Role of Gut Bacteria in Tomato Leaf Miner Tuta absoluta Gaining Resistance to α-Tomatine by Converting It to Cholesterol

Tuta absoluta is a worldwide invasive pest that causes severe losses in tomato industry in China, while its resistance mechanism to tomato's protective alkaloid of α-tomatine remains unclear. This study explores the role of its gut microbiota, and results showed that the abundance of the gut symbiont Enterococcus mundtii was significantly higher in T. absoluta feeding on wild-type tomatoes than that in those feeding on α-tomatine-deficient GAME2 mutant tomatoes. Isolated E. mundtii strain E14 degraded 72.2 ± 1.3% of α-tomatine in vitro; reinoculating it into antibiotic-treated T. absoluta restored the degradation ability. Inoculating E14 into five other lepidopteran pests (except noncolonized Plutella xylostella) enhanced their α-tomatine tolerance. Multiomics and in vitro pure-culture experiments showed that α-tomatine degrades into cholesterol via deglycosylation, reduction, and hydrolysis. This study reveals α-tomatine's dual role (toxin/cholesterol precursor) and E. mundtii as a key adaptation mediator, advancing our understanding of insect-plant coevolution and invasive pest control.