Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change

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. 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. 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. 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.