, Function, Regulation, and Evolution of α-Glucans Metabolic Enzymes in Prokaryotes

Bacteria have acquired sophisticated mechanisms for assembling and disassembling polysaccharides of different chemistry. alpha-D-Glucose homopolysaccharides, so-called alpha-glucans, are the most widespread polymers in nature being key components of microorganisms. Glycogen functions as an intracellular energy storage while some bacteria also produce extracellular assorted alpha-glucans. The classical bacterial glycogen metabolic pathway comprises the action of ADP-glucose pyrophosphorylase and glycogen synthase, whereas extracellular alpha-glucans are mostly related to peripheral enzymes dependent on sucrose. An alternative pathway of glycogen biosynthesis, operating via a maltose 1-phosphate polymerizing enzyme, displays an essential wiring with the trehalose metabolism to interconvert disaccharides into polysaccharides. Furthermore, some bacteria show a connection of intracellular glycogen metabolism with the genesis of extracellular capsular alpha-glucans, revealing a relationship between the storage and structural function of these compounds. Altogether, the current picture shows that bacteria have evolved an intricate alpha-glucan metabolism that ultimately relies on the evolution of a specific enzymatic machinery. The structural landscape of these enzymes exposes a limited number of core catalytic folds handling many different chemical reactions. In this Review, we present a rationale to explain how the chemical diversity of alpha-glucans emerged from these systems, highlighting the underlying structural evolution of the enzymes driving alpha-glucan bacterial metabolism.