Abstract
Eukaryotes most often synthesize storage polysaccharides in the cytosol or vacuoles in the form of either alpha (glycogen/starch)- or beta-glucosidic (chrysolaminarins and paramylon) linked glucan polymers. In both cases, the glucose can be packed either in water-soluble (glycogen and chrysolaminarins) or solid crystalline (starch and paramylon) forms with different impacts, respectively, on the osmotic pressure, the glucose accessibility, and the amounts stored. Glycogen or starch accumulation appears universal in all free-living unikonts (metazoa, fungi, amoebozoa, etc.), as well as Archaeplastida and alveolata, while other lineages offer a more complex picture featuring both alpha- and beta-glucan accumulators. We now infer the distribution of these polymers in stramenopiles through the bioinformatic detection of their suspected metabolic pathways. Detailed phylogenetic analysis of key enzymes of these pathways correlated to the phylogeny of Stramenopila enables us to retrace the evolution of storage polysaccharide metabolism in this diverse group of organisms. The possible ancestral nature of glycogen metabolism in eukaryotes and the underlying source of its replacement by beta-glucans are discussed.
Highlights
Storage polysaccharides are central components of the cell, used to store energy and carbon in an osmotically inert form
In Stramenopila, only two enzymes are known to be clearly involved in Chrysolaminarin biosynthesis, GT48 and GH16_2, and among these two, only GT48 was functionally fully demonstrated to be involved
By looking at the sequence distributions in Stramenopila using the CAZy database as basic knowledge to determine candidates involved in beta-glucan metabolism and the freely available HMM profile from the automated Carbohydrate-active enzyme annotation to further assign the sequences detected to their corresponding enzyme subfamilies, we were able to propose the possible involvement of both the GH81 and GH5_33 enzymes
Summary
Storage polysaccharides are central components of the cell, used to store energy and carbon in an osmotically inert form They can be found under diverse forms including mannans and glucans; by far the two most widespread kinds consist of glucose polymers (glucans) linked by either beta (subsequently called beta-glucan polysaccharides)- or alpha (subsequently called alpha-glucan polysaccharides)-glucosidic bonds. Storage polysaccharides can be found under either water-soluble polymers (e.g., glycogen and chrysolaminarins) or insoluble solid crystalline material (e.g., starch and paramylon) This difference in physical state of these polymers directly impacts both glucose accessibility (which is slow with solid crystalline granules) and stored amounts (which appear generally higher for crystalline material) as well as the osmotic activity of the cellular compartments concerned by their accumulation (cytosol, vacuoles, and plastid). The glucose is in all cases first activated in the form of a nucleotide sugar (UDP-glucose or ADP-glucose), which is transferred to a growing chain through glycosyl transferases (GT) behaving as glucan synthases
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