The Early Metazoan Trichoplax adhaerens Possesses a Functional O-GlcNAc System

Background: Protein O-GlcNAcylation and orthologues of O-GlcNAc transferase (OGT) and O-GlcNAcase (OGA) occur separately or together in all kingdoms of life. Results: The basal metazoan Trichoplax adhaerens is the simplest organism to possess functional OGT, OGA, and protein O-GlcNAcylation together. Conclusion: Reversible protein O-GlcNAcylation is conserved throughout the metazoan lineage. Significance:T. adhaerens can be used as a reductionist model to identify evolutionarily conserved O-GlcNAc targets. Protein O-GlcNAcylation is a reversible post-translational signaling modification of nucleocytoplasmic proteins that is essential for embryonic development in bilateria. In a search for a reductionist model to study O-GlcNAc signaling, we discovered the presence of functional O-GlcNAc transferase (OGT), O-GlcNAcase (OGA), and nucleocytoplasmic protein O-GlcNAcylation in the most basal extant animal, the placozoan Trichoplax adhaerens. We show via enzymatic characterization of Trichoplax OGT/OGA and genetic rescue experiments in Drosophila melanogaster that these proteins possess activities/functions similar to their bilaterian counterparts. The acquisition of O-GlcNAc signaling by metazoa may have facilitated the rapid and complex signaling mechanisms required for the evolution of multicellular organisms.