The mycorrhizal tragedy of the commons

The mycorrhizal tragedy of the commons

It is increasingly recognized that plant C allocation to mycorrhizal symbionts plays a critical role for plant nutrition and the future global CO₂ fertilization effect on plants (Terrer et al., 2019). At the same time its future impacts are hard to predict because we do not fully understand the mechanisms underlying the symbiosis. The traditional view of mycorrhizal symbiosis always helping plants has been challenged by observations of negative effects, e.g. on tree N uptake (Näsholm et al., 2013), which makes it difficult to understand why the symbiosis has evolved and why it is so widespread.

We propose, and tested, a theory explaining the contrasting findings by showing that mycorrhizal symbiosis can be both mutualistic and parasitic at the same time. Plants and fungi are connected in a mycorrhizal network where each fungus has multiple plant partners and vice versa. Each plant can gain additional N at the expense of the other plants by supplying more C to the fungi, i.e. paying a higher C price for N. At the same time the additional C supply increases N immobilization in fungal biomass, which reduces the total N export to all plants. Thus, an individual plant can gain N at the expense of its neighbors while the negative side effects are shared among all, resulting in a tragedy of the commons effect that reduces plant N uptake and drives N immobilization in the soil.

While some observations support this hypothesis, it had not yet been thoroughly tested experimentally – until now. Based on laboratory and field experiments in boreal pine forest we tested both key components of this hypothesis - individual level mutualism and the community parasitism (decline in plant N uptake). We also estimated the strength of the fungal discrimination among its plant partners, which drives the competitive C for N trading. Finally, we highlight potential consequences of these mechanisms for boreal forest C allocation and responses to rising CO₂.

References

Näsholm, T. et al., 2013. Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests? New Phytologist, 198(1): 214-221.

Terrer, C. et al., 2019. Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass. Nature Climate Change, 9(9): 684-689.