Evolution of Storage Polysaccharide Metabolism in Archaeplastida Opens an Unexpected Window on the Molecular Mechanisms That Drove Plastid Endosymbiosis

Abstract

Plastid endosymbiosis was selected through the establishment of a biochemical link between the disconnected metabolic networks of the cyanobiont and its eukaryote host. This link is likely to have consisted of the efflux of photosynthetic carbon from the bacterial symbiont to the cytosol of the eukaryote. Storage molecules are suspected to have played a pivotal role in the establishment of such a flux. The latter provided an immediate opportunity to feed carbon upon a supply dictated by cyanobacterial metabolism while allowing the host to tap these resources upon demand according to its own regulatory circuits. The presence of the stores thus buffered the disconnected and unrelated sources and sink pathways of photosynthetic carbon metabolism during the early stages of plastid endosymbiosis. Comparisons of extant biochemical networks explaining storage polysaccharide metabolism in the three lineages that emerged after plastid endosymbiosis have enabled the reconstruction of the simplest hypothetical ancient network. The latter possibly consisted of the export of photosynthate from the cyanobiont in the form of the bacteria-specific metabolite ADP-glucose and the polymerization of the latter in the host cytosol through an ADP-glucose-specific glucan synthase. Neither the required ADP-glucose transporter nor the glucan synthase can be suspected to have been encoded by the cyanobacterial or host genomes prior to endosymbiosis. Nevertheless these critical components were required to trigger the event. The possible origin of these two key proteins is reviewed.