Harvard Forest Nitrogen Saturation Experiment uncovers microbial response to long-term nitrogen additions

Human activities such as fossil fuel burning and intensive agriculture have raised atmospheric nitrogen deposition to 10 times or more above natural background levels in highly polluted regions. The Harvard Forest Nitrogen Saturation Experiment began in 1988 to examine ecosystem sensitivity, resilience, and resistance to long-term nitrogen enrichment. Sustained nitrogen enrichment over more than two decades has promoted ecosystem carbon storage, with soils accumulating as much or more carbon as trees and providing the main sink for nitrogen inputs. Nitrogen enrichment has also altered the structure and function of the soil microbial community which is responsible for key nutrient cycling processes.

Ectomycorrhizal fungi are root mutualists that provide an interface for carbon and nutrient exchange between plants and soil. Here, we address the question: Does nitrogen enrichment affect soil organic matter transformations by ectomycorrhizal fungi?

Over a 6-month period between bud break and litter fall, we found that ectomycorrhizal fungi consistently produced more carbon-degrading enzymes in nitrogen-enriched soil. We also observed tradeoffs between nitrogen-mobilizing and carbon-degrading enzyme production that were related to nitrogen-induced changes in ectomycorrhizal fungal community composition. Cortinarius species, which specialized in enzymes that liberate amino acids from protein, declined from 22 percent of in the ambient (control) nitrogen treatment to just 3 percent under high nitrogen additions. Conversely, Russula species, which specialized in enzymes catalyzing cellulose breakdown and organic matter oxidation, colonized 31 percent of ectomycorrhizal roots under ambient nitrogen conditions compared to over 70 percent under high nitrogen inputs.

Strong linkages between nitrogen-induced changes in ectomycorrhizal species composition and extracellular enzyme production suggest that enzymes are important factors underlying community responses to nitrogen supply. In addition, increased ectomycorrhizal enzyme synthesis in nitrogen-enriched soils supports a hypothesis of biotic soil nitrogen retention, whereby reactive nitrogen inputs are rapidly assimilated and secreted by mycorrhizal fungi as extracellular enzymes. Altogether, our findings suggest that anthropogenic nitrogen enrichment may alter the role of ectomycorrhizal fungi in carbon and nitrogen cycling in forest soils.