The Transition from Glycogen to Starch Metabolism in Cyanobacteria and Eukaryotes

Abstract

'-1,4-linked glucan chains branched through '-1,6 glucosidic lineages define the most frequently found storage polysaccharides in living cells. These glucans come in two very distinct forms known as glycogen and starch. The small water-soluble glycogen particles distribute widely in Archaea, Bacteria, and heterotrophic eukaryotes, while semicrystalline solid starch seems to be restricted to photosynthetic eukaryotes. This review focusses on the so-called glycosylnucleotide-dependent pathway of starch and glycogen synthesis. Through comparative biochemistry of storage polysaccharide metabolism in distinct clades, we will review the evidence sustaining that starch has evolved from preexisting glycogen metabolism several times during the evolution of photosynthetic eukaryotes and cyanobacteria. This review will also describe the possible function of storage polysaccharide metabolism in establishing metabolic symbiosis during plastid endosymbiosis. We will detail the evidence sustaining that storage polysaccharide metabolism was used by three distinct organisms to establish a tripartite symbiosis that facilitated metabolic integration of free-living cyanobacteria into evolving organelles.

Altering the Structure of Carbohydrate Storage Granules in the Cyanobacterium Synechocystis sp. Strain PCC 6803 through Branching-Enzyme Truncations

“…For example, there are 4 potential amylase enzymes in Cyanothece sp. ATCC 51142 (35). What role do they play, if any, in semi-amylopectin formation in this strain?…”

“…Compared to many eubacteria, cyanobacteria have an unusually high number of isoforms for each step in the glycogen metabolic pathway. Ball et al (35) have recently examined the genomes of many sequenced cyanobacteria and eukaryotic algae that produce starch or semi-amylopectin and have developed a more complete and complex picture of the evolution of starch production. Indeed, they have rejected their earlier hypothesis that a single event resulted in starch acquisition by a host after an endosymbiotic event that led to plastid development in eukaryotic algae and subsequently in plants (26,31,36,37).…”

“…They have demonstrated by laborious genetic screens that an isoamylase-like DBE (termed GlgX2) in Cyanobacterium Clg1 was responsible for formation of a starch-like material. Their genomic analyses led them to conclude that starch acquisition had occurred frequently in cyanobacteria and eukaryotes and that the glycogento-starch transition has likely occurred numerous times (35). This glgX2 gene product or any GH13-like DBE seems to be completely absent in Cyanothece sp.…”

Characterization of Function of the GlgA2 Glycogen/Starch Synthase in Cyanobacterium sp. Clg1 Highlights Convergent Evolution of Glycogen Metabolism into Starch Granule Aggregation

“…The answer to this question seems at first glance to be no. Indeed, some cyanobacteria, cryptophytes, and alveolates apparently lack the GH13 GlgX-like enzymes, while SSIII/SSIV/GlgA2 glycogen (starch) synthases are lacking in red algae, cryptophytes, and alveolates (Ball et al, 2015). We believe that other, more distantly related CAZymes will be recruited to do the very same job, but this still needs to be demonstrated.…”

“…Archaeplastida), stemming from primary plastid endosymbiosis and some of their secondary endosymbiosis derivatives (i.e. alveolates and cryptophytes; Cenci et al, 2014;Ball et al, 2015). Several lines of evidence suggest that starch metabolism evolved shortly after plastid endosymbiosis from a preexisting cytosolic eukaryotic glycogen metabolism enzyme network.…”