Understanding the diversity and community structure of arbuscular mycorrhizal fungi (AMF) is important for potentially optimizing their role in mining phosphorus (P) in agricultural ecosystems. Here, we conduct a comprehensive study to investigate the vertical distribution of AMF in a calcareous field and their temporal structure in maize-roots with fertilizer P application over a three-year period. The results showed that soil available-P response to P fertilization but maize yields did not. Phosphorus fertilization had no-significant effect on richness of AMF except at greater soil-depths. High P-supply reduced root colonization while optimum-P tended to increase colonization and fungal richness on all sampling occasions. Crop phenology might override P-supply in determining the community composition of active root inhabiting fungi. Significant differences in the community structure of soil AMF were observed between the controls and P treatments in surface soil and the community shift was attributable mainly to available-P, N/P and pH. Vertical distribution was related mainly to soil electrical conductivity and Na content. Our results indicate that the structure of AMF community assemblages is correlated with P fertilization, soil depth and crop phenology. Importantly, phosphorus management must be integrated with other agricultural-practices to ensure the sustainability of agricultural production in salinized soils.

Background: Arbuscular mycorrhizal fungi (AMF) are key soil organisms and their extensive hyphae create a unique hyphosphere associated with microbes actively involved in N cycling. However, the underlying mechanisms how AMF and hyphae-associated microbes may cooperate to influence N₂O emissions from “hot spot” residue patches remain unclear. Here we explored the key microbes in the hyphosphere involved in N₂O production and consumption using amplicon and shotgun metagenomic sequencing. Chemotaxis, growth and N₂O emissions of isolated N₂O-reducing bacteria in response to hyphal exudates were tested using in vitro cultures and inoculation experiments. Results: AMF hyphae reduced denitrification-derived N₂O emission (max. 63%) in C- and N-rich residue patches. AMF consistently enhanced the abundance and expression of clade I nosZ gene, and inconsistently increased that of nirS and nirK genes. The reduction of N₂O emissions in the hyphosphere was linked to N₂O-reducing Pseudomonas specifically enriched by AMF, concurring with the increase in the relative abundance of the key genes involved in bacterial citrate cycle. Phenotypic characterization of the isolated complete denitrifying P. fluorescens strain JL1 (possessing clade I nosZ) indicated that the decline of net N₂O emission was a result of upregulated nosZ expression in P. fluorescens following hyphal exudation (e.g. carboxylates). These findings were further validated by re-inoculating sterilized residue patches with P. fluorescens and by an 11-year-long field experiment showing significant positive correlation between hyphal length density with the abundance of clade I nosZ gene. Conclusions: The cooperation between AMF and the N₂O-reducing Pseudomonas residing on hyphae significantly reduce N₂O emissions in the microsites. Carboxylates exuded by hyphae act as attractants in recruiting P. fluorescens and also as stimulants triggering nosZ gene expression. Our discovery indicates that reinforcing synergies between AMF and hyphosphere microbiome may provide unexplored opportunities to stimulate N₂O consumption in nutrient-enriched microsites, and consequently reduce N₂O emissions from soils. This knowledge opens novel avenues to exploit cross-kingdom microbial interactions for sustainable agriculture and for climate change mitigation.

The challenge of producing food at low monetary cost comes with high environmental impacts as yield maximization by excessive fertilization and chemical pest control drive farmers away from using the natural multifunctional potential of soils. We show how the ecological concept of plant-soil feedback can be used to restore the capacity of agricultural soils to provide nutrients, suppress pathogens, and enhance crop resilience sustainably. We review how recent advances in molecular and multiomic methods, soil management, and crop diversification reduce negative and promote positive plant-soil feedback, emphasizing the need for rhizosphere microbiome engineering and soil restoration strategies. Applying nature-based plant-soil feedback principles would enhance transformation to more sustainable agricultural practices that secure food production by restoring natural soil functions, while simultaneously mitigating climate change.