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.

Decay by ectomycorrhizal fungi couples soil organic matter to nitrogen availability

“…Specifically, investment in ECM symbionts with energetically costly organic N acquisition capacities is beneficial to plant hosts where inorganic N is scarce, favouring ECM taxa with a greater genetic potential to obtain N from SOM using peroxidases and other oxidative enzymes (Baskaran et al, 2017;Defrenne et al, 2019;. These decay traits enable ECM communities in soils with low inorganic N availability to more substantially supplement tree N nutrition with N from SOM across the ecosystems in our study (Pellitier, Ibáñez, et al, 2021;, and our current findings suggest this enhanced decay, in turn, reduces lignin-derived SOM and soil C storage (Figure 6). We propose that this nutritional tradeoff continues to operate in relatively fertile boreal forests, in which ECM fungi with peroxidases decline with increasing N availability and plausibly enable greater SOM decay by ligninolytic saprotrophs (Figure 6; Kyaschenko et al, 2017).…”

“…Our plots ranged in mineralisation rates from 0.08 to 1.19 μg N g −1 day −1 (Figure ). These values captured the full gradient of inorganic N availability in the upper Lake States region and have remained seasonally and interannually stable since the 1980s (Pellitier, Ibáñez, et al, 2021; Zak et al, 1989; Zak & Pregitzer, 1990).…”

“…Plots were in mixed stands of Quercus rubra (red oak) and Acer rubrum (red maple), which co‐occur across the inorganic N availability gradient, to minimise differences in the biochemistry of litter inputs. Plots were adjacent to previously studied ECM communities in Q. rubra root tips (Pellitier, Ibáñez, et al, 2021; Pellitier & Zak, 2021; Pellitier, Zak, et al, 2021). Our plots ranged in mineralisation rates from 0.08 to 1.19 μg N g −1 day −1 (Figure ).…”

“…Here, we tested the hypothesis that soil C storage increases with soil inorganic N availability and that this response is linked to declines in saprotrophic as well as ECM fungi with the genetic potential to decay lignin and lignin-derived SOM (Figure 1). We characterised fungal community composition, lignin-derived SOM, and soil C storage across a natural gradient of soil inorganic N availability in northern broadleaf temperate forests (Pellitier, Ibáñez, et al, 2021;Zak et al, 1989), in which microsite differences in topography create an inorganic N availability gradient by influencing water availability and nutrient retention (Zak et al, 1989; F I G U R E 1 Two fungal mechanisms (Saprotroph Mechanism and ECM Mechanism) could cause naturally high inorganic N availability to suppress the decay of lignin and its derivatives, thereby promoting the accumulation of lignin-derived SOM and increasing soil C storage 1990). We predicted that the relative abundance of ligninolytic fungi in decaying fine root litter and ECM fungi with peroxidases in soil would decline with increasing soil inorganic N availability.…”

Forest tree growth is linked to mycorrhizal fungal composition and function across Europe

“…The entire period covered was 1999–2017, the mean initial census year was 2005, the mean final census year was 2008, and the mean growth interval was 5.5 years. Although there is some variation in the annual sampling of tree growth versus the fungal community at some sites, previous work has shown that year-to-year variation in fungal communities is low at regional to continental scales [ 42 , 43 ]. Allometric equations for dominant tree species within our observed size and geographic range were used to calculate aboveground biomass using equations from the GlobeAllomeTree database [ 44 ]:…”