Ectomycorrhizal access to organic nitrogen mediates CO2 fertilization response in a dominant temperate tree

Abstract

Plant-mycorrhizal interactions mediate plant nitrogen (N) limitation and can inform model projections of the duration and strength of the effect of increasing CO₂ on plant growth. We present dendrochronological evidence of a positive, but context-dependent fertilization response of Quercus rubra L. to increasing ambient CO₂ (iCO₂) along a natural soil nutrient gradient in a mature temperate forest. We investigated this heterogeneous response by linking metagenomic measurements of ectomycorrhizal (ECM) fungal N-foraging traits and dendrochronological models of plant uptake of inorganic N and N bound in soil organic matter (N-SOM). N-SOM putatively enhanced tree growth under conditions of low inorganic N availability, soil conditions where ECM fungal communities possessed greater genomic potential to decay SOM and obtain N-SOM. These trees were fertilized by 38 years of iCO₂. In contrast, trees occupying inorganic N rich soils hosted ECM fungal communities with reduced SOM decay capacity and exhibited neutral growth responses to iCO₂. This study elucidates how the distribution of N-foraging traits among ECM fungal communities govern tree access to N-SOM and subsequent growth responses to iCO₂.

Fig. 1. Hypothesized contribution of different nitrogen (N) forms to tree growth (red and orange lines; y-axis) and tree responses to historic increases in CO₂ (iCO₂).

These responses occur along a gradient of varying supply rates of inorganic N (net N mineralization rates: x-axis). Dark blue arrows show the relativized fertilization response (arrow width) to iCO₂. ECM fungal community composition, morpho-traits, and community aggregated decay traits (CADT) estimated using metagenomic approaches, are  hypothesized to vary with soil inorganic N availability. Note hypothesized turnover in the dominance of ECM taxa with extra-radical rhizomorphic hyphae and long-and medium-distance exploration morphologies. White speckles on roots depict hypothesized relative abundance of ECM root-tips. Illustration by Callie R. Chappell, with permission from Reinhard Agerer.

Fig. 2. Analysis framework and modeled contribution of inorganic N and N-SOM to plant growth.

A Representative analysis of tree growth as a function of net N mineralization rates. The change point analysis identifies the occurrence and location of an inflection point, if any, and the value of the slope parameters on each side. B Basal Area Increment (BAI), from 54 Q. rubra trees along the studied net N mineralization gradient (black circles correspond to an individual growth year). Red and blue lines indicate model estimated BAI mean and 95% PI above and below the identified change-point (BAI change point; estimates were calculated at average values of the other covariates). R² denotes overall Bayesian model fit. C Slope parameters are significantly different from each other (95% CIs do not overlap; different letters (n = 54). Asterisks indicates parameter is different from zero (95% CI does not overlap with zero).

Fig. 3. Compositional, morphological and functional turnover along the soil nitrogen gradient consistent with shifts in ectomycorrhizal (ECM) fungal N foraging traits.

A, and B relative sequence abundance of the ECM fungal genera Cortinarius and Russula along the gradient of net N mineralization rates (x-axis). Colored bands depict GAM fits. C Box-and whisker plot depicting ECM fungi forming short or medium-distance exploration types. Letters denote statistical significance D. ECM fungi forming rhizomorphic hyphae above and below the BAI statistical threshold (0.53 µgN g soil⁻¹ day⁻¹); letters adjacent to median line of box, denote statistical significance, points are individual communities totaling n = 58. Upper and lower hinges depict 25^th and 75^th percentiles. E Sum of CAZy gene counts (n = 100 gene families). F Specific gene families (headers) significantly enriched below the BAI change point. AA10, AA11 encode lytic polysaccharide monooxygenases, AA12 is an oxidoreductase, AA3_1: cellobiose dehydrogenase, CE5: acetyl xylan esterase.

Fig. 4. Analysis framework and evidence for context-dependent iCO₂ fertilization responses.

A Representative analysis framework of growth-nitrogen efficiency index (GNE) as a function of increasing concentrations of historic atmospheric CO₂ at each point along the net N mineralization gradient (different lines and their relative slopes). B Conceptual diagram of the effects of iCO₂ (λ) on plant growth; change point analysis can detect an inflection point along the soil gradient, if any. C Differences in $\mathbf{\theta }$ derived from the red and blue portion of panel B, indicate distinct slope values. D Dendrochronological data collected from 54 Q. rubra trees from the past 38 years. Individual points represent estimated annual GNE values colored by tree-specific rates of net-N mineralization. E Individual points represent individual trees response to iCO₂ (mean model slopes derived from D) over the study period. Red and blue lines denote Bayesian change-point model with plotted 95% PI (dashed lines; estimated at average values of other covariates) (n = 54). F Denotes mean and 95% CI for the red and blue slopes depicted in E; different letters denote significant differences between slopes, asterisks indicate significant differences from zero (95% CI do not include zero; n = 54).