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Underground Mycology: The Relation Between Fungi, Soil and Tree Lynne Boddy, PhD Cardiff School of Biosciences, Biomedical Building, Museum Avenue, Cardiff CF10 3AX Summary Fungi interact directly with trees as biotrophs (obtaining nutrients from living cells/tissues) - either parasites or mutualistic mycorrhizas, and as necrotrophs (obtaining nutrition from cells/tissues that they kill). Mycorrhizas are crucial to the health of the vast majority of plants in nature, supplying them with water and mineral nutrients, and protecting against root pathogens. Fungi affect trees indirectly as saprotrophs, by decomposing dead organic matter and releasing the nutrients that were locked up therein. The relations between fungi, soil and tree are complex since fungi also interact with each other, with other microorganisms and with soil invertebrates affecting mycelial growth and functioning. With changing climate the outcome of these interactions is likely to differ, and hence the interaction between fungi and trees will also differ. Ecological roles of fungi Fungi have 3 main ways by which they obtain nutrition: (1) saprotrophy, in which dead plant, animal and microbial cells are utilised; (2) biotrophy, where nutrients are obtained from living cells; and (3) necrotrophy, where cells and tissues are killed. Biotrophs damage hosts when they are parasites, but others provide benefits and are mutualists. These latter include: (1) lichens, organisms comprising a fungal partner and an algal or cyanobacterial partner; and (2) mycorrhizas, an association between plant roots and a fungus. These nutritional modes are not mutually exclusive: for example, many mycorrhizal fungi have some saprotrophic ability, some mycorrhizal fungi can become pathogenic, and necrotrophs continue to live, for variable times, following death of the host. Saprotrophs Saprotrophic fungi are the major agents of decomposition (Boddy et al. 2008). In temperate forests 12-13 tonnes per hectare of biomass is added per year as a result of photosynthesis. In balanced systems a similar amount is decomposed to carbon dioxide and water, with release of mineral nutrients that had been ‘locked up’ in plant tissues. Fungi as a whole can decompose all naturally produced organic compounds, though their individual abilities vary. Cellulose and lignin are the main components of wood cell walls and the most abundant organic compounds on the planet. Cellulose can be decomposed by a wide range of microorganisms, but lignins are very complex molecules that can only be decomposed by a narrow range of microorganisms, mainly some basidiomycetes and a few xylariaceous ascomycetes (Baldrian 2008). These fungi are, therefore, hugely important in nutrient release and cycling in woodlands, allowing continued productivity of plants. Moreover, they play important roles in humus formation, soil structure and stability, provide food sources for invertebrates, and some are biocontrol agents. The organic resources upon which saprotrophic fungi feed are usually discrete, and vary in size from small plant fragments and invertebrates, through leaves, twigs, branches and stumps, to whole trees (Rayner & Boddy 1988; Fricker et al. 2008). They are located attached to living plants, dead plants, lying on the surface of soil and within soil. They are patchily distributed in time and space, though the leaf litter, for example, can form a more or less continuous layer on the forest floor. For continuing survival saprotrophic fungi must be able to spread between these resources, and this can be achieved by spores or mycelium. Spores allow rapid spread, sometimes over long distances, but contain relatively small amounts of nutrients. Mycelia, on the other hand, can draw upon a larger supply of nutrients than spores when colonizing new territory. Within organic matter, fungi spread as mycelium. Some fungi, especially cord-forming wood decay fungi and mycorrhizal species (see below) are able to grow into soil in search of new supplies of nutrients (Fricker et al. 2008). Some can cover several m2 or even hectares of forest floor, and are potentially immortal. These include fungi that colonize large patches of leaf litter on the forest floor (e.g. Collybia spp. and Marasmius spp.), fairy-ring-formers (e.g. Clitocybe nebularis) that grow as an ever increasing annulus of mycelium about 30 cm wide, small (e.g. Marasmius androsaceus) and large rhizomorph formers (e.g. Armillaria spp.), and cord-forming fungi (e.g. Hypholoma fasciculare, Phallus impudicus and Phanerochaete velutina). The cord- and rhizomorph-formers typically extend between spatially discrete woody resources separated by many centimeters (cms) or even meters, and can draw on resources held within the mycelium to sustain growth; cord-formers can also absorb soluble nutrients from soil, but insulated rhizomorphs are less able to do so. Plant matter, especially wood, is low in nitrogen and phosphorous compared to carbon. Thus a lot of wood has to be decomposed to provide sufficient minerals for production of enzymes and new mycelium. Not surprisingly, therefore, saprotrophic cord-forming fungi are extremely conservative of nutrients. Further, they adopt foraging strategies, with reallocation of biomass, for efficient discovery of new resources (Boddy & Jones 2007). Obviously, nutrients must be lost to soil at some point otherwise plant productivity would not continue, but exactly when this occurs is not known. Presumably nutrients are released when invertebrates graze on them and during mycelial battles with each other (see below). Biotrophic mutualists Lichens are not quantitatively important in photosynthesis in most ecosystems. They are, however, of major significance in some extreme environments where they may be the major vegetation type and/or may have a crucial role in soil formation, e.g. lichen heath. Elsewhere, lichens on rock and bare ground begin the soil formation by eroding the rock surface and by input of organic matter from dead tissues. Mycorrhizas, literally fungus roots, are formed by 85% of plant species including not only angiosperms and gymnosperms, but also pteridophytes, and it therefore comes as no surprise that there is a range of different types of mycorrhizas based on form and function (Smith & Read 2008). Those most commonly found in trees are termed ectomycorrhizas (ECM). Essentially they comprise a sheath of fungal material surrounding the fine roots, to a greater or lesser extent. Some hyphae grow within the roots, surrounding but not penetrating the root cortex cells to form a network – the Hartig net. This is the site of exchange of sugars from the plant and water and mineral nutrients from the fungus. This ‘swap’ forms the basis of mutualism in most mycorrhizal relationships. The mycelium of the fungus spreads extensively in soil enabling it to obtain water and nutrients that would be unavailable to the tree. Root hairs are suppressed in ectomycorrhizal roots, and often the fine roots make no contact with soil, thus the plants are entirely reliant on the fungus for water and nutrients. Moreover, the fungal sheath and dense mycelial network in soil provide protection against soil-borne root pathogens (see below). Also, some associations allow plants to tolerate and colonize toxic soils, e.g. contaminated with heavy metals. The specificity of the fungus and host varies between species. Some fungi form mycorrhizas with plants from widely different taxa, e.g. Paxillus involutus with Pinus and Betula, whereas others are specific to single or closely related plant species, e.g. Suillus grevilli with Larix, and Leccinum carpinum with hornbeam (Carpinus betula). Most plants form mycorrhizas with a range of fungal partners but some are, apparently, only mutualist with a few species, e.g. Alnus rubra in the USA with only Alpova dipophloens and Lactarius obscuratus. Arbuscular Mycorrhizas (AM) are the most common and widespread type forming with herbaceous plants, some trees, e.g. Acer, pteridophytes, and occasionally bryophytes. Only a few plant families lack them, e.g. Cruciferae and Chenopodiaceae (Smith & Read 2008). They are an ancient association being found in fossils from 400500 million years ago, and it is by virtue of these associations that plants were able to colonize land. Like ECM, AM fungi form a large mycelial biomass in soil that extends from plant roots. Unlike ECM, however, AM fungi do not form a sheath around the roots, nor change root morphology, and they actually penetrate root cortex cells, in which they branch profusely (forming arbuscles – ‘dwarf trees’) providing a large surface area for the exchange of carbon, mineral nutrients and water. They have also been implicated in protection against root pathogens. Ericoid mycorrhizas are the third most important ecological group (Smith & Read 2008). These are associations between fungi and the fine hair roots of heathland plants on peaty soils, e.g. heathers, Rhododendron and Vaccinium. About 80% of the volume of root cells is packed with coils of hyphae, and these extend into the soil. Again the fungus provides the plant with water and mineral nutrients, and the plant ‘pays’ with sugars. Plants in the genus Arbutus (e.g. Pacific mandrone, Arctostaphylos and several species of Pyrolaceae form arbutoid mycorrhizas with basidiomycetes that form ECM with forest trees. Thus, these plants are probably linked to trees via fungal mycelium, with the potential for exchange of carbon between the two. Indeed, ECM mycelium can link trees of different species, and sugars derived from photosynthesis in one tree have been detected in other trees (Leake et al. 2004; Smith & Read 2008). Plants in the Monotropaceae (e.g. Indian pipe) do not contain chlorophyll, and hence are unable to photosynthesise. Moreover they form balls of roots that are not spread out in soils. They form monotropoid mycorrhizas with genera such as Russula, Rhizopgon and Suillus, which form ECM in the coniferous forests in which they grow. These monotropid plants are thus effectively parasitic on the fungi for mineral nutrients and water, and on coniferous trees for carbon, via the mycorrhizal mycelium! Orchids are also effectively parasites for at least part of their lives. All orchids produce very small seeds and upon germination must rapidly establish mycorrhizal relationships, young plants being dependent on the fungus for not only mineral nutrients but also fixed carbon. The achlorophyllous species are dependent on the fungus throughout their lives, i.e. they are parasites, whereas mature chlorophyllous orchids provide fixed carbon to the fungus. The fungi involved are wood decay basidiomycetes, e.g. species in the genera Coriolus, Fomes and Marasmius, and pathogens, e.g. species in the genera Armillaria and Rhizoctonia. There is a delicate balance in the relationship involving fungi that have pathogenic ability. If insufficient sugars are provided by the orchid the balance can shift with the fungus becoming pathogenic. Mycorrhizas and nutrient cycling Mycorrhizas obviously play a major role in nutrient cycling since they provide plants with their mineral nutrients. In the past mycorrhizas were thought only to access inorganic nutrient pools, but it is now clear that they have the ability to access organic nitrogen and phosphorus, i.e. they have decomposer ability (Leake et al. 2004; Smith & Read 2008). ECM are particularly good at utilizing organic nitrogen (N), which is important in N-limited forests, e.g. many boreal forests. Its utilization short-circuits the conventional N cycle and, by by-passing the normal mineralization pathway, it restricts the supply of mineral N to non-ECM plants and other micro-organisms, and ACM plants may suppress other guilds such as AM herbs and some angiosperm seedlings whose AM fungal partners are less effective at N capture (Leake et al. 2004). Utilization of organic N and effective scavenging of ammonium by ECM reduces flow of N through the ammonification pathway, and thus minimises the residence time of mineral N in soil solution and eliminates loss of N from the ecosystem through ammonium leaching, nitrate leaching and denitrification. Addition of nitrogen in fertilizers and by deposition from the atmosphere has resulted in the loss of some mycorrhizal fungi, presumably because trees do not need to expend sugars on a mycorrhizal relationship that is unnecessary when nutrients are in luxary supply. The stipitate hydnoids, for example, are now endangered in Britain. Parasites and pathogens Biotrophic parasites, i.e. those fungi that obtain nutrition from living cells, tend to parasitize aerial plant parts, e.g. the rusts and smuts. Those fungi that attack plant roots are usually necrotrophs. Necrotrophs often attack plants that are not in possession of a strong host defence system, e.g. immature, over mature, suppressed or otherwise weakened, for example fungi that cause ‘damping off’. Phytophthora spp. (technically not Fungi, but Oomycota), that are becoming increasingly troublesome (Brasier 1999), however, colonize healthy tissues. Root pathogens move from one host to another via spores, mycelium, aggregated mycelial structures, such as cords and rhizomorphs, and via root contacts. For example, Phytophthoras spread by spores, Armillaria mellea via rhizomorphs, and Heterobasidion annosum via root grafts (Rayner & Boddy 1988). From a tree growers perspective pathogens are a nuisance, but from the point of view of how natural ecosystems function, pathogens are simply adding material to the decomposition system rather sooner than usual. Plants are obviously killed in nature by pathogenic fungi, but the problem is exacerbated when man plants extensive monocultures. Moreover, man has caused many of our new problems. For example, long-distance spread of Phytophthoras is often via soil or infected plant material, and many of the more serious diseases have probably resulted from man inadvertently introducing them to new and susceptible hosts (Brasier 1999). Interspecific interactions Fungi do not exist in isolation but rather continually encounter other organisms that impact upon their growth and activity. These organisms include other fungi (Woodward & Boddy 2008), invertebrates (Boddy & Jones 2008) and bacteria (de Boer 2008), though the latter have been little studied. When basidiomycete mycelia meet in organic resources their aggressive interactions may result in one fungus killing the other or a deadlock situation in which neither makes any headway into the territory of the other, often with the formation of interaction zone lines comprising plates formed from highly melanised contorted hyphae. Interactions also occur when mycelia meet in soil, and can be easily seen in laboratory soil microcosms though less easily in nature. Not only do mycelia of the same ecological group meet, e.g. saprotroph-saprotroph interactions, but so also do mycelia of different ecological groups, e.g. saprotroph-pathogen, saprotrophmycorrhiza and mycorrhiza-pathogen interactions. Since many saprotrophs are more combative than pathogens, saprotrophic mycelia can constrain the growth of pathogens. This will occur both in nature and following manipulation by man, and is the basis of biological control (Woodward & Boddy 2008). The classic example is application of spores of Phlebiopsis gigantea to cut stumps to prevent colonization and spread of the pathogen H. annosum. Saprotrophic cordforming basidiomycetes also have potential to control rhizomorphic spread of Armillaria spp.. Mycorrhizal fungi have long been known to offer protection to roots from soil-borne pathogens. Not only does this result from the physical and antimicrobial barrier of the ECM mycelium sheathing the root (Smith & Read 2008), but also from the extensive extra-radical mycelium (J.R. Leake, D.P. Donnelly & L. Boddy unpub.). Since saprotrophic and mycorrhizal mycelium are found in the upper layers of soil, they interact (Woodward & Boddy 2008). They compete directly for easily available nutrients and by aggressive mycelial interactions. Not only do these interactions result in changes to the space occupied by the mycelia, but also saprotrophs can alter mycorrhizal functioning: when mycelium of the saprotrophic cord-forming basidiomycete interacted with that of Paxillus involutus and Suillus bovinus allocation of photosynthate from the plant to the mycorrhizal mycelial tips was inhibited by Phanerochaete velutina (Leake et al. 2001). Nutrients may even be released to soil. Certainly, when saprotrophic mycelia meet each other nutrients are released into the soil, not only in the interaction region, but also elsewhere in the mycelium (J.M. Wells & L. Boddy unpub.). Further, decomposition rate of wood sometimes increases during interactions, and sometimes decreases (Woodward & Boddy 2008). These interactions could clearly alter nutrient uptake by trees, and nutrient recycling. Soil invertebrates often graze on fungal mycelia either directly or incidentally while ingesting colonized organic material. Fungal mycelia contain massively greater concentrations of nitrogen and phosphorus than does wood and even leaf litter, and is thus highly nutritious. Grazing by collembola dramatically alters mycelial morphology and growth rate, sometimes causing increases and sometimes decreases (Boddy & Jones 2008). Rate of wood decomposition and hence of nutrient cycling can also be affected, and nutrients are probably released during invertebrate grazing. Moreover, the outcomes of interspecific mycelial interactions can also change as a result of grazing (TD Rotheray, TH Jones & L. Boddy unpub.). This could have further repercussions for the composition of fungal communities, decomposition processes and nutrient cycling. Mycorrhizal fungi are also food for invertebrates, and grazing can disrupt the flow of carbon through mycorrhizal mycelia (Johnson et al. 2005). Conclusions Fungi are crucial to tree health. The relationship between fungi and trees is, however, likely to alter as climate changes. Temperature and moisture regime are major determinants of decomposition rate and hence of nutrient cycling. The optimum temperature for growth and metabolism of most fungi in temperate ecosystems lies between 25-35ºC. Clearly, most decomposer fungi experience suboptimal temperatures most of the time. Thus, increase in temperature, as a result of climate change, may result in an increased rate of fungal growth and organic matter decomposition, but only if sufficient water is available. Abiotic environment, however, affects the outcome of interactions between fungal mycelia, thus climate change is likely to affect the composition of fungal communities in soil and dead organic matter. Likewise mycorrhizal relationships may also alter. Currently, we have insufficient knowledge to understand what changes will occur and how these will affect decomposition processes, other aspects of ecosystem function and tree health. References Baldrian, P. (2008) Enzymes of saprotrophic basidiomycetes. In: Ecology of Saprotrophic Basidiomycetes (eds L. Boddy, J.C. Frankland & P. van West) pp. 19-42, Elsevier, Amsterdam. Boddy, L., Frankland, J.C. & van West, P. (eds) (2008) Ecology of Saprotrophic Basidiomycetes. Elsevier, Amsterdam. Boddy, L. & Jones, T.H. (2007). Mycelial responses in heterogeneous environments: parallels with macroorganisms. In Fungi in the Environment, ed. G. M. Gadd, S.C. Watkinson & P. Dyer, pp 112-140. Cambridge: Cambridge University Press. Boddy, L. & Jones, T.H. (2008) Interactions between Basidiomycota and invertebrates. In: Ecology of Saprotrophic Basidiomycetes (eds L. Boddy, J.C. Frankland & P. Van West) pp. 153 - 177, Elsevier, Amsterdam. Brasier, C. (1999) Phytophthora pathogens of trees: their rising profile in Europe. Information note. Forestry Commission, Edinburgh, UK. de Boer, W. & van der Wal, A. (2008) interactions between saprotrophic basidiomycetes and bacteria. In: Ecology of Saprotrophic Basidiomycetes (eds L. Boddy, J.C. Frankland & P. van West) pp. 143-154. Elsevier, Amsterdam. Fricker, M.D., Bebber, D. & Boddy, L. (2008) Mycelial networks: structure and dynamics. In: Ecology of Saprotrophic Basidiomycetes (eds L. Boddy, J.C. Frankland & P. van West) pp. 3- 18, Elsevier, Amsterdam. Johnson D, Kresk M, Wellington EMH, Stott AW, Cole L, Bardgett RD, Leake JR (2005) Soil invertebrates disrupt carbon flow through fungal networks. Science 309, 1047. Leaake, J.R., Donnelly, D.P., Saunders, E.M., Boddy, L. & Read, D.J. (2001) Carbon flux to ectomycorrhizal mycelium following 14C pulse labelling of Pinus sylvestris L. seedlings: effects of litter patches and interaction with a wood-decomposer fungus. Tree Physiology, 21, 71-82. Rayner, A. D. M. & Boddy, L. (1988). Fungal Decomposition of Wood: Its Biology and Ecology. John Wiley International, Chichester. Smith, S.E., Read, D.J. (2008) Mycorrhizal Symbiosis. 3rd edn. Academic Press. Woodward, S. & Boddy, L. (2008) Interactions between saprotrophic fungi. In: Ecology of Saprotrophic Basidiomycetes (eds L. Boddy, J.C. Frankland & P. van West) pp. 123 139, Elsevier, Amsterdam.