Nitrogen cycling microbiomes are structured by plant mycorrhizal associations with consequences for nitrogen oxide fluxes in forests

Abstract

Volatile nitrogen oxides (N₂ O, NO, NO₂ , HONO, …) can negatively impact climate, air quality, and human health. Using soils collected from temperate forests across the eastern United States, we show microbial communities involved in nitrogen (N) cycling are structured, in large part, by the composition of overstory trees, leading to predictable N-cycling syndromes, with consequences for emissions of volatile nitrogen oxides to air. Trees associating with arbuscular mycorrhizal (AM) fungi promote soil microbial communities with higher N-cycle potential and activity, relative to microbial communities in soils dominated by trees associating with ectomycorrhizal (ECM) fungi. Metagenomic analysis and gene expression studies reveal a 5 and 3.5 times greater estimated N-cycle gene and transcript copy numbers, respectively, in AM relative to ECM soil. Furthermore, we observe a 60% linear decrease in volatile reactive nitrogen gas flux (NO_y ≡ NO, NO₂ , HONO) as ECM tree abundance increases. Compared to oxic conditions, gas flux potential of N₂ O and NO increase significantly under anoxic conditions for AM soil (30- and 120-fold increase), but not ECM soil-likely owing to small concentrations of available substrate ( ${\text{NO}}_3^{-}$ ) in ECM soil. Linear mixed effects modeling shows that ECM tree abundance, microbial process rates, and geographic location are primarily responsible for variation in peak potential NO_y flux. Given that nearly all tree species associate with either AM or ECM fungi, our results indicate that the consequences of tree species shifts associated with global change may have predictable consequences for soil N cycling.

Keywords: forest soils; metagenomes; mycorrhizae; nitrogen cycle; nitrous oxide; reactive nitrogen oxides.