Mycorrhizal Fungi Respond to Resource Inequality by Moving Phosphorus from Rich to Poor Patches across Networks

Matthew D Whiteside,Gijsbert D.A Werner,Victor E.A Caldas,Anouk Van’T Padje,Simon E Dupin,Bram Elbers,Milenka Bakker,Gregory A.K Wyatt,Malin Klein,Mark A Hink,Marten Postma,Bapu Vaitla,Ronald Noë,Thomas S Shimizu,Stuart A West,E Toby Kiers

doi:10.1016/j.cub.2019.04.061

Abstract

SummaryThe world’s ecosystems are characterized by an unequal distribution of resources [1]. Trade partnerships between organisms of different species—mutualisms—can help individuals cope with such resource inequality [2, 3, 4]. Trade allows individuals to exchange commodities they can provide at low cost for resources that are otherwise impossible or more difficult to access [5, 6]. However, as resources become increasingly patchy in time or space, it is unknown how organisms alter their trading strategies [7, 8]. Here, we show how a symbiotic fungus mediates trade with a host root in response to different levels of resource inequality across its network. We developed a quantum-dot-tracking technique to quantify phosphorus-trading strategies of arbuscular mycorrhizal fungi simultaneously exposed to rich and poor resource patches. By following fluorescent nanoparticles of different colors across fungal networks, we determined where phosphorus was hoarded, relocated, and transferred to plant hosts. We found that increasing exposure to inequality stimulated trade. Fungi responded to high resource variation by (1) increasing the total amount of phosphorus distributed to host roots, (2) decreasing allocation to storage, and (3) differentially moving resources within the network from rich to poor patches. Using single-particle tracking and high-resolution video, we show how dynamic resource movement may help the fungus capitalize on value differences across the trade network, physically moving resources to areas of high demand to gain better returns. Such translocation strategies can help symbiotic organisms cope with exposure to resource inequality.

Highlights

Because of our inability to precisely track how resources are moved between different species, it has not been possible to test these hypotheses about how exposure to resource inequality influences trading strategies in mutualisms
We developed a quantum-dot nutrient-tracking technique that allowed us to track the trade of fluorescently labeled phosphorus in arguably the world’s most widespread trade partnership: the mutualism between arbuscular mycorrhizal fungi and land plants [15]
By tagging phosphorus with highly fluorescent nanoparticles of different colors, we could follow the movement of resources from their points of origin, across a fungus, and into the host root

Summary

Introduction

We developed a quantum-dot nutrient-tracking technique that allowed us to track the trade of fluorescently labeled phosphorus in arguably the world’s most widespread trade partnership: the mutualism between arbuscular mycorrhizal fungi and land plants [15]. Arbuscular mycorrhizal fungi form underground networks of filamentous hyphae in the soil [16]. The fungus mobilizes and collects phosphorus from the soil and trades this commodity with its host plants for carbon in a market-like exchange [6, 8, 17,18,19,20]. By tagging phosphorus with highly fluorescent nanoparticles of different colors, we could follow the movement of resources from their points of origin, across a fungus, and into the host roo

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