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

摘要

class="head no_bottom_margin" id="sec1title">Results and DiscussionMutualistic partnerships are ubiquitous [] and allow species to colonize diverse environments that fluctuate dramatically in resource availability, from our mammalian guts [] to deep-sea trenches []. Although mutualistic trade can help individuals, the relative benefits to each partner will shift according to how resources are distributed [, ]. As resources become increasingly patchy in time or space, returns can become more variable, and thus less reliable [, , ]. Consequently, individuals may be favored to hoard resources—be it for consumption, to retain a competitive edge, or for trading later [, , ]. This can lead to a decrease in current trade. Alternatively, individuals may be able to exploit local resource variation to dictate favorable terms of trade [, ]. These higher returns would lead them to invest more heavily in trade. However, 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 []. Arbuscular mycorrhizal fungi form underground networks of filamentous hyphae in the soil []. The fungus mobilizes and collects phosphorus from the soil and trades this commodity with its host plants for carbon in a market-like exchange [href="#bib6" rid="bib6" class=" bibr popnode">6, href="#bib8" rid="bib8" class=" bibr popnode">8, href="#bib17" rid="bib17" class=" bibr popnode">17, href="#bib18" rid="bib18" class=" bibr popnode">18, href="#bib19" rid="bib19" class=" bibr popnode">19, href="#bib20" rid="bib20" class=" bibr popnode">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 root.Our aim was to examine how the trading strategy of a fungus responds to varying levels of resource inequality. We manipulated resource distributions across a fungus, simultaneously exposing it to rich and poor patches of tagged phosphorus across its network (href="/pmc/articles/PMC6584331/figure/fig1/" target="figure" class="fig-table-link figpopup" rid-figpopup="fig1" rid-ob="ob-fig1" co-legend-rid="lgnd_fig1">Figure 1). We then asked whether the fungus responds to higher resource inequality by increasing trade with the host plant, or by hoarding resources and trading less. Because our phosphorus was fluorescently labeled according to whether it came from a resource-rich or -poor patch (href="#mmc1" rid="mmc1" class=" supplementary-material">Figure S1), we could determine where these phosphorus resources were hoarded, relocated, or transferred to the host.href="/pmc/articles/PMC6584331/figure/fig1/" target="figure" rid-figpopup="fig1" rid-ob="ob-fig1">class="inline_block ts_canvas" href="/core/lw/2.0/html/tileshop_pmc/tileshop_pmc_inline.html?title=Click%20on%20image%20to%20zoom&p=PMC3&id=6584331_gr1.jpg" target="tileshopwindow">target="object" href="/pmc/articles/PMC6584331/figure/fig1/?report=objectonly">Open in a separate windowclass="figpopup" href="/pmc/articles/PMC6584331/figure/fig1/" target="figure" rid-figpopup="fig1" rid-ob="ob-fig1">Figure 1Experimental Design(A) Illustration of the experimental setup in which quantum-dot-tagged phosphorus was added to two nutrient compartments, keeping the absolute amount consistent but varying the ratios to create high (90:10), medium (70:30), and no resource inequality (50:50) across the fungus. Roots were confined to the root compartment, but the fungus was able to cross the plastic lip and enter fungus-only nutrient compartments. A plastic barrier prevented any non-fungal movement of injected nutrients.(B) Mock-up of inequality replicate with resource patches of cyan and red quantum-dot-tagged phosphorus and fungal network.(C) A close-up of a single fungal hypha with quantum-dot-tagged phosphorus in its network. See bar for scale.See also href="#mmc1" rid="mmc1" class=" supplementary-material">Figures S1 and href="#mmc1" rid="mmc1" class=" supplementary-material">S2.