Mycorrhizal plants from a variety of ecosystems have the capacity to take up organic forms of nitrogen, yet the fraction of plant nitrogen demand met by organic N (ON) uptake remains unclear. ON uptake by mycorrhizal plants is a biochemical process that involves multiple steps, including breakdown and uptake of soil ON by mycorrhizal fungi, internal transformation of ON, and transfer of N to the host plant. We present hypothetical mechanisms controlling each of these steps and outline predictions for how these mechanisms structure patterns of ON uptake by mycorrhizal plants in ecosystems. Using a synthesis of published data, we found that uptake of amino acids by mycorrhizal fungi is related to the relative abundance, N content, and carbon structure of the amino acid. We hypothesize that the bond strength and structural diversity of soil ON controls the breakdown of polymeric ON by mycorrhizal fungi. In addition, the availability of carbon resources for the mycorrhizal fungus influences the capacity for mycorrhizal fungi to assimilate amino acids and produce extracellular enzymes that catalyze the breakdown of polymeric ON. © 2009 Elsevier GmbH. All rights reserved.

1. In the conventional view of soil carbon (C) cycling, mycorrhizal fungi are primarily considered vectors for plant C input to soils. However, there is accumulating evidence that mycorrhizal fungi may also contribute to the direct loss of soil C by acting as decomposers, that is by producing extracellular lytic enzymes and metabolizing soil C. 2. Most of the evidence that mycorrhizal fungi can act as decomposers comes from studies of ericoid and ectomycorrhizal fungi, although there is increasing experimental evidence for a role of arbuscular mycorrhizal fungi in soil C decomposition. Decomposition by mycorrhizal fungi implies that soil C balance is subjected to the ecological factors that affect both plant and fungal symbionts; this interaction has important consequences for how soil C stocks respond to global change. 3. In this synthesis, we propose a new model of soil C cycling, including decomposition of soil C by mycorrhizal fungi, and we evaluate how this new integrative model alters our predictions of soil C feedbacks to global change. We present three hypothetical mechanisms by which mycorrhizal fungi may metabolize significant quantities of soil C. The first hypothesis ('Plan B' hypothesis) is that mycorrhizal fungi metabolize soil C as an alternate C source when supplies of photosynthate from the host plant are low. Our second hypothesis ('Coincidental Decomposer' hypothesis) is that mycorrhizal fungi decompose soil C as a consequence of mining soil for organic nutrients. The third hypothesis ('Priming Effects' hypothesis) is that mycorrhizal fungi decompose soil C when allocation of plant photosynthate to mycorrhizal roots is high, such that plant C 'primes' the growth and activity of mycorrhizal fungi. 4. Further empirical tests of these hypotheses will clarify the role of mycorrhizal fungi in soil C balance and improve our understanding of soil C responses to global change. © 2008 The Authors.