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 stinkbug Plautia stali and the model bacterium Escherichia coli, disruption of a single bacterial gene tnaA encoding tryptophanase makes E. coli mutualistic to P. stali. Survey of natural bacterial mutualists across wild populations of P. stali and other stinkbug species uncovered that their Pantoea-allied symbionts consistently lack tnaA gene. Some Pantoea species like P. ananatis retain tnaA gene and cannot establish symbiosis with P. stali, but tnaA-disrupted P. ananatis partially restored the symbiotic capability. When a natural Pantoea mutualist of P. stali was transformed with a functional tna operon, its symbiotic capability reduced significantly. Our finding suggests that tryptophanase disruption may have facilitated the evolution of gut bacterial mutualists in insects.