Gut microbiota and metabolic adaptations in apple snails Pomacea canaliculata: Insights into cold tolerance

Ample evidence highlights the pivotal role of gut microbiota in facilitating invasive species' adaptation to harsh environments. However, the molecular mechanisms underlying gut microbiota-mediated regulation of host metabolism and cold tolerance in snails remain elusive. Herein, we adopted a multidisciplinary approach to elucidate how gut microbiota contribute to cold tolerance in the apple snail Pomacea canaliculata. Under cold stress, high-latitude Group H snails had higher survival rate, energy level, and antioxidant enzyme activity than low-latitude Group G. After 60 h at 0 ℃, the survival rate of Group H increased by 5.53 times compared to that of Group G. Notably, 14 proteins related to fatty acid synthesis and energy metabolism, such as fatty acid-binding protein (FABP), pyruvate dehydrogenase E1 subunit (PDHE1), and aldo-keto reductase (AKR), were significantly upregulated. Group H exhibited higher abundances of psychrotrophs (Frackibacter, Massilia), lipid metabolism-related microbes (Herbiconiux, Achromobacter), and lactic acid bacteria (Aerococcus, Vagocococcus), boosting lipid metabolism and energy supply. Metabolomics showed increased synthesis of 19 long-chain fatty acids. Correlation analysis identified significant correlations among snail proteins, gut microbiota, and metabolites. Gut microbial responses modulated host fatty acid synthesis-related proteins, promoting fatty acid metabolite accumulation, enhancing energy supply and cell membrane fluidity, and collectively improving apple snails' cold tolerance. This study highlights the critical role of gut microbiota in mediating cold tolerance in apple snails, providing novel insights into invasive species' adaptation to climate change.