A horizontally transferred bacterial gene for pantothenic acid biosynthesis regulates diapause and reproduction in the spider mite Amphitetranychus viennensis

Horizontal gene transfer (HGT) has contributed substantially to the evolution of arthropod genomes, yet the functional significance of many horizontally acquired genes remains poorly understood. The hawthorn spider mite, Amphitetranychus viennensis, is a devastating agricultural pest whose high fecundity and overwintering diapause afford its exceptional ecological resilience. Through a genome-wide screen, we identified 37 high-confidence horizontally transferred genes (HTGs) in A. viennensis. Among these candidates, we prioritized AvPBL, a gene encoding pantothenate-β-alanine ligase, for functional characterization because it controls the rate-limiting step of a distinctly non-metazoan pantothenic acid (vitamin B5) biosynthesis pathway. RNAi-mediated suppression of AvPBL significantly reduced transcript abundance and endogenous pantothenic acid levels, triggering a 23.7% reduction in cumulative fecundity and severely compromising the mites' ability to enter winter diapause. Importantly, exogenous pantothenic acid supplementation rescued these reproductive and diapause defects, directly linking the observed phenotypes to the disruption of pantothenic acid biosynthesis. Our results demonstrate that the horizontally transferred bacterial gene AvPBL has been functionally integrated into the endogenous metabolic network of A. viennensis, playing a critical role in vitamin B5 biosynthesis, reproduction, and diapause regulation. These findings provide direct evidence that horizontally acquired metabolic genes can shape key life-history traits and drive adaptive evolution in arthropods.