Mycorrhizal type determines root–microbial responses to nitrogen fertilization and recovery

Nitrogen (N) fertilization has enhanced the forest land carbon (C) sink by increasing the amount of C stored in soils, possibly through reductions in decomposition. Established differences in nutrient acquisition strategies between trees that associate with arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) fungi have been shown to influence the magnitude of this N effect on decomposition and soil C stocks. However, N deposition is declining across many temperate North American forests and little is known about how mycorrhizal-associated strategies in trees may impact short-term recovery. To examine divergent nutrient acquisition responses to N between AM and ECM systems, we developed a conceptual framework based on the idea that N fertilization reduces the C cost of N acquisition. In this framework, under N fertilization, ECM trees shift from N mining to N foraging and AM trees shift from mycorrhizal foraging to root foraging. We expanded on this framework by hypothesizing that initial recovery occurs across a spectrum, where nutrient foraging strategies either (1) persist in their N fertilized state, (2) return to the ambient state, or (3) shift to a new steady state. We tested this framework by examining fine root biomass and morphology, mycorrhizal colonization, and soil enzyme activities in organic horizon, bulk mineral, and rhizosphere mineral soils in AM and ECM dominated plots during the last year of a ~ 30 year N fertilization experiment and 1-year after fertilization ceased at Bear Brook Watershed, in Maine USA. Overall, our results indicate that N fertilization disrupted the organic N mining nutrient economy of ECM trees by reducing fine root biomass and mycorrhizal colonization and altering root morphology to improve N foraging. In contrast, AM trees appeared to shift from mycorrhizal foraging toward root foraging by reducing mycorrhizal colonization while maintaining root biomass. While AM and ECM mycorrhizal colonization in the fertilized plots remained lower than the ambient plots during the year after fertilization ceased, the rapid recovery of roots in fertilized ECM soils back to a level similar to those of the control soils was mirrored by ECM rhizosphere and organic horizon enzyme recovery. The ECM bulk mineral and all of the AM soil enzymes activities remained at their N fertilized levels. Although these are short-term recovery responses, our results suggest that the recovery of enzyme activities in the majority of ECM soil fraction