Microbial mediators in plant-vole interactions: Linking grassland plant traits and gut microbiota for conservation of Brandt’s voles

Understanding tripartite interactions among food plants, their associated microbiota, and herbivorous animals is crucial for advancing biodiversity conservation in grassland ecosystems. This study explores how plant palatability influences the epiphytic and endophytic microbiota of grassland plants and affects the gut microbiota of Brandt’s vole (Lasiopodomys brandtii), a key but declining herbivore in Inner Mongolian steppes. We analyzed the microbial communities of eight candidate food plants and the fecal microbiota of field and captive voles using 16S rDNA high-throughput sequencing. Results show that high-palatable plants (e.g., Leymus chinensis) had significantly lower endophytic bacterial diversity compared to low-palatable plants (e.g., Cleistogenes squarrosa). Low-palatable plants were enriched with Actinobacteria (24.66 %) and exhibited higher secondary metabolite synthesis capabilities, such as antibiotic production by Pseudomonas, potentially deterring herbivory. In contrast, high-palatable plants were dominated by Proteobacteria (98.45 %), including genera like Ralstonia which enhance plant digestibility, and suppress plant defenses to prioritize growth. Crucially, field Brandt’s voles consuming diverse plants show Bacteroidetes-dominated microbiomes for fiber digestion, while laboratory-reared voles on restricted diets develop dysbiosis with pathogenic Proteobacteria. Notably, 15 microbial phyla were shared between plant surfaces and vole guts, suggesting microbial transmission. These findings suggest a coevolutionary continuum wherein low-palatable plants utilize microbial defenses to resist herbivory, while high-palatable plants promote digestibility and vole attraction. This continuum shapes herbivore foraging behavior and nutrient cycling. We conclude that supporting diverse vegetation and microbe-mediated interactions is critical for conserving Brandt’s vole populations and maintaining ecological balance in grassland systems.