Arbuscular mycorrhizal (AM) fungi can significantly contribute to plant nitrogen (N) uptake from complex organic sources, most likely in concert with activity of soil saprotrophs and other microbes releasing and transforming the N bound in organic forms. Here, we tested whether AM fungus (Rhizophagus irregularis) extraradical hyphal networks showed any preferences towards certain forms of organic N (chitin of fungal or crustacean origin, DNA, clover biomass, or albumin) administered in spatially discrete patches, and how the presence of AM fungal hyphae affected other microbes. By direct N labeling, we also quantified the flux of N to the plants (Andropogon gerardii) through the AM fungal hyphae from fungal chitin and from clover biomass. The AM fungal hyphae colonized patches supplemented with organic N sources significantly more than those receiving only mineral nutrients, organic carbon in form of cellulose, or nothing. Mycorrhizal plants grew 6.4-fold larger and accumulated, on average, 20.3-fold moreN originating from the labeled organic sources than their nonmycorrhizal counterparts. Whereas the abundance of microbes (bacteria, fungi, or Acanthamoeba sp.) in the different patches was primarily driven by patch quality, we noted a consistent suppression of the microbial abundances by the presence of AM fungal hyphae. This suppression was particularly strong for ammonia oxidizing bacteria. Our results indicate that AM fungi successfully competed with the other microbes for free ammonium ions and suggest an important role for the notoriously understudied soil protists to play in recycling organic N from soil to plants via AM fungal hyphae.

Mycorrhizal fungi interconnect two different kinds of environments, namely the plant roots with the surrounding soil. This widespread coexistence of plants and fungi has important consequences for plant mineral nutrition, water acquisition, carbon allocation, tolerance to abiotic and biotic stresses and interplant competition. Yet some current research indicates a number of important roles to be played by hyphae-associated microbes, in addition to the hyphae themselves, in foraging for and acquisition of soil resources and in transformation of organic carbon in the soil-plant systems. We critically review the available scientific evidence for the theory that the surface of mycorrhizal hyphae in soil is colonized by highly specialized microbial communities, and that these fulfill important functions in the ecology of mycorrhizal fungal hyphae such as accessing recalcitrant forms of mineral nutrients, and production of signaling and other compounds in the vicinity of the hyphae. The validity of another hypothesis will then be addressed, namely that the specific associative microbes are rewarded with exclusive access to fungal carbon, which would qualify them as hypersymbionts (i.e., symbionts of symbiotic mycorrhizal fungi). Thereafter, we ask whether recruitment of functionally different microbial assemblages by the hyphae is required under different soil conditions (questioning what evidence is available for such an effect), and we identify knowledge gaps requiring further attention.

Arbuscular mycorrhizal (AM) fungi lack efficient exoenzymes to access organic nutrients directly. Nevertheless, the fungi often obtain and further channel to their host plants a significant share of nitrogen (N) and/or phosphorus from such resources, presumably via cooperation with other soil microorganisms. Because it is challenging to disentangle individual microbial players and processes in complex soil, we took a synthetic approach here to study 15N-labelled chitin (an organic N source) recycling via microbial loop in AM fungal hyphosphere. To this end, we employed a compartmented in vitro cultivation system and monoxenic culture of Rhizophagus irregularis associated with Cichorium intybus roots, various soil bacteria, and the protist Polysphondylium pallidum. We showed that upon presence of Paenibacillus sp. in its hyphosphere, the AM fungus (and associated plant roots) obtained several-fold larger quantities of N from the chitin than it did with any other bacteria, whether chitinolytic or not. Moreover, we demonstrated that adding P. pallidum to the hyphosphere with Paenibacillus sp. further increased by at least 65% the gain of N from the chitin by the AM fungus compared to the hyphosphere without protists. We thus directly demonstrate microbial interplay possibly involved in efficient organic N utilisation by AM fungal hyphae.