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Ectomycorrhizal Fungi: Participation in Nutrient Turnover and Community Assembly Pattern in Forest Ecosystems

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Ectomycorrhizal Fungi: Participation in Nutrient Turnover and Community Assembly Pattern in Forest Ecosystems Review Ectomycorrhizal Fungi: Participation in Nutrient Turnover and Community Assembly Pattern in Forest Ecosystems Yanjiao Liu 1,2, Xiangzhen Li 2 and Yongping Kou 2,* 1 College of Resources and Environment, Fujian Agriculture and Forestry University, Fujian University Engineering Center of Soil Remediation, Fuzhou 350002, China; [email protected] 2 Key Laboratory of Environmental and Applied Microbiology, CAS, Environmental Microbiology Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China; [email protected] * Correspondence: [email protected]; Tel.: +86-158-2822-1726 Received: 18 February 2020; Accepted: 15 April 2020; Published: 17 April 2020 Abstract: Ectomycorrhizal fungi (EcMF) are involved in soil nutrient cycling in forest ecosystems. These fungi can promote the uptake of nutrients (e.g., nitrogen (N) and phosphorus (P)) and water by host plants, as well as facilitate host plant growth and resistance to stresses and diseases, thereby maintaining the aboveground primary productivity of forest ecosystems. Moreover, EcMF can acquire the carbon (C) sources needed for their growth from the host plants. The nutrient regulation mechanisms of EcMF mainly include the decay of soil organic matter via enzymatic degradation, nonenzymatic mechanism (Fenton chemistry), and priming effects, which in turn promote C and N cycling. At the same time, EcMF can secrete organic acids and phosphatases to improve the availability of soil P,or increase mycelium inputs to facilitate plant acquisition of P.The spatiotemporal distribution of EcMF is influenced by a combination of historical factors and contemporary environmental factors. The community of EcMF is associated with various factors, such as climate change, soil conditions, and host distribution. Under global climate change, investigating the relationships between the nutrient cycling functions of EcMF communities and their distribution patterns under various spatiotemporal scales is conducive to more accurate assessments of the ecological effects of EcMF on the sustainable development of forest. Keywords: ectomycorrhizal fungi; nutrient cycling; community; biogeographic distribution; environmental response 1. Ectomycorrhizal Fungi and Forest Ecosystems Mycorrhizal fungi are an important group of soil microorganisms that form symbiosis, namely, mycorrhiza, with 97% of known terrestrial plants [1]. According to the criteria for root morphological differentiation and host plant phylogeny, there are mainly four types of mycorrhiza: arbuscular mycorrhiza (AM), ectomycorrhiza (EcM), orchid mycorrhiza (OrM), and ericoid mycorrhiza (ErM) [2]. EcM is formed by fungi infecting the roots of approximately 2% of vascular plants (mainly including Pinaceae, Fagaceae, Dipterocarpaceae, and Myrtaceae) [2–4]; this type of mycorrhiza is structurally characterized by the presence of a mantle and a Hartig net, with intercellular hyphae that do not enter cells [5]. In total, approximately 7750 species of fungi are known to form EcM in the world, although a final estimate of ectomycorrhizal fungi (EcMF) species richness would likely be between 20,000 and 25,000 on the basis of estimates of knowns and unknowns in macromycete diversity [6]. These EcMF belong to more than 80 independently evolved lineages and also belong to more than 250 genera [7,8], mainly from Basidiomycota and Ascomycota [9]. Forests 2020, 11, 453; doi:10.3390/f11040453 www.mdpi.com/journal/forests Forests 2020, 11, 453 2 of 16 EcMF are essential for plant nutrient uptake, seedling settlement, community restoration, and succession processes [10–13] (Figure1a). Specifically, symbiosis between plant roots and2 of EcMF 16 are through a favorable exchange for photosynthetic product to enhance plant uptake of nitrogen (N) EcMF are essential for plant nutrient uptake, seedling settlement, community restoration, and and phosphorus (P), thus playing a role in the carbon (C), N, and P cycles in forest ecosystems [5]. succession processes [10–13] (Figure 1a). Specifically, symbiosis between plant roots and EcMF are Moreover,through seedlings a favorable exhibit exchange enhanced for photosynthetic resistance toproduct pathogens to enhance due plant to the uptake mycelial of nitrogen network, (N) while their nutrientand phosphorus uptake is (P), also thus promoted playing a [role11]. in The the mycelialcarbon (C), networks N, and P formedcycles in byforest EcMF ecosystems are also [5]. involved in waterMoreover, transport seedlings among exhibit plants enhanced [14]. Additionally, resistance to pathogens EcMF can due relieve to the mycelial salt stress network, and heavywhile metal stress intheir host nutrient plants uptake [15–17 is also]. The promoted involvement [11]. The my ofcelial EcMF networks in the formed material by EcMF cycle are and also their involved nutritional relationshipsin water with transport plants among are comprehensively plants [14]. Additiona regulatedlly, EcMF by can host relieve type, salt EcM stress species, and heavy and climaticmetal and stress in host plants [15–17]. The involvement of EcMF in the material cycle and their nutritional environmentalrelationships conditions with plants (temperature, are comprehensively rainfall, regula andted N by availability). host type, EcM Recently,species, and based climatic on and a climate predictionenvironmental model, Steidinger conditions et (temperature, al. [18] indicated rainfall, thatand theN availability). global abundance Recently, ofbased EcM-associated on a climate trees will declineprediction by 10% model, by the Steidinger end of 2070,et al. [18] and indicated the maximum that the proportionglobal abundance of decline of EcM-associated will occur in trees the boreal and temperatewill decline ecotone. by 10% Inby lightthe end of of the 2070, decline and the in maximum biodiversity proportion that may of decline occur will under occur global in the climate change,boreal studies and of temperate fungal composition ecotone. In light and of richness the decline across in biodiversity habitats are that crucial may occur for understandingunder global and climate change, studies of fungal composition and richness across habitats are crucial for predicting fungi–host–environment relationships and their influence on forest ecosystem function [19]. understanding and predicting fungi–host–environment relationships and their influence on forest Numerousecosystem studies function have [19]. investigated the spatiotemporal distribution patterns of EcMF at various scales (suchNumerous as global, studies regional, have investigated and local the scales). spatiotemp Theoral results distribution demonstrated patterns of EcMF that theat various variation of biogeographicscales (such patterns as global, in EcMF regional, communities and local wasscales). scale-dependent The results demonstrated [20–22]. In that addition, the variation environmental of selectionbiogeographic (deterministic patterns processes) in EcMF and dispersal communities limitation was (stochasticscale-dependent processes), [20–22]. as In the addition, main processes influencingenvironmental biological selection community (deterministic assembly processes) in ecosystems and dispersal [23 limitation–26] (Appendix (stochasticA processes),), could drive as the the main processes influencing biological community assembly in ecosystems [23–26] (Appendix A), community assembly of EcMF simultaneously [27,28]. could drive the community assembly of EcMF simultaneously [27,28]. Figure 1.FigureThe 1. role The of role ectomycorrhizal of ectomycorrhizal fungi fungi (EcMF) (EcMF) in nutrient nutrient cycling: cycling: (a) Carbon (a) Carbon (C) flow (C) through flow through EcMF promotesEcMF promotes the turnoverthe turnover of of soil soil organic matter matter (SOM) (SOM) and cycling and cycling of nutrients ofnutrients [29]. (1) Plant [29 hosts]. (1) Plant transfer photosynthate to EcMF primarily as simple sugars [5]. (2) EcMF increase the effective hosts transfer photosynthate to EcMF primarily as simple sugars [5]. (2) EcMF increase the effective absorptive surface area of roots enabling the transfer of nutrients, water, and other soil resources to absorptive surface area of roots enabling the transfer of nutrients, water, and other soil resources hosts. (3) Hyphae can form inter- and intraspecific host mycelial networks for the bi-directional to hosts.exchange (3) Hyphae of nutrients can form and carbohydrates inter- and intraspecific [30,31]. (4) Root–mycorrhizal host mycelial networkssystems are forinvolved the bi-directional in the exchangerelease of nutrients of carbon anddioxide carbohydrates (CO2) by soil respiration [30,31]. (4) [32]. Root–mycorrhizal (5) The turnover of EcMF systems and arefine involvedroots are in the release of carbon dioxide (CO2) by soil respiration [32]. (5) The turnover of EcMF and fine roots are important sources of labile C and nutrients for microbial processes [29], and the residues of EcMF and the extramatrical mycelium are incorporated into organic matter [33]. (b) EcMF participate in the decay Forests 2020, 11, 453 3 of 16 of organic matter through enzymatic degradation and Fenton chemistry [29], the priming effect mediated by root and EcMF exudates [34] and the Gadgil effect caused by reduced saprotrophs activity based on the competitive interactions between mycorrhizal fungi and saprotrophs [35]. (c) EcMF transport phosphorus (P) from the soil to the symbiotic interface through phosphate transporters [36]. (d) EcMF accelerate weathering
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