Evolutionary origin of terpenoid biosynthesis in termites

Termites produce the most diverse array of terpenoids among metazoans, comprising over 200 structures. However, their biosynthesis has not yet been elucidated. Here, we identify a gene family which arose through the duplication of geranylgeranyl pyrophosphate synthase in the common ancestor of Neoisoptera, the terpene-producing termite lineage. We functionally characterized several proteins from this family as terpene synthases generating biologically relevant sesqui-and diterpenes. These include the queen pheromone (3R,6E)-nerolidol in Embiratermes neotenicus and the precursor of polycyclic defensive diterpenes (E,E,E)-neocembrene in Nasutitermes takasagoensis. We explore transposable element-mediated genomic mechanisms and selection pressures acting in the evolution of this gene family and report an amino acid site crucial for cyclization capacity as well as the enantiospecificity of the characterized enzymes. We conclude that we have identified an enzyme family underlying the remarkable richness of termite terpenoids, which likely contributed to the ecological success of Neoisoptera.