Seasonal dynamics of microbiota in winter-adapted Collembola: Insights into symbiotic relationships and adaptation to low temperatures

Soil-dwelling invertebrates, found worldwide, are essential for decomposition of plant litter and other soil processes, requiring adaptations to changes in the climate. The microbiota associated with these animals profoundly impacts their health and fitness. While seasonal changes have been shown to shape vertebrate microbiota, the microbiota of arthropods adapted to winter remains unknown. In this study, we investigated microbiota of two Collembola species with different overwintering strategies, Tomocerus cf. jilinensis and Tomocerus nigrus, in summer and three different periods in winter (early, mid, and late winter) using 16S rRNA gene amplicon sequencing. The results reveal pronounced alterations in microbial diversity and composition of the Collembola driven by seasonal variations and temperatures. Collembola associated microbiota exhibited higher Shannon diversity during mid and late winter. Furthermore, early, mid, and late winter periods were characterized by an enrichment of representatives from Hungateiclostridiaceae, Pseudomonas, and Pedobacter, respectively. Distinct seasonal patterns in microbiota were observed across different Collembola species. Bacterial community networks in winter Collembola were predominatly marked by positive interactions. Ground temperature exhibited a negative correlation with the Shannon index of Collembola-associated bacteria and the relative abundance of Comamonadaceae, Renibacterium, Mycobacterium, Sphingomonas, and Aeromicrobium. Our study indicates that season alters Collembola associated microbiota and these microbial changes could facilitate Collembola activity in low temperatures. Overall, our study extends our knowledge of symbiotic relationships between winter-adapted animals and their microbiota.