Tryptophanase disruption underlies the evolution of insect-bacterium mutualism

Animal-microbe symbioses are omnipresent, where both partners often gain benefits as mutualists. How such mutualism has evolved between originally unrelated organisms is of interest. Here we report that, using an experimental symbiotic system between the stinkbugPlautia staliand the model bacteriumEscherichia coli, disruption of a single bacterial genetnaAencoding tryptophanase makesE. colimutualistic toP. stali. Survey of natural bacterial mutualists across wild populations ofP. staliand other stinkbug species uncovered that theirPantoea-allied symbionts consistently lacktnaAgene. SomePantoeaspecies likeP. ananatisretaintnaAgene and cannot establish symbiosis withP. stali, buttnaA-disruptedP. ananatispartially restored the symbiotic capability. When a naturalPantoeamutualist ofP. staliwas transformed with a functionaltnaoperon, its symbiotic capability reduced significantly. Our finding suggests that tryptophanase disruption may have facilitated the evolution of gut bacterial mutualists in insects.