Digging into the "Gadgil effect": how the competitive balance between fungal guilds affects carbon and nitrogen cycling

Forest soils are part of the solutions to global climate change by sequestering carbon (C) to compensate for anthropogenic CO2 emissions, which are the major cause of rising global temperatures. Soil C-sequestration depends on two contrasting processes: soil organic matter (SOM) decomposition which results in C-loss, and SOM stabilisation that results in C-storage by converting C-containing biomolecules into decay-resistant particles. Decomposition processes are primarily controlled by the free-living saprotrophic (ST) soil fungi. These fungi gain C (energy) for their metabolism by decomposing SOM. Another group of soil organisms are root dwelling symbiotic ectomycorrhizal (EM) fungi that obtain C from their association with trees, and explore the soil for other nutrients such as nitrogen and phosphorus. As EM fungi have a C supply from trees most have lost their enzymatic capabilities to acquire C from SOM degradation, as this is not an imperative for their nutrition.

As ST and EM fungi are both forest soil-borne organisms they interact and compete, particularly for soil nutrients. This competitive interaction may result in suppression of SOM decomposition (under EM dominance) as the EM fungi do not need to breakdown SOM for carbon but do rapidly acquire soil nutrients such as N and P. The observed effect that causes the suppression of SOM decomposition as these fungal types compete is known as the "Gadgil effect". If true, this phenomenon controls CO2 release from soil during decomposition and consequently offers one of the few options for climate change mitigation through enhanced C sequestration in soils. However, the mechanism by which ST and EM fungi interact in C cycling remains controversial and poorly understood, with an inconsistent evidence-base. In our project, we propose to determine whether the interactions between ST and EM fungi could be a neglected component of forest soil ecology that may be manipulated to augment soil C-sequestration in forests.

For the last half of the century, since the Gadgil effect was posited, the prevailing view has been that the group of EM or ST fungi act as a whole. However, recent genetic studies suggest a high functional diversity among EM fungi, indicating it would be wrong to treat them as one group. This may well explain why numerous contradictory findings of Gadgil effect have been reported in the scientific literature. Our new understanding of abundant functions in the metabolism of EM fungi as a group opens new avenues of interrogating and finally confirming the existence (or otherwise) of the Gadgil effect. We intend to identify the mechanisms that lead to alteration of soil C-sequestration due to ST and EMF fungal interactions: e.g. increasing the dominance of certain EM fungi may lead to an increase in the creation of stable SOM in forest soils. In this way, the soil mycota may be able to be harnessed as a managed component in mitigating global climate change.

In this proposal, we specifically address 3 fundamental questions: (1) What is the role of ST-EM fungal interactions in SOM decomposition and stabilisation? (2) Does the evolutionary origin and functional ecology of fungal taxa effect their interactions on SOM dynamics? (3) What are the mechanisms operating in communities in regard to ST-EM interactions under different environmental conditions?

We have selected four distinct fungal groups, each of them consisting of one EM fungus paired with the closest related ST species. We designed a robust model system to quantitatively address the functional effect of fungal interactions on SOM decomposition and stabilisation. Our experimental plan includes four levels of complexity that sequentially validate the findings of ST-EM fungal interactions: (1) fungal cultures on growth-media, (2) microcosms, where EM fungi are in symbiosis with the plant, (3) mesocosms with forest tree seedlings, and (4) field sites differing in tree species and soil N availability.