Honeybee-Gilliamella synergy in carbohydrate metabolism enhances host thermogenesis in cold acclimation: Honeybee-Gilliamella cold coadaptation

How gut symbionts contribute to host adaptation remains largely elusive. Studying co-diversified honeybees and gut bacteria across climates, we found cold-adapted species (Apis mellifera, A. cerana) exhibit enhanced genomic capacity for glucose, pyruvate, lipid and glucuronate produc-tion versus tropical species. Metagenomics revealed Gilliamella as the most enriched gut bacte-rium in cold-adapted bees. Germ-free honeybees inoculated with the Gilliamella from A. cerana showed increased activity, body temperature and fat storage upon cold exposure. Saccharide metabolomics demonstrated higher hindgut glucose levels in Gilliamella-colonized A. mellifera versus germ-free bees, and in A. cerana versus three sympatric tropical species. Although Gilliamella can hydrolyze β-glucan into glucose, cultural experiments suggest it preferentially degrades glucuronate to pyruvate. In turn, monocolonized bees upregulated hindgut glu-cose/pyruvate utilization while increasing glucuronate productionprovision, suggesting nutrition-al complementarity. Gilliamella's transporter genes predominantly target ascorbate (a glucu-ronate derivative), which is elevated in inoculated hindguts. Accordingly, Gilliamella converts ascorbate to D-xylulose-5P (promoting lipogenesis), while showing reduced growth on glucu-ronate/ascorbate versus glucose, potentially minimizing glucose competition with hosts. We re-vealed a highly coordinated host-symbiont metabolic synergy enhancing host energy acquisition for cold adaptation.