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

森林土壤通过固碳来补偿人为二氧化碳排放，是全球气候变化解决方案的一部分，而人为二氧化碳排放是全球气温上升的主要原因。土壤碳固存依赖于两个截然不同的过程：土壤有机质（SOM）分解导致碳流失，土壤有机质稳定通过将含碳生物分子转化为抗腐颗粒而导致碳储存。分解过程主要由自由生长的腐养（ST）土壤真菌控制。这些真菌通过分解SOM获得用于新陈代谢的C（能量）。另一类土壤生物是根系共生外生菌根真菌（EM），它们从与树木的联系中获得碳，并探索土壤中其他营养物质，如氮和磷。由于EM真菌从树木中获得C供应，大多数真菌已经失去了从SOM降解中获得C的酶能力，因为这不是它们营养的必要条件。由于ST真菌和EM真菌都是森林土壤传播的生物，它们相互作用和竞争，特别是争夺土壤养分。这种竞争相互作用可能导致抑制SOM分解（在EM优势下），因为EM真菌不需要分解SOM以获得碳，但可以快速获取土壤养分，如N和p。观察到的抑制SOM分解的效应，因为这些真菌类型的竞争被称为“Gadgil效应”。如果这是真的，这一现象控制了土壤在分解过程中释放的二氧化碳，从而提供了通过加强土壤中的碳固存来减缓气候变化的为数不多的选择之一。然而，ST和EM真菌在C循环中相互作用的机制仍然存在争议，并且缺乏了解，证据基础不一致。在我们的项目中，我们建议确定ST和EM真菌之间的相互作用是否可能是森林土壤生态中被忽视的组成部分，可以通过操纵来增加森林中土壤碳的固存。自从加吉尔效应被提出后的上半个世纪，主流观点一直认为EM或ST真菌是一个整体。然而，最近的遗传研究表明EM真菌具有高度的功能多样性，这表明将它们视为一个群体是错误的。这可以很好地解释为什么在科学文献中报道了许多关于加吉尔效应的相互矛盾的发现。我们对EM真菌代谢中丰富功能的新认识为质疑和最终确认Gadgil效应的存在（或不存在）开辟了新的途径。我们打算确定由于ST和EMF真菌相互作用导致土壤碳固存改变的机制：例如，增加某些EM真菌的优势地位可能会导致森林土壤中稳定SOM的产生增加。通过这种方式，土壤真菌可能能够作为减缓全球气候变化的可控组成部分加以利用。在本提案中，我们具体解决了3个基本问题：(1)ST-EM真菌相互作用在SOM分解和稳定中的作用是什么？(2)真菌类群的进化起源和功能生态学是否影响它们的相互作用对SOM动力学的影响？(3)不同环境条件下，群落中ST-EM相互作用的机制是什么？我们选择了四个不同的真菌群体，每个群体都由一个EM真菌与最接近的ST物种配对组成。我们设计了一个强大的模型系统来定量地解决真菌相互作用对SOM分解和稳定的功能影响。我们的实验计划包括四个复杂程度，依次验证ST-EM真菌相互作用的发现：(1)生长培养基上的真菌培养，(2)微观环境，其中EM真菌与植物共生，(3)与森林树木幼苗的中生态环境，以及(4)不同树种和土壤N有效性的野外地点。

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.