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Coupled Shifts in Ectomycorrhizal Communities and Plant Uptake of Organic Nitrogen Along a Soil Gradient: An Isotopic Perspective

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Abstract

Plants associating with mutualistic ectomycorrhizal (ECM) fungi may directly obtain nitrogen (N) bound in soil organic matter (N-SOM). However, the contribution of N-SOM to plant growth under field conditions remains poorly constrained. We tested the hypothesis that turnover in ECM communities along soil inorganic N gradients mediates a functional transition from plant reliance on N-SOM in low inorganic N soils, to primarily inorganic N uptake in inorganic N-rich condition soils. We quantified the δ 15 N of Q. rubra foliage and roots, organic and inorganic soil N pools, and used molecular sequencing to characterize ECM communities, morpho-traits associated with N-foraging, and a community aggregated sporocarp δ 15 N. In support of our hypothesis, we document the progressive enrichment of root and foliar δ 15 N with increasing soil inorganic N supply; green leaves ranged from − 5.95 to 0.16‰ as the supply of inorganic N increased. ECM communities inhabiting low inorganic N soils were dominated by the genus Cortinarius, and other fungi forming hyphal morphologies putatively involved in N-SOM acquisition; sporocarp estimates from these communities were enriched (+ 4‰), further supporting fungal N-SOM acquisition. In contrast, trees occurring in high inorganic N soils hosted distinct communities with morpho-traits associated with inorganic N acquisition and depleted sporocarps (+ 0.5‰). Together, our results are consistent with apparent tradeoffs in the foraging cost and contribution of N-SOM to plant growth and demonstrate linkages between ECM community composition, fungal N-foraging potential and foliar δ 15 N. The functional characteristics of ECM communities represent a mechanistic basis for flexibility in plant nutrient foraging strategies. We conclude that the contribution of N-SOM to plant growth is likely contingent on ECM community composition and local soil nutrient availability.

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Data Availability

All data will be deposited upon acceptance in Dryad. Molecular sequencing data will be uploaded to GenBank upon acceptance. Isotopic data used in this study is available on Dryad at https://doi.org/10.5061/dryad.4f4qrfjbt.

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Acknowledgements

We thank J. Matthews, N. Ahmad, E. Herrick, B. VanDusen and the Dublin Store for valuable laboratory and field support. We thank J. Allgeier and L. Cline for their thoughtful comments on a draft of this manuscript. This work is supported by NSF award 1754369 to DRZ, and an Integrated Training in Microbial Systems (ITiMS) Fellowship to PTP.

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  1. School for Environment and Sustainability, University of Michigan, Ann Arbor, Michigan, 48109, United States of America

    Peter T. Pellitier, Donald R. Zak, William A. Argiroff & Rima A. Upchurch

  2. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, 48109, United States of America

    Donald R. Zak

  3. Department of Biology, Stanford University, Stanford, California, 94305, United States of America

    Peter T. Pellitier

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  1. Peter T. Pellitier
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Correspondence to Peter T. Pellitier.

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PP, DZ, and WA conceived of the study. All authors contributed to data collection. PP analyzed data with input from DZ and WA. PP wrote the paper and all authors provided constructive edits.

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Pellitier, P.T., Zak, D.R., Argiroff, W.A. et al. Coupled Shifts in Ectomycorrhizal Communities and Plant Uptake of Organic Nitrogen Along a Soil Gradient: An Isotopic Perspective. Ecosystems 24, 1976–1990 (2021). https://doi.org/10.1007/s10021-021-00628-6

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