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Ectomycorrhizal fungi mediate belowground carbon transfer between pines and oaks

Abstract

Inter-kingdom belowground carbon (C) transfer is a significant, yet hidden, biological phenomenon, due to the complexity and highly dynamic nature of soil ecology. Among key biotic agents influencing C allocation belowground are ectomycorrhizal fungi (EMF). EMF symbiosis can extend beyond the single tree-fungus partnership to form common mycorrhizal networks (CMNs). Despite the high prevalence of CMNs in forests, little is known about the identity of the EMF transferring the C and how these in turn affect the dynamics of C transfer. Here, Pinus halepensis and Quercus calliprinos saplings growing in forest soil were labeled using a 13CO2 labeling system. Repeated samplings were applied during 36 days to trace how 13C was distributed along the tree-fungus-tree pathway. To identify the fungal species active in the transfer, mycorrhizal fine root tips were used for DNA-stable isotope probing (SIP) with 13CO2 followed by sequencing of labeled DNA. Assimilated 13CO2 reached tree roots within four days and was then transferred to various EMF species. C was transferred across all four tree species combinations. While Tomentella ellisii was the primary fungal mediator between pines and oaks, Terfezia pini, Pustularia spp., and Tuber oligospermum controlled C transfer among pines. We demonstrate at a high temporal, quantitative, and taxonomic resolution, that C from EMF host trees moved into EMF and that C was transferred further to neighboring trees of similar and distinct phylogenies.

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Fig. 1: Evidence for 13C transfer in the QuercusPinusQuercus combination (n = 2).
Fig. 2: Root δ13C of three treatments: Donor, Recipient, and Control (top to bottom).
Fig. 3: The relative abundance of fungal genera on roots of the studied pine and oak trees.
Fig. 4: Labeled carbon in the DNA of mycorrhizal fungi  as evidence for their role in belowgruond carbon transfer.

Data availability

Sequences were submitted to the National Center for Biotechnology Information Sequence Read Archive with the accession codes: Bioproject PRJNA777920.

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Acknowledgements

The authors wish to thank Ido Rog (Weizmann TreeLab) for help with the labeling system; Ishai Sher (WIS) for his help with the graphic design; and Alexander Brandis (WIS) for his help with performing MSMS analysis. RA was supported by MEYS (EF16_013/0001782 - SoWa Ecosystems Research). The study was funded by the European Research Council project RHIZOCARBON, granted to TK.

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TK, SLL and RC conceived and designed the experiment. RC and SLL performed the experiment and analyzed the data under the guidance of TK. SIP procedures and analysis were guided by RA. RC wrote the paper with SLL and TK, and all authors contributed substantially to revisions.

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Correspondence to Tamir Klein.

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Cahanovitc, R., Livne-Luzon, S., Angel, R. et al. Ectomycorrhizal fungi mediate belowground carbon transfer between pines and oaks. ISME J 16, 1420–1429 (2022). https://doi.org/10.1038/s41396-022-01193-z

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