Canonical terpene synthases in arthropods: Intraphylum gene transfer

Insects employ terpenoids for communication both within and between species. While terpene synthases derived from isoprenyl diphosphate synthase have been shown to catalyze terpenoid biosynthesis in some insects, canonical terpene synthases (TPS) commonly found in plants, fungi, and bacteria were previously unidentified in insects. This study reveals the presence of TPS genes in insects, likely originating via horizontal gene transfer from noninsect arthropods. By examining 361 insect genomes, we identified TPS genes in five species of the Sciaridae family (fungus gnats). Additionally, TPS genes were found in Collembola (springtails) and Acariformes (mites) among diverse noninsect arthropods. Selected TPS enzymes from Sciaridae, Collembola, and Acariformes display monoterpene, sesquiterpene, and/or diterpene synthase activities. Through comprehensive protein database search and phylogenetic analysis, the TPS genes in Sciaridae were found to be most closely related to those in Acariformes, suggesting transfer of TPS genes from Acariformes to Sciaridae. In the model Sciaridae Bradysia coprophila , all five TPS genes are most highly expressed in adult males, suggesting a sex- and developmental stage-specific role of their terpenoid products. The finding of TPS genes in insects and their possible evolutionary origin through intraphylum gene transfer within arthropods sheds light on metabolic innovation in insects.