Tripartite interactions among free-living, N-fixing bacteria, arbuscular mycorrhizal fungi, and plants: Mutualistic benefits and community response to co-inoculation

Interactions between arbuscular mycorrhizal (AM) fungi and free-living nitrogen fixers (FLNF) occur in the rhizosphere where they can enhance plant nutrient acquisition, impact plant growth, and affect soil processes. Tripartite mutualism commonly occurs between nodule-forming plants, symbiotic diazotrophs, and AM fungi, and can occur between non-nodulating plants, FLNF, and AM fungi. However, information on the extent of, and controls on, tripartite mutualism in non-nodulating plant systems is limited to a small number of crop plants and culturable microbial inoculum, mostly in greenhouse growing conditions. We conducted a systematic literature review to synthesize the current understanding of the responses of plants, AM fungi, and FLNF to co-inoculation, as well as the conditions affecting tripartite mutualism and the magnitude and range of benefits conferred. Our review shows that plants generally benefit from co-inoculation with AM fungi and FLNF taxa, but benefits are highly variable and context dependent, ranging from 94% reduction in plant shoot biomass to 255% increase in total plant biomass. Additionally, the presence of AM fungi can increase abundance of FLNF and the presence of FLNF can increase AM fungal root colonization, but these responses also vary widely. Major factors influencing variation in response to co-inoculation by all organisms include plant phenology/age, soil type and nutrient availability, and partner pairing. There is potential for leveraging these tripartite mutualisms to improve plant productivity and soil microbial function, but successful application is more likely with a thorough understanding of the environmental and mechanistic controls on these relationships and testing of field-scale implementation.