Cooperation through Competition—Dynamics and Microeconomics of a Minimal Nutrient Trade System in Arbuscular Mycorrhizal Symbiosis

Abstract

In arbuscular mycorrhizal (AM) symbiosis, fungi and plants exchange nutrients (sugars and phosphate, for instance) for reciprocal benefit. Until now it is not clear how this nutrient exchange system works. Here, we used computational cell biology to simulate the dynamics of a network of proton pumps and proton-coupled transporters that are upregulated during AM formation. We show that this minimal network is sufficient to describe accurately and realistically the nutrient trade system. By applying basic principles of microeconomics, we link the biophysics of transmembrane nutrient transport with the ecology of organismic interactions and straightforwardly explain macroscopic scenarios of the relations between plant and AM fungus. This computational cell biology study allows drawing far reaching hypotheses about the mechanism and the regulation of nutrient exchange and proposes that the “cooperation” between plant and fungus can be in fact the result of a competition between both for the same resources in the tiny periarbuscular space. The minimal model presented here may serve as benchmark to evaluate in future the performance of more complex models of AM nutrient exchange. As a first step toward this goal, we included SWEET sugar transporters in the model and show that their co-occurrence with proton-coupled sugar transporters results in a futile carbon cycle at the plant plasma membrane proposing that two different pathways for the same substrate should not be active at the same time.

Nitrogen and phosphate metabolism in ectomycorrhizas

“…At pH 6 and a Pi concentration of 10 μM in the apoplast, Schott et al . () demonstrated the establishment of an equilibrium state in which 2H + : H 2 PO 4 − influx into root cells would result in a corresponding efflux from fungal hyphae. The speed of equilibrium establishment, but not the equilibrium itself, was dependent on the apoplastic pH (a pH of c .…”

Nutrient exchange in arbuscular mycorrhizal symbiosis from a thermodynamic point of view

“…). Interestingly, this general network looks similar to the minimal network proposed previously for the P/C trade (Schott et al ., ). Indeed, if we model P and N as one combined commodity, the results presented previously for the P/C exchange would be (from a technical/mathematical/computational point of view) identical for a (PN)/C trade.…”

“…Likewise, the proton‐coupled phosphate transporter HcPT2 from the fungus Hebeloma cylindrosporum has been shown recently to be important for the unloading of radiolabelled 32 Pi towards Pinus pinaster roots during this ectomycorrhizal association (Becquer et al ., ). The model predicts the existence of nutrient status‐dependent regulations of the different transporters. For example, it has been proposed previously that the plant sugar transporters should be regulated in response to the plant's intracellular phosphate level (Schott et al ., ). Indeed, different experimental evidence points to diverse nutrient status‐dependent regulation cascades (Roth & Paszkowski, ; Wang et al ., ). Our analyses indicate that the release of C sources in an electroneutral manner, albeit not optimal in terms of energetics and C use efficiency, could be beneficial in terms of P acquisition.…”

“…However, when it comes to obtaining another nutrient in return for phosphate, the modelled ‘ what‐if ’ scenarios provide strong arguments against the involvement of anion channels. Instead, they further substantiate the notion that phosphate is released by proton‐coupled phosphate transporters (Schott et al ., ), which so far have been associated with phosphate uptake only. Meanwhile, this conclusion is also supported by experimental data.…”

“…A minimal transporter network for phosphate/sugar nutrient exchange in arbuscular mycorrhizal ( AM ) symbiosis modified from Schott et al . (). In the minimal model, both plant and fungal plasma membranes contain proton‐coupled phosphate transporters (H/P), proton‐coupled sugar transporters (H/C) and H + ‐ ATP ase‐driven background conductances.…”