PAN: Philosophy, Activism, Nature 10, 2013 Fungi The unsung heroes of the planet Lynne Boddy1 Introduction We all know that plants are the "ʺpower stations"ʺ of the natural world – they fix energy from sunlight which fuels most other organisms including us. What many people do not realise is that fungi are equally important, and that without them the plants and, hence, the ecosystems of our planet would not work. If number of species is anything to go by then with an estimated five million, fungi are significant. For comparison there are estimated to be up to 400,000 species of flowering plants, 11,000 species of ferns and 12,000 species of moss. There is a tendency for people to think of fungi only as organisms that kill our plants, rot our food and even have the temerity to grow on us and sometimes kill us, perhaps also sometimes remembering that some are good to eat. Certainly, fungal diseases do cause annual crop losses of around US$ 140 billion worldwide, and losses of major crops can sometimes be over 50 percent. Crop losses do not stop there. Spoilage in storage sometimes accounts for as much as a further 25–30 percent loss. Fungi also grow on animals, including humans. While many infections are superficial, irritating and inconvenient, such as athlete’s foot and vaginal and oral thrush, and can be relatively easily controlled, it is a different story when they colonise deep within our bodies. Worldwide, about two million people die from fungal infections annually, particularly if the patients have immune systems that are already compromised, for example, those suffering from AIDS or surgical trauma, or undergoing cancer therapy or organ transplants. Some animal species have even been driven to extinction by mortality resulting from fungal infection including at least three species of frog: the Australian gastric brooding frog (Rheobatrachus sp.), the Panamanian golden frog (Atelopus zeteki) and the sharp-­‐‑snouted day frog (Taudactylus acutirostris) killed by the chytrid Batrachochytrium dendrobatidis (commonly known as Bd).2 My first encounter with fungi was on the negative side, at least from a human perspective. I was an undergraduate living with other students in rented accommodation in the basement of a house at the end of a Georgian terrace. One day I tried to open a wooden drawer and only succeeded by applying considerable force. The drawer had become attached to the back of the unit by a fungus. In fact, the unit was attached to the wall by a fungus. We discovered, in a cupboard under the stairs, a waft of fungal tissue occupying half a cubic metre. Later fungal brackets emerged and produced millions of rust coloured spores. It was the dreaded dry rot fungus Serpula lacrimans, which has the ability to grow through plaster, concrete and brickwork, translocating water and nutrients so that it can grow from damp regions into dry. I now 112 Lynne Boddy, Fungi – the unsung heroes of the planet wonder whether it grew into the other houses in the Georgian terrace. It is difficult and expensive to eradicate but, of course, I only learned all of this much later. My first formal encounter with fungi, and the beginning of my appreciation of their uniqueness and importance, took place during a soil ecology course at about the same time. This dry rot fungus was not mentioned since it does not grow outside of buildings in most parts of the world. What are fungi and why are they important? Before explaining why fungi are crucial to the functioning of Earth’s ecosystems, it is worth considering what a fungus is.3 The image that often springs to mind first is that of a mushroom or toadstool (the words are interchangeable in meaning). However, a mushroom is simply the sexual reproductive structure of one major grouping of fungi – Basidiomycota, which appear fairly infrequently in the life of a fungus. It is equivalent to the flowers or fruits of flowering plants. Though some fungi exist as single cells (e.g., yeasts), the main body of most fungi is the mycelium (Figure 1). This structure comprises an interconnected network of fine filaments (or tubes termed hyphae), which grow from their tips, and feed on the organic matter in which or upon which they are growing. They feed by exuding enzymes that break down (digest) large molecules into small ones that they can absorb through the walls and membranes surrounding their hyphae. Taken as a whole, kingdom Fungi can probably breakdown all naturally produced organic molecules, though individual species have narrower abilities. It is this vast enzymatic ability and filamentous body form, allowing fungi to penetrate into bulky objects, which make fungi so important in the natural world. Fungi obtain their nutrition in three main, but not mutually exclusive, ways: firstly, by feeding on the remains of dead plants, animals and other organisms – termed saprotrophy; secondly, by killing cells and tissues and then feeding on them – necrotrophy; and, thirdly, from living cells – biotrophy. It is the necrotrophs and biotrophic parasites that give the superficial impression that fungi are bad news for humans. Figure 1. Fungal mycelium. Fungal hyphae are microscopic, but in some fungi hyphae aggregate together to form larger mycelial structures visible to the naked eye. Here mycelium of the stinkhorn fungus (Phallus impudicus) is growing from a wood block (sides 2 cm) across the surface of soil from a woodland. © Alaa Alawi 113 PAN: Philosophy, Activism, Nature 10, 2013 The saprotrophic fungi are the planet’s major recyclers – the garbage disposal agents of the natural world.4 The significance of these fungi is immediately clear, when you consider that 150 billion tonnes of organic matter are produced each year in forest ecosystems worldwide.5 Most of this organic matter is lignocellulose, which comprises complex, recalcitrant molecules that can only be broken down by a narrow range of specialist basidiomycete and xylariaceous ascomycete fungi.6 It is not just that we would be up to our proverbial armpits in dead organic matter if it were not for decomposer fungi. "ʺLocked up"ʺ in this dead organic matter are mineral nutrients, such as nitrogen and phosphorous which are essential for plant growth. If these were not released from dead organic matter the supply of available mineral nutrients would run out in a few years, and plants would not be able to grow. Though the Earth’s atmosphere contains almost 80 percent of nitrogen gas, it cannot be used in this form and the amount converted by nitrogen-­‐‑fixing bacteria into a form that can be used by plants is insufficient for their needs. Rocks contain insoluble phosphate, but again this is in a form that is unavailable to most organisms. Though some of the fungi that obtain nutrition as biotrophs from living cells and tissues of other organisms are parasites, many others are mutualists benefiting their partners as well. Lichens are one such group. They are intimate associations between fungi and photosynthetic partners, either cyanobacteria or green algae. The basis of the mutualism is that the photosynthetic partner provides carbon compounds from photosynthesis while the fungus obtains nutrients and water from the air or surface on which it is growing. Lichens are among the most stress-­‐‑tolerant organisms on the planet. While their role as fixers of carbon in most ecosystems is small, they dominate in many extreme environments including on rocks and in hot, dry deserts and the cold deserts of Antarctica, and alpine and arctic tundra. In the latter they cover vast tracts of land where they are without doubt the most important contributors to photosynthesis.7 Biotrophic fungi also form mutualistic associations with the roots of flowering plants and conifers, and with ferns and mosses. Such an association is termed a "ʺmycorrhiza"ʺ from the Greek mykes meaning fungus and rhiza meaning root. Over 90 percent of plants in nature form this intimate association in which, as with lichens, the photosynthesiser provides carbon compounds to the fungus, while the fungus provides water and mineral nutrients and also protection against soil-­‐‑borne root pathogens.8 Also, some mycorrhizal fungi allow some plants to colonise toxic or polluted sites, and can be used to help in land reclamation. In the absence of the fungal partner, nutrients in the vicinity of root hairs – the absorptive part of root cells – are soon completely depleted. Hyphae, which are much more "ʺcost-­‐‑effective"ʺ to produce, extend beyond these zones of nutrient depletion to absorb nutrients (Figure 2). To give some idea of the extent of the absorptive surface produced by fungi, it has been estimated that the column of soil beneath one square metre contains a total length of 16,000 kilometres of hyphae. The fungal partners often have some saprotrophic abilities, and ectomycorrhizal fungi (so called because they typically form a sheath of fungal tissue around the outside of absorptive roots, growing between the outer layers of roots cells but not within them) associated with trees can often short-­‐‑circuit the nitrogen cycle by obtaining nutrients by decomposing dead organic matter, while others (termed arbuscular mycorrhizal fungi by dint of the fact that they produce much branched, dwarf tree-­‐‑like structures for exchange of molecules within plant cells) can additionally release insoluble phosphate from rocks.9 Arbuscular mycorrhizal associations are the most widely distributed both geographically and in terms of host range, including important crop species such as maize (Zea mays), rice (Oryza sativa), soybean (Glycine max) and wheat (Triticum aestivum). Ectomycorrizal associations are the next most abundant – on forest trees, then the association with ericaceous plants. In some relationships "ʺcheaters"ʺ have evolved. 114 Lynne Boddy, Fungi – the unsung heroes of the planet Orchids, for example, with their minute seeds must quickly form a mycorrhizal association when they germinate otherwise they will not survive. Initially the fungal partner not only provides water and mineral nutrients but also sugars, which they obtain from other sources, for example, as saprotrophs from wood decomposition or from trees with which they are simultaneously mycorrhizal. When the orchids start to photosynthesise the normal "ʺsharing"ʺ relationship begins. However, some orchid species do not produce chlorophyll and are unable to photosynthesise, and are effectively parasites. Other plants are "ʺcheaters"ʺ in a similar way, for example, the yellow bird’s-­‐‑nest (Monotropa hypopitys). Figure 2. Mycorrhizal associations between fungi and plants are essential to the success of most plants in the natural environment. The yellow threads are mycelium of a Piloderma species extending from a tree root. © Andy Taylor Not only are mycorrhizal fungi integral to the success of plants on land nowadays, but it was also fungi that allowed plants to colonise land 400-­‐‑500 million years ago.10 Fossilised fungi have been found within cells of the rhizomes of early land plants petrified in rocks laid down 460 million years ago in the Ordovician period. These are identifiable as belonging to arbuscular mycorrhizal fungi, and predate vascular plants with roots. While plants evolving in water would have had little difficulty in absorbing nutrients from the solution in which they were bathed, the move to land would have been hugely problematic because of extremely slow diffusion of nutrients through soil. Association with filamentous fungi solved this. Plants associate with fungi in other ways too. All have symptomless endophytes11 within both their above-­‐‑ground and below-­‐‑ground tissues.12 There is a wide diversity of fungi involved, and these have different ways of spreading between plants and a range of different functions within plants. Though tantalisingly little is yet known about these relations, some certainly confer benefits to the plant, including herbivore deterrents and stress tolerance. They can also influence plant community composition and productivity, and the predators or parasites of the grazers that feed upon them.13 Fungi also have other roles in soil. In particular they contribute significantly to soil microbial biomass, carbon and nutrient storage.14 Their hyphae and exudates stabilise soil particles into aggregates and they convert organic compounds into humus which improves soil structure, and nutrient and water holding capacities.15 When fungi decompose dead organic matter, effectively they burn off carbon and hence concentrate mineral nutrients. Their mycelium and fruit bodies are, therefore, highly nutritious, 115 PAN: Philosophy, Activism, Nature 10, 2013 much more so than plant material. It comes as no surprise, therefore, that a wide range of invertebrates and vertebrates feed on them.16, 17 In fact, many mutualisms have evolved between fungi and animals, some of the best known being those with fungus-­‐‑
gardening ants and termites.18 The basis of the mutualism is that the fungus breaks down organic matter, and part of the nutrient rich fungus is eaten; the invertebrates bring organic matter to the fungus in the nest, control climate and potentially invasive microbes. In contrast, fungal pathogens of invertebrates can act as natural biocontrol agents.19 In addition fungi are used as or used in the production of a wide variety of human food. Eating edible fungi and the reliance on yeast for the production of beer, wine and bread are obvious examples. Less obvious is that Quorn, a meat substitute, is fungus. As well as providing the flavour and texture of blue cheeses, the fungal enzyme chymosin is now used in most commercial cheese production. Citric acid, used in many food products, including most soft drinks is produced commercially by fungi. Fungi also produce important medicines, antibiotics such as penicillin, being most obvious. Statins for control of cholesterol are another fungal product.20 The fascination of studying fungi In view of the foregoing, the need for understanding how fungi function and behave is self-­‐‑evident. Aside from this, I study them because their behaviour is fascinating. The basidiomycetes, many of which produce the familiar mushroom-­‐‑
shaped fruit body, operate aggressive strategies for capturing territory, which can be likened to warfare (Figure 3).21, 22 They employ a variety of different aggressive mechanisms. Some are combative only after contact, perhaps analogous to hand-­‐‑to-­‐‑
hand combat. Others are antagonistic at a distance producing volatile and diffusible compounds that harm their opponent – chemical warfare. The overall outcome between two combative fungi can be: firstly, deadlock, where neither fungus gains territory from the opponent; secondly, replacement, where one fungus wrests territory from the other; thirdly, partial replacement, where one of the fungi takes some of the territory of the other, but then progress ceases, perhaps because the opponent took a while to assemble its defences or because conditions changed altering "ʺthe balance of power"ʺ; finally, mutual replacement, where one fungus replaces the other in one region and the opposite occurs in another area, akin to the movement of cavalry lines in battles of earlier eras. Some species are good at attack, some at defence, some at both, and others at neither. They have a hierarchy of combative ability in which, like in a sports league, those at the top usually beat those at the bottom of the league, but on occasions there are surprises. The victor also depends on climatic conditions and where the encounter is taking place. For example, with some of the decay fungi that can grow out of wood across the surface of soil, victory against a specific competitor may occur when they meet in soil, but not when they meet in wood. When a strong combatant meets several weaker combatants simultaneously, the weakest is usually attacked first – in the human world this is the typical behaviour of bullies! 116 Lynne Boddy, Fungi – the unsung heroes of the planet Figure 3. Fungi are aggressive combatants. The outcome of confrontations can vary, for example depending on the environment. The sulphur tuft fungus (Hypholoma fasciculare) (left) is growing from a beech (Fagus sylvatica) wood block (with sides 2 cm) across the surface of woodland soil compressed into a 24 x 24 cm dish. It has encountered the mycelium of the stinkhorn fungus (Phallus impudicus) growing from the wood block on the top right. In the left image, sulphur tuft mycelium is replacing that of the stinkhorn fungus. In the right image, the opposite is occurring. Those fungi that grow out of resources in search of new food sources exhibit behaviour somewhat analogous to animals.23 When they successfully locate a new resource the mycelium interconnecting the two thickens into a cord-­‐‑like structure, and mycelium from areas not successful in searching out new resources dies back, and the cellular contents are reused (Figure 4). These mycelia cords are "ʺmycological motorways"ʺ or, continuing our warfare analogy, are the supply routes or pipelines from the storage depots to the front. Nutrients are rapidly translocated from the storage sites to locations where they are needed, for example, to enable the fungus to make mycelium and enzymes so that it can colonise new, unexplored territory or for invasion into resources already occupied by another fungus. Figure 4. Fungi respond to new resources. Phanerochaete velutina has grown from a wood beech block across the surface of woodland soil compressed into a 50 x 50 cm tray and encountered four uncolonised wood blocks at the compass points N, E, S and W. (Note that the Perspex blocks in the corners of the trays were simply to support other trays in a stack). Left image: Foraging mycelium has encountered new resources and colonisation is beginning. Centre image: One month after encountering new resources the mycelium is beginning to thin out, and cords interconnecting resources are thickening. Right image: Two months after encountering new resources, only thick cords remain, most of them interconnecting wood resources. Photos by Jon Woods. Conclusions In conclusion, fungi have a multitude of roles in natural ecosystems. However, it is their role as nutrient recyclers and plant feeders, which is of paramount importance to the continued health and functioning of natural ecosystems. With a world population 117 PAN: Philosophy, Activism, Nature 10, 2013 predicted to rise from the current 6.3 billion to 9 billion by 2050, our need for increasing food supplies is obvious. This requires understanding the roles of fungi in ecosystems so that we can manipulate agricultural systems to best effect; understanding mechanisms of fungal spread, evolution and pathogenesis of plants is also essential for reduction of crop losses and post harvest spoilage. Furthermore, fungi are also one of the most likely sources of new antibiotics and other medicines. Notes 1.
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