Organic nitrogen and ectomycorrhizal fungi mediate plant growth response to elevated CO2

Background/Question/Methods: Net primary productivity (NPP) has been globally stimulated by elevated atmospheric CO₂ (eCO₂). The magnitude and extent to which this effect continues is highly uncertain, but depends on plant assimilation of growth limiting soil nitrogen (N). Organic N bound in soil organic matter (N-SOM) has been widely proposed as an additional N source that could sustain plant response to eCO₂. Assimilation of N-SOM under field conditions remains poorly understood as does the role of this N source in plant growth response to eCO₂. Plant access to N-SOM is governed by ectomycorrhizal fungi (ECM), which represent a widespread and polyphyletic group of root symbionts. Using a natural soil inorganic N gradient in northern Michigan, we analyzed how shifts in ECM community composition mediate red oak (Quercus rubra) access to N-SOM. Next, we tested if N-SOM predominately supports red oak growth in soils in which the supply of inorganic N is low. Our third analysis tests if red oak uptake of organic N is a requisite for sustained growth response to rising ambient CO₂ concentrations. We employed dendrochronological measures of red oak growth paired with molecular characterization of ECM communities inhabiting the root-systems of 60 individual trees to address these predictions.

Results/Conclusions: Historical increases in CO₂ (+75 mmol/mol) over the past 38 years stimulated red oak growth in a context-dependent and threshold manner. Relative tree growth response to CO₂ was highest in soils where the supply of inorganic N was low. Our integrative analyses revealed coupled shifts in ECM community composition and function; hyphal morphologies associated with plant uptake of N-SOM dominated soils where the supply of soil inorganic N is low. In contrast, fungi possessing these morphological attributes declined in abundance in soils where inorganic N supplies were high. Together, these results suggest that assimilation of N-SOM is necessary for a robust eCO₂ response, and that plant assimilation of N-SOM is facilitated by a specialized subset of ECM taxa. Our results challenge the paradigm that all plants associating with ECM fungi can gain access to N-SOM, instead coupled compositional and functional changes in ECM communities may drive plant plasticity in plant nutrient assimilation. Finally, our results provide novel insight into plant growth response to eCO₂, documenting that the natural supply of inorganic N alone is insufficient to generate a sustained and positive NPP response. These analyses provide unprecedented mechanistic insight into the global fertilizing effect of eCO₂ on plant growth.