Hyphosphere microorganisms facilitate hyphal spreading and root colonization of plant symbiotic fungus in ammonium-enriched soil

Abstract

Anthropogenic nitrogen inputs lead to a high ammonium (NH4+)/nitrate (NO3−) ratio in the soil, which restricts hyphal spreading of soil fungi. Access of symbiotic fungi to roots is a prerequisite for plant-fungal interactions. Hyphosphere bacteria protect fungi from environmental stress, yet the impact of hyphosphere bacteria on adaptation of host fungi to NH4+-enriched conditions remains unclear. By developing soil microcosm assays, we report that a plant-symbiotic fungus, Phomopsis liquidambaris, harbors specific hyphosphere bacteria that facilitate hyphal spreading and assist in the root colonization in NH4+-enriched soil. Genetic manipulation, 16S rRNA gene analysis and coinoculation assays revealed that the genus Enterobacter was enriched in the hyphosphere of NH4+-sensitive wild-type compared to NH4+-preferring nitrite reductase-deficient strain. The representative Enterobacter sp. SZ2-promoted hyphal spreading is only evident in nonsterilized soil. We further identified an increased abundance and diversity of ammonia-oxidizing archaea (AOA) and a synchronously decreased NH4+:NO3− ratio following SZ2 inoculation. Microbial supplementation and inhibitor assays showed that AOA-mediated reduction in NH4+:NO3− ratio is responsible for SZ2-enhanced fungal adaptation to NH4+-enriched conditions. The Ph. liquidambaris-Enterobacter-AOA triple interaction promoted rice growth in NH4+-enriched soil. Our study reveals the essential role of hyphosphere microorganism-based hyphal spreading in plant-fungal symbiosis establishment within nitrogen-affected agroecosystems.

The Diverse Mycorrizal Morphology of Rhododendron dauricum, the Fungal Communities Structure and Dynamics from the Mycorrhizosphere

“…The formation of mycorrhizal microecology is closely related to the habitat, as climatic elements [23] and edaphic features [24] in the habitat both influence the mycorrhizal microecology. Soil fungi community is a vital component of soil that has a critical influence on soil health and ecological functionality [25], and is also the direct interface with mycorrhizal interactions.…”

Decoding the microbiome for sustainable agriculture

“…Future exploration will be required to comprehend the molecular mechanisms by which the LNE-specific SynComs interact with soybean to facilitate plant N nutrition absorption, in a non-N 2 -fixing manner. In addition, apart from rootbacterial interactions, the cooperations between other functional microbiomes (including fungi and archaea) are common in the rhizosphere zone (Sun et al 2023). Therefore, the potential cross-kingdom communications among rhizobionts and their effects on plant fitness are of significant interest to advance sustainable agriculture.…”