Microbiota as Potential Functional Traits Facilitating Springtail Activity in Winter

Understanding the role of microbiota in supporting animal survival and activity under extreme environmental conditions provides valuable insights into adaptation and resilience mechanisms in ecosystems. While vertebrate microbiota have received considerable attention, those associated with arthropods, particularly species capable of surviving sub-zero temperatures, remain poorly understood. Springtails (Collembola), key contributors to litter decomposition and soil ecosystem functioning, require specialized adaptations to endure harsh winter conditions. Using the α- and β-niche trait concept and phylogenetic comparative approaches, we investigated the microbiota of 10 coexisting springtail species with different overwintering strategies. Our results revealed that certain bacterial genera, including Marmoricola, Mycobacterium, Rhodococcus, and Vibrionimonas, exhibited phylogenetic signal, suggesting evolutionary constraints on their potential roles in hosts. Winter-active springtail species harbored higher bacterial diversity and distinct microbial community compositions compared to inactive species, with enrichment in bacteria such as Wolbachia, Morganellaceae, and Micrococcaceae. Additionally, winter-active species exhibited higher energy metabolism and lower lipid metabolism, alongside more frequent positive interactions within bacterial networks. These findings suggest that microbiota may play a functional role in supporting the metabolic demands of winter-active springtails, potentially contributing to their adaptation to cold environments. Overall, our study highlights the role of microbiota in shaping ecological success and adaptation of arthropods to extreme conditions, providing new perspectives for soil animal research by integrating microbial functional traits with the evolutionary context of microbe-host interactions.