Common mycorrhizal networks of European Beech trees drive belowground allocation and distribution of plant-derived C in soil

Mycorrhizal fungi are an important partner of almost all land plants, who trade soil nutrients, such as Phosphorus or Nitrogen, for photosynthetic Carbon (C). Moreover, mycorrhizal fungi connect multiple plants with their mycelium in so called Common Mycorrhizal Networks (CMNs). CMNs formed by ectomycorrhizal (EM) fungi are an inherent part of boreal and temperate forests, often termed the ‘wood-wide web’. However, the role of these networks for plant belowground C allocation and distribution is not well known.

Here, we examined how plant photosynthates are distributed within EM mycelium networks connecting pairs of young beech trees, addressing the following questions: (1) Is the total belowground C allocation of plant photosynthates influenced by the size of the mycorrhizal network and its access to resources? (2) Is the belowground C distribution within a CMN altered if trees have unequal access to C from photosynthesis? (3) Do CMNs amplify or alleviate competition for nutrients between connected trees?

We planted young beech trees in pots in a special two-plant box set-up which allows to control the establishment of mycorrhizal networks between them. For this, two plant pots, penetrable by fungal hyphae but not by roots, were placed inside of plastic boxes and the interstitial space was filled with quartz sand. In addition, a hyphal-exclusive N source consisting of ¹⁵N labeled peat (‘peat bag’), was buried within each plant pot. Two treatments were applied in a fully factorial design: 1) Allowing/preventing the establishment of a CMN between the pots (some pots were turned around at a regular interval to prevent the establishment of CMNs) and 2) inequality of access to photoassimilated C (in part of the boxes one of the two plants was shaded). In a ¹³C-CO₂ labeling approach, we traced ¹³C assimilated by one plant of each tree pair into belowground pools of both plants by isotope ratio mass spectrometry (EA-IRMS) and ¹³C phospholipid fatty acid (PLFAs) analysis (GC-IRMS). At the same time, we investigated plant uptake of ¹⁵N via mycorrhiza by EA-IRMS.

Our results demonstrate that plants relied mostly on their fungal partners to acquire nutrients (63% of plant N was derived from mycorrhiza-exclusive peat bags), and also directed the majority of the C allocated belowground to their mycorrhizal partners. The presence of a larger mycorrhizal network connecting to another plant and an additional N source almost doubled photosynthetic CO₂ assimilation and belowground C allocation by plants. Fungi translocated carbon via hyphal linkages preferentially into mycorrhiza-exclusive nutrient patches, even when they were located within the realm of a neighboring plant and this necessitates to cross a nutrient-poor zone of sand. Shading did not affect the belowground distribution of C.

We conclude that belowground ectomycorrhizal networks represent a significant sink strength for plant photosynthates and may thus be a major driver of C sequestration in beech forest soils. The belowground distribution of C via fungal networks is mainly related to the distribution of nutrient-rich patches in the soil and less to differences in the photosynthetic capacity of the host plants.