Rapid and chemically diverse C transfer from trees to mycorrhizal fruit bodies in the forest

Ectomycorrhizal fungi (EMF) are common belowground tree symbionts, supplying trees with water and nutrients. In return, large amounts of C assimilated by trees can be allocated into EMF. However, the chemical forms in which the C is transferred from trees to fungi under field conditions are mostly unknown. In this study, we aimed to unravel the fate of tree-derived C in EMF. We conducted 13CO2 pulse labeling of Pinus halepensis trees in two forest sites with adjacent EMF sporocarps, combined with a non-targeted metabolomics profiling of root and sporocarp tissues. 13C was measured in sporocarps of Tricholoma terreum and Suillus collinitus up to 3 m from pine stems. C was assimilated in the labeled trees’ needles and transferred to their roots. Starting from day 2 after labeling, the C was transferred to adjacent sporocarps, peaking on day 5. We identified more than 100 different labeled metabolites of different chemical groups present in roots and sporocarps. Of them, 17 were common to pine roots and both EMF species, and an additional 8 were common to roots and one of the two EMFs. The major labeled metabolites in the root tips were amino acids and tricarboxylic acid intermediates. The major labeled metabolites in sporocarps were amino acids, nucleotides, and fatty acids. We also identified labeled carbohydrates in all tissues. Labeling patterns diverged across different tissues, which can hint at how the C was transferred. Considering the young tree as a sole C source for these sporocarps, and with a diurnal assimilation of 5.4 g C, the total monthly C source is ~165 g C. On average, there were 10 sporocarps around each tree, each requiring ~1 g C. Therefore, a 10 g C investment would make 6% of total tree C allocation, and about 12% of net primary productivity. Overall, we found that this significant and ubiquitous transfer of metabolites from tree roots to EMF sporocarps is more rapid and chemically diverse than once thought.

外生菌根真菌（Ectomycorrhizal fungi, EMF）是一类常见的地下树木共生体，可为宿主树木提供水分与营养元素。作为回报，树木同化的大量碳（C）可被分配至外生菌根真菌中。然而，在野外条件下，碳从树木向真菌转移的具体化学形态仍不完全明确。本研究旨在阐明树木来源碳在外生菌根真菌中的归趋。我们在两个毗邻外生菌根真菌子实体的林地里，对阿勒颇松（Pinus halepensis）开展了13CO2脉冲标记实验，并结合根与子实体组织的非靶向代谢组学分析。对距离松树树干3米范围内的口蘑（Tricholoma terreum）和粘盖牛肝菌（Suillus collinitus）子实体中的13C含量进行了检测。碳被标记树木的针叶同化，并转运至根系。自标记后第2天起，碳开始向相邻的子实体转运，并于第5天达到峰值。我们在根系与子实体中鉴定出100余种隶属于不同化学类别的标记代谢物。其中，17种代谢物在松树根系与两种外生菌根真菌中均存在，另有8种代谢物仅存在于根系与其中一种外生菌根真菌中。根尖中主要的标记代谢物为氨基酸与三羧酸循环中间产物；子实体中主要的标记代谢物则为氨基酸、核苷酸与脂肪酸。我们还在所有组织中鉴定出了标记的碳水化合物。不同组织的标记模式存在差异，这可为碳的转运机制提供线索。假设幼树是这些子实体的唯一碳源，且其日间同化碳量为5.4克，则月总碳源约为165克。每棵树周围平均有10个子实体，每个子实体约需1克碳。因此，10克的碳投入将占树木总碳分配量的6%，约占净初级生产力的12%。总体而言，我们发现碳从树木根系向外生菌根真菌子实体的代谢物转运不仅显著且普遍存在，其速率与化学多样性均远超此前的认知。