Plants evolve complex interactions with diverse soil mutualist organisms to enhance P mobilization from the soil. These strategies are particularly important when P is poorly available. It is still unclear how the soil P source (e.g., mineral P versus recalcitrant organic P) and its mobility in the soil (high or low) affect soil mutualist biological (ectomycorrhizal fungi, bacteria and bacterial-feeding nematodes) richness—plant P acquisition relationships. Using a set of six microcosm experiments conducted in growth chamber across contrasting P situations, we tested the hypothesis that the relationship between the increasing addition of soil mutualist organisms in the rhizosphere of the plant and plant P acquisition depends on P source and mobility. The highest correlation (R2 = 0.70) between plant P acquisition with soil rhizosphere biological richness was found in a high P-sorbing soil amended with an organic P source. In the five other situations, the relationships became significant either in soil conditions, with or without mineral P addition, or when the P source was supplied as organic P in the absence of soil, although with a low correlation coefficient (0.09 < R2 < 0.15). We thus encourage the systematic and careful consideration of the form and mobility of P in the experimental trials that aim to assess the role of biological complexity on plant P nutrition.

Free-living nematodes have beneficial effects on plant growth and nutrition. Exploring how agricultural practices modulate these beneficial effects is still challenging. A study was conducted in Ferralsols from Madagascar from one unmanaged grassland and 16 upland rainfed rice fields, representative of different agricultural practices: rotation, agroforestry and monoculture. Intact soil cores in plastic cylinders were sampled in the field to assess the effects of agricultural practices on changes in plant growth and nutrition induced by the presence of bacterial-feeding nematodes. The soil cores were fumigated to kill the nematodes and moistened with a filtered fresh soil suspension containing only microbial cells. A rice seed was introduced in the core, which was then incubated under natural climatic conditions for 40 days with or without inoculation of the bacterial-feeding nematode Acrobeloides sp. The inoculation of the nematodes induced lower, similar or higher plant biomass and nutrient content in comparison to the control according to the agricultural practices. Positive effects of Acrobeloides sp. on plant functions were frequent in soil cores sampled from fields with high plant diversity, especially from agroforestry systems. The intact soil core technique appears to be a robust means of mimicking field conditions and constitutes a promising tool to assess effects on soil processes of the ecological intensification of agricultural practices.

Phytate is considered a poorly available plant P source but proved to be useful for particular soil bacteria strains. In soil-free conditions, it has been shown that bacteria locked up the mineralized phosphorus from phytate whereas bacterial grazers like nematodes were able to deliver P to plants. Here, we aimed to determine if the interactions between phytate-mineralizing bacteria, bacterial grazer nematodes, and mycorrhizal fungi could increase plant P acquisition from phytate in high P-adsorbing soils. Pinus pinaster was grown in a Cambisol supplemented with phytate. Plants, whether associated or not associated with the ectomycorrhizal fungus Hebeloma cylindrosporum, were either inoculated or not inoculated with the phytase-releasing bacteria Bacillus subtilis and the bacterial-feeding nematode Rhabditis sp. After 100 days, the dual inoculation of bacteria and nematodes significantly increased net plant P accumulation. We observed that, on average, mycorrhizal plants accumulated more P in their shoots than non-mycorrhizal plants. However, the highest plant P acquisition efficiency was found when the three soil organisms were present in the P. pinaster rhizosphere. We conclude that, in a highly inorganic P-fixing soil, plant P acquisition from phytate strongly depends on the grazing of phytate-mineralizing bacteria. Our results confirm the importance of the soil microbial loop to improve plant P nutrition from phytate, which should be considered a route to improve the utilization of this source of poorly available P by plants.

Soil bacterivorous nematodes are key plant mutualists that increase nutrient availability for plants either by enhancing the mineralization of organic compounds (the “mineralization pathway”) or by increasing plant lateral root branching following shifts in internal plant metabolism, and subsequently leading to a higher volume of soil prospected by the roots (the “hormonal pathway”). The effects of these organisms on the nutrition of plants growing in strongly nutrient-deficient ferrallitic soils, especially in soils with limited available inorganic phosphorus (P), are poorly known, as are the pathways involved. In our study, using Oryza sativa (Poaceae) and Acrobeloides sp. (Cephalobidae), we tested the “mineralization” and “hormonal” hypotheses in an acidic P-depleted Ferralsol from the Madagascar highlands. We assessed the effect of nematode inoculation on (i) inorganic P flow from soil to plant using the 32P labelling technique and (ii) plant root architecture using a rhizobox device. We showed that the ability of Acrobeloides sp. to enhance P uptake in plants is strongly limited in Ferralsols. However, when the soil pH was corrected with dolomite, Acrobeloides sp. increased plant P uptake probably through the “mineralization” pathway (higher microbial turnover). Indeed, the L-value increased by 49% in the presence of nematodes and dolomite, suggesting the production of unlabelled plant-available P, probably through a higher net P mineralization when the nematodes were inoculated. Using the rhizobox technique, we also observed increased root length in the presence of nematodes but the specific root length, the tip number and the root branching density did not increase in the presence of nematodes, suggesting that nematodes did not increase plant P uptake and growth in this soil as proposed by the “hormonal” hypothesis. From an ecological intensification perspective, to promote agro-ecological development in tropical regions, our results suggest that amending ferrallitic soils with P-rich organic matter and correcting soil pH with an appropriate amount of dolomite may constitute suitable agronomic actionable triggers to drive the mutualistic activity of bacterivorous nematodes.

We tested the ability of root-adhering soils (RAS) from eight rice cultivars to attract a bacterivorous nematode (Acrobeloides sp.) living in a poor-nutrient soil in Madagascar. We showed that the ability of rice to attract bacterivorous nematodes in its rhizosphere is variable among cultivars. FOFIFA 172 was the cultivar with the highest attraction value, the lowest root biomass (RB) and the highest RAS: RB ratio and RAS respiration. In contrast, nematodes exhibited strong repellent response to W880 RAS. Also, nematode attractancy was not related to rice resistance against pests (blast rice disease and Striga asiatica) neither to cultivar ability to grow at specific altitude. Our results suggest a trade-off in carbon allocation between plant biomass and root exudation driving nematode attractancy and raise questions about the impact of plant breeding on cultivar ability to interact with soil mutualists such as bacterivorous nematodes. Further investigations are required into (i) variation in root exudate quantity and composition among the eight cultivars and (ii) the response of rice cultivars to bacterivorous nematode inoculation.

Dispersion of bacterivorous nematodes in soil is a crucial ecological process that permits settlement and exploitation of new bacterial-rich patches. Although plant roots, by modifying soil structure, are likely to influence this process, they have so far been neglected. In this study, using an original three-compartment microcosm experimental design and polyvinyl chloride (PVC) bars to mimic plant roots, we tested the ability of roots to improve the dispersion of bacterivorous nematode populations through two wet, nonuniform granular (glass bead) media imitating contrasting soil textures. We showed that artificial roots increased migration time of bacterivorous nematode populations in the small-bead medium, suggesting that plant roots may play an important role in nematode dispersion in fine-textured soils or when soil compaction is high.