Positive response of soil microbes to long-term nitrogen input in spruce forest: Results from Gårdsjön whole-catchment N-addition experiment

Abstract

Chronic nitrogen (N) deposition from anthropogenic emissions alter N cycling of forests in Europe and in other impacted areas. It disrupts plant/microbe interactions in originally N-poor systems, based on a symbiosis of plants with ectomycorrhizal fungi (ECM). ECM fungi that are capable of efficient nutrient mining from complex organics and their long-distance transport play a key role in controlling soil N mineralization and immobilization, and eventual nitrate (NO3−) leaching. Current meta-analyses highlight the importance of ECM biomass in securing the large soil N pool. At the same time, they point to the adverse effect of long-term N input on ECM fungi. The functioning of N-poor and N-overloaded forests is well understood, while the transient stages are much less explored. Therefore, we focused on the spruce-forest dominated catchment at Gårdsjön (Sweden) that received N addition of 40 kg N ha−1yr−1 over 24 years (a cumulative N input of >1200 kg N ha−1) but still loses via runoff only <20% of annual N input (deposition + addition) as NO3−. We found that, compared to the control, the N-addition catchment had a much larger soil microbial biomass. The N addition did not change the fungi/bacteria ratio, but a larger share of the bacterial community was made up of copiotrophs. Furthermore, fungal community composition shifted to more nitrophilic ECM fungi (contact and short exploration type ECM species) and saprotrophs. Such a restructured community has been more active, possessed a higher specific respiration rate, enhanced organic P and C mining through enzymatic production and provided faster net N mineralization and nitrification. These may be early indications of alleviation of N limitation of the system. We observed no signs of soil acidification related to N additions. The larger, structurally and functionally adapted soil microbial community still provides an efficient sink for the added N in the soil and is likely to be one of the explanations for low NO3− leaching that have stabilized in the last decade. Our results suggest that a microbial community can contribute to effective soil N retention in spite of the partial relative retreat (20–30%) of nitrophobic ECM fungi with large external mycelia, provided the fungal biomass remains high because of replacement by other ECM and saprotrophic fungi. Furthermore, we assume that N retention of similar C-rich boreal forests (organic soil molar C/N ~35) is not necessarily threatened by a large cumulative N dose provided N enters at a moderate rate, does not cause acidification and the soil microbial community has time to adapt through structural and functional changes.