Experimental Sodalis infection eliminates ancient insect symbiont

Many insects benefit from ancient nutrient-supplementing endosymbionts. While symbiont losses and replacements occur on evolutionary timescales, their dynamics remain enigmatic due to the lack of experimentally tractable systems. Here, we report on the experimental establishment of the culturable bacterium Sodalis praecaptivus in a grain pest beetle (Oryzaephilus surinamensis) and its effect on the native symbiont Shikimatogenerans silvanidophilus, which produces the tyrosine precursor prephenate. Injection of Sodalis into female beetles led to systemic intracellular infection and efficient transovarial vertical transmission but reduced host survival and reproduction. Interestingly, Sodalis also invaded the host’s bacteriomes, causing irregular morphology and rapid loss of Shikimatogenerans within three beetle generations. Transcriptomics revealed a strong upregulation of host immune effectors upon Sodalis infection, but little reaction from Shikimatogenerans, indicating that the ancient symbiont is incapable of responding adaptively to the introduced competitor. The rapid elimination of the native symbiont in O. surinamensis showcases the fragility of ancient beneficial symbioses and experimentally recapitulates a crucial step towards a functional symbiont replacement.