Do multitrophic interactions matter for tree nutrition? A laboratory study involving bacteria, bacterial-feeding nematodes and ectomycorrhizal fungi

Soil microorganisms act as a sink and a source of available N and P by mediating key processes in the biogeochemical N and P cycling. The microbial loop, based upon the grazing of bacteria is thought to play a major role in the mineralization of nutrients such as nitrogen (N) and phosphorus (P) in terrestrial ecosystems. However, little is known about the impact of grazing by nematodes on mineral nutrition of ectomycorrhizal woody plants. We addressed this question in young seedlings of Pinus pinaster, whether or not associated with the ectomycorrhizal basidiomycete Hebeloma cylindrosporum. Plants, whether inoculated or not with Bacillus subtilis and bacterial-feeding nematodes, isolated from the same P. pinaster plantation in ectomycorrhizae and soil respectively, were grown in sterile agar gel. N was supplied equally as nitrate and bacterial N, and P as mineral P, bacterial P or phytate. Phytate is a well-known poorly available P source to plants but is used by B. subtilis able to release phytase in the medium. Nematode grazing upon 15N labeled bacteria increased plant growth and induced a low accumulation of 15N in shoots compared to medium N. This effect disappeared with bacterial P as the sole source of P. In contrast, nematode grazing considerably enhanced plant P access from phytate, and ectomycorrhizae increased plant P accumulation. These results underline the importance of multitrophic interactions to increase mineral nutrition of a woody species from nutrients locked up in bacteria and the prominent role of P availability for microbial loop efficiency