Microbial-mediated redistribution of ecosystem nitrogen cycling can delay progressive nitrogen limitation

Soil nitrogen (N) availability constrains future predictions of ecosystem primary productivity and carbon storage. The progressive N limitation (PNL) hypothesis predicts that forest net primary productivity (NPP) will decline with age, and that the response of NPP to elevated CO2 will attenuate through time due to negative feedbacks of NPP on the soil N cycle. A central assumption of the PNL hypothesis is that, without changes in exogenous exchange of N in an ecosystem, increases in plant N uptake require increased soil N cycling rates. However, at ecosystem scale, microbial N uptake exceeds plant uptake. Hence, a change in the partitioning of N between plants and soil microorganisms may represent an alternative mechanism to sustain plant N uptake in the face of PNL. To estimate N partitioning of total N cycling between plants and microbes, we measured and modeled growth and N uptake of trees, bacteria, saprotrophic fungi, and ectomycorrhizal fungi across a forest succession and N limitation gradient. The combined plant and ectomycorrhizal N uptake increased from early to late succession, and nearly matched saprotrophic N uptake in late successional sites, while total N cycling remained stable or even declined. Changes in microbial community structure can thus mediate a redistribution of ecosystem nitrogen cycling, allowing an increase in plant N uptake without concomitant increases in soil N cycling. We further suggest that microbe-mediated changes in N partitioning can delay PNL and may thereby act as a mechanism to extend the duration of the land carbon sink in response to rising atmospheric CO2.