Arbuscular mycorrhizal fungi foster carbon and nitrogen storage in soil microaggregates even under drought conditions

Soil organisms such as arbuscular mycorrhizal fungi (AMF) and the roots they inhabit are key actors for shaping soil structure, which fosters a multitude of functions such as carbon storage and water availability. The expansion of AMF external hyphae, by being in direct contact with soil particles, can promote soil structure formation and thus induce a positive feedback on plant growth under unfavorable conditions such as drought.

Here, we aim at disentangling the complexity of the root-AMF-soil interface by partitioning the respective effects of AMF, of root, and of their interaction on soil structure formation and organic matter cycling, under both drought and well-watered conditions. To discriminate the effects of plant and AMF, we used the wild-type and two mutants of the plant species Lotus japonicus that cannot be properly colonized by AMF (ccamk and ram2-2). The mutant ccamk impairs root entry by the fungus and ram2-2 causes impaired arbuscule development. To exclude confounding factors, we used an artificial soil mixture (quartz, illite, goethite; loamy texture) that was free of microorganisms and native organic matter. The wild type and the mutants were grown in this substrate during a 60-day incubation in a climate chamber. Half of the mesocosms were inoculated with spores of the AMF Rhizophagus irregularis. We stopped the watering two weeks before the end of the experiment in half of the cylinders to create drought conditions. At the end, roots and shoots were sampled and the rhizosphere soil was separated from the non-rhizosphere soil. We analyzed root architecture, AMF traits (intraradical colonization, hyphae length), as well as aggregate distribution and their organic carbon and nitrogen contents in the rhizosphere soil.

Our results highlight the major role of AMF in promoting plant growth, with an increase of above-ground biomass, total root length and root surface area in the soil colonized with AMF, regardless of the water conditions. While plant root vigor (biomass, length, surface area) is reduced under drought conditions, the AMF are resistant to drought, with unchanged mycorrhization intensity and hyphae length in the soil that received less water. Under well-watered conditions, we quantified a higher share of macroaggregates. While AMF did not significantly affect soil structure formation, the presence of fungal hyphae resulted in an increase of carbon and nitrogen contribution of microaggregates in the rhizosphere soil. We are thus able to demonstrate that irrespective of soil water availability, AMF foster the vigor of the host plant. Furthermore, the expansion of AMF into soil, leading to higher carbon and nitrogen storage in rhizosphere soil microaggregates, is not dependent of soil moisture conditions.