Foliar-feeding weevils hijack tannin-degrading bacteria from the oak phyllosphere

The gut microbiota is a critical component in the life history of animals, particularly in the interactions between herbivores and plants. Phytophagous insects that feed on oak leaves face the challenge of detoxifying high-level tannins. Although the intestinal microbial community plays a key role in improving detoxification, it is not yet known where and how insects acquire the key tannin-degrading bacteria. Here, we tracked the source of tannin-degrading bacteria in the guts of Nothomyllocerus illitus Reitter, a major pest weevil that primarily consumes oak leaves, using 16S rDNA sequencing of gut microbiota, isolation and culture of bacteria, determination of tannin degradation activity of bacteria, as well as tracing fluorescently labeled bacteria. Our study showed that Bacillus, Acinetobacter, and Enterobacter represent the core bacterial genera involved in tannin degradation within the intestinal tract of N. illitus. Our findings provide strong evidence that N. illitus acquires these tannin-degrading bacteria from the oak phyllosphere rather than from the soil microbiome. The successful colonization of fluorescently labeled Bacillus and Acinetobacter in the weevil gut confirms that these bacteria empower N. illitus to degrade toxic tannins, enabling the weevil to thrive on oak leaves despite the presence of high concentrations of defensive chemicals, such as tannins.