Soil-derived bacteria endow Camellia weevil with more ability to resist plant chemical defense.

Background: Herbivorous insects acquire their gut microbiota from diverse sources, and these microorganisms play significant roles in insect hosts' tolerance to plant secondary defensive compounds. Camellia weevil (Curculio chinensis) (CW) is an obligate seed parasite of Camellia oleifera plants. Our previous study linked the CW's gut microbiome to the tolerance of the tea saponin (TS) in C. oleifera seeds. However, the source of these gut microbiomes, the key bacteria involved in TS tolerance, and the degradation functions of these bacteria remain unresolved.

Results: Our study indicated that CW gut microbiome was more affected by the microbiome from soil than that from fruits. The soil-derived Acinetobacter served as the core bacterial genus, and Acinetobacter sp. was putatively regarded responsible for the saponin-degradation in CW guts. Subsequent experiments using fluorescently labeled cultures verified that the isolate Acinetobacter sp. AS23 can migrate into CW larval guts, and ultimately endow its host with the ability to degrade saponin, thereby allowing CW to subsist as a pest within plant fruits resisting to higher concentration of defensive chemical.

Conclusions: The systematic studies of the sources of gut microorganisms, the screening of taxa involved in plant secondary metabolite degradation, and the investigation of bacteria responsible for CW toxicity mitigation provide clarified evidence that the intestinal microorganisms can mediate the tolerance of herbivorous insects against plant toxins. Video Abstract.