Arbuscular mycorrhizal fungi and Streptomyces: brothers in arms to shape the structure and function of the hyphosphere microbiome in the early stage of interaction.

BACKGROUND: Fungi and bacteria coexist in a wide variety of environments, and their interactions are now recognized as the norm in most agroecosystems. These microbial communities harbor keystone taxa, which facilitate connectivity between fungal and bacterial communities, influencing their composition and functions. The roots of most plants are associated with arbuscular mycorrhizal (AM) fungi, which develop dense networks of hyphae in the soil. The surface of these hyphae (called the hyphosphere) is the region where multiple interactions with microbial communities can occur, e.g., exchanging or responding to each other's metabolites. However, the presence and importance of keystone taxa in the AM fungal hyphosphere remain largely unknown. RESULTS: Here, we used in vitro and pot cultivation systems of AM fungi to investigate whether certain keystone bacteria were able to shape the microbial communities growing in the hyphosphere and potentially improved the fitness of the AM fungal host. Based on various AM fungi, soil leachates, and synthetic microbial communities, we found that under organic phosphorus (P) conditions, AM fungi could selectively recruit bacteria that enhanced their P nutrition and competed with less P-mobilizing bacteria. Specifically, we observed a privileged interaction between the isolate Streptomyces sp. D1 and AM fungi of the genus Rhizophagus, where (1) the carbon compounds exuded by the fungus were acquired by the bacterium which could mineralize organic P and (2) the in vitro culturable bacterial community residing on the surface of hyphae was in part regulated by Streptomyces sp. D1, primarily by inhibiting the bacteria with weak P-mineralizing ability, thereby enhancing AM fungi to acquire P. CONCLUSIONS: This work highlights the multi-functionality of the keystone bacteria Streptomyces sp. D1 in fungal-bacteria and bacterial-bacterial interactions at the hyphal surface of AM fungi. Video Abstract.

Potential Role of Sugars in the Hyphosphere of Arbuscular Mycorrhizal Fungi to Enhance Organic Phosphorus Mobilization.

Arbuscular mycorrhizal (AM) fungi engage in symbiosis with more than 80% of terrestrial plants, enlarging root phosphorus (P) absorption volume by producing extensive extraradical hyphae (ERH) in the soil. In addition, AM fungi recruit and cooperate with soil bacteria to enhance soil organic P mobilization and improve fungal and plant fitness through hyphal exudates. However, the role of the dominant compounds in the hyphal exudates in enhancing organic P mobilization in the mycorrhizal pathway is still not well understood. In this study, we added sugars, i.e., glucose, fructose, and trehalose, which are detected in the hyphal exudates, to the hyphal compartments (HCs) that allowed the ERH of the AM fungus to grow or not. The results showed that in AM fungus-inoculated pots, adding three sugars at a concentration of 2 mmol C kg-1 soil significantly increased the phosphatase activity and facilitated the mobilization of organic P in the HCs. The addition of fructose at a concentration of 2 mmol C kg-1 soil was the most efficient in increasing the phosphatase activity and enhancing organic P mobilization. The released inorganic P was then absorbed by the ERH of the AM fungus. The enhanced mobilization of organic P was correlated with the increase in phoD gene number and the changing bacterial community in the presence of fungal hyphae. The sugar addition enriched the relative abundance of some bacterial taxa, e.g., Betaproteobacteriales. Our study suggested that the addition of the sugars by mycorrhizae could be a pivotal strategy in managing P uptake in agricultural production, potentially directing future practices to optimize plant-fungi-bacteria interactions for improved P use efficiency.

Arbuscular mycorrhizal fungi enhance plant phosphorus uptake through stimulating hyphosphere soil microbiome functional profiles for phosphorus turnover.

The extraradical hyphae of arbuscular mycorrhizal (AM) fungi are colonized by different bacteria in natural and agricultural systems, but the mechanisms by which AM fungi interact with the hyphosphere soil microbiome and influence soil organic phosphorus (P) mobilization remain unclear. We grew Medicago in two-compartment microcosms, inoculated with Rhizophagus irregularis, or not, in the root compartment and set up P treatments (without P, with P addition as KH2 PO4 or nonsoluble phytate) in the hyphal compartment. We studied the processes of soil P turnover and characterized the microbiome functional profiles for P turnover in the hyphosphere soil by metagenomic sequencing. Compared with the bulk soil, the hyphosphere soil of R. irregularis was inhabited by a specific bacterial community and their functional profiles for P turnover was stimulated. At the species level, the shift in hyphosphere soil microbiome was characterized by the recruitment of the genome bin2.39 harbouring both gcd and phoD genes and genome bin2.97 harbouring the phoD gene, which synergistically drove nonsoluble phytate mobilization in the hyphosphere soil. Our results suggest that AM fungi recruits a specific hyphosphere soil microbiome and stimulated their functional profiles for P turnover to enhance utilization of phytate.