Hyphosphere core taxa link plant-arbuscular mycorrhizal fungi combinations to soil organic phosphorus mineralization

Arbuscular mycorrhizal (AM) fungi acquire photosynthetically fixed carbon (C) from host plants and transport some of it to hyphosphere bacteria via an extensive extraradical hyphal network. The hyphosphere microbiome, fostered by hyphal exudates, is crucial for AM fungi to access soil organic phosphorus (Po) and enhance plant growth, but the impact of plant-AM fungal combinations is still not well-elucidated. To answer this question, we selected two plant species with differing photosynthetic efficiency, medic (a C₃ plant) and maize (a C₄ plant), along with 4 AM fungal species, and successfully established various plant-AM fungal combinations. We examined the growth of plants and AM fungi, the mineralization process of soil Po, and the absolute quantity, community composition, and metabolic preferences of the hyphosphere microbiome.

Maize-AM fungi combinations exhibited greater abilities to increase soil phosphatase activity and promote Po mineralization compared to medic-AM fungi combinations. This was related to substantial disparities in the hyphosphere core microbiome between maize and medic. Massilia, a pivotal member of the core microbiome and a keystone taxon within the hyphosphere network, showed a notably greater relative abundance in maize-AM fungal systems than in the medic treatment. Thirteen core bacterial strains isolated from the hyphosphere showed a universal ability to secrete phosphatase, with Massilia being the most proficient. Additionally, community level physiological profiles showed that the maize-associated hyphosphere microbiomes had a heightened capacity for metabolizing fructose and glucose, key components of hyphal exudates.

Our study demonstrates that different combinations of plants and AM fungal species modulate the relative abundance of the core taxon through hyphal exudates, thus influencing the functionality of hyphosphere microbiomes for Po mineralization in the phytate-enriched soil. This provides novel insights into AM symbiosis for nutrient cycling and underscores the potential of tailored plant-fungal pairings in improving agricultural nutrient management and soil health.