Fungi Read online

  Ganoderma applanatum is a white rot fungus with very striking fruit bodies. Its brackets have a brown top and smooth white underside and extend horizontally from trees like bookshelves. The lower surface is perforated with pores that are the open ends of spore-producing tubes. The pores are barely visible without a hand lens. A new layer of tubes grows on the bottom of the bracket each year and some fruit bodies live for years until the tree trunk is completely digested. Ganoderma brackets that are the size of a laptop computer release five trillion (5 × 1012) basidiospores in a growing season from an array of two million tubes. If you crouch below one of these fruit bodies and move your head until the sun casts a beam of light just beneath the white tubes, waves of sparkling spores—fairy dust—can be seen cascading from the bracket. The common name for this fungus is artist’s conk, which refers to the etchings that can be made on the white pore surface using a stylus. In the author’s opinion, collection of this giant fungus to serve the whims of woodland artists should be discouraged. The live fungus on its log is beautiful enough.

  The largest recorded fruit body is produced by another white rot fungus called Phellinus ellipsoideus. This was discovered in 2010 on the underside of an oak log in old-growth tropical woodland on Hainan Island in China. During twenty years of growth, this fungus formed a metre-long crust that weighed 500 kilograms and shed an estimated one trillion spores per day from hundreds of millions of pores.

  White rot fungi include a family of ascomycetes called the Xylariaceae. Daldinia concentrica is a common species in the Xylariaceae. Its fruit bodies are hard black balls that expand each year, like Ganoderma, producing a new layer of tissue on the surface. Young specimens are pea-sized; older ones are the size of walnuts. Common names for this fungus include King Alfred’s cakes, referring to the legendary baking disaster by the distracted Anglo-Saxon monarch, and cramp balls, which describes the supposed value of pocketing the fruit bodies to relieve arthritis pain. Xylaria polymorpha is a related fungus, which is called dead man’s fingers for the resemblance between its black fruit bodies and charred and swollen digits protruding from the ground.

  Brown rot fungi decompose wood in a different fashion by breaking down cellulose without eliminating lignin. Lignin is modified to varying degrees by these fungi, but much of it remains after the cellulose is extracted and gives the powdery remnants of the wood a brown colour. Phylogenetic studies show that this decay mechanism evolved from the white rot form of decomposition. White rot fungi remove the lignin, but do not seem to derive any energy from its breakdown. They are simply clearing the polymer to access the cellulose. The development of the brown rot mechanism of decay, which bypasses lignin decomposition, may be a more efficient way of accessing the energy in cellulose. Brown rot basidiomycetes include Laetiporus sulphureus, sulphur shelf, which forms a bright yellow bracket. This is an edible mushroom that provides a splash of colour in stir-fry recipes. Fomitopsis pinicola, the red-belt conk, is another brown rot fungus that grows on dead conifers. The mycelium of this fungus can also colonize the wounded trunks and broken crowns of old trees causing stem decay. Stem decay produces cavities in large trees that become occupied by birds and mammals. The mechanism of wood decay by ascomycetes is different from rots caused by basidiomycetes and the effects of some of these fungi are described as soft rots rather than white or brown rots.

  Most of the fungi that engage in wood decomposition are filamentous species rather than yeasts. Daldinia concentrica and other ascomycetes fashion a relatively restricted mycelium within decaying wood, but many of the basidiomycetes access dead trees from an expansive mycelium in the soil. The development of a large mycelium allows the fungus to transfer phosphorus and nitrogen from the soil and leaf litter to the sites of wood decomposition. This is vital because the levels of these nutrients in decaying wood are often too low to support growth of saprotrophic fungi. Transmission of water and nutrients across mycelia of some fungi occurs through channels within multicellular structures called cords and rhizomorphs. The term rhizomorph is reserved for the larger of these ‘organs’ that have a distinct rounded tip, like a plant root, that pushes through soil. Cords and rhizomorphs vary in complexity from bundles of hyphae that combine to produce thin cylinders, to fat pipes produced by the coordinated growth of hundreds of thousands of hyphae. Mycelia use cords and rhizomorphs to reallocate water and minerals between locations to optimize growth and decomposition.

  Mycelia of different species of fungi or different strains of the same species compete for access to the cellulose in wood. When the combatants meet in the soil or within rotting timber they attack one another’s hyphae by releasing toxins. These bouts can end with the destruction of one of the contestants, or in a deadlock in which hyphae of both mycelia stop growing in a zone of interference. In dying trees, these interactions are revealed as plates of dead hyphae that blacken with pigmentation. These plates can define territories occupied by a single fungus that runs lengthways along the trunk but is constrained from growing sideways by neighbouring fungi. A single tree can become filled with decay columns formed by interactions between different fungi. No scrap of wood is left alone. The patterns of dark lines in spalted wood are created by this process of mycelial competition. Every decorative bowl turned from spalted wood is a record of internecine warfare.

  Cooperation between mycelia is another common phenomenon among individuals of the same species. This is manifested in the fusion of hyphae and the creation of large networks of hyphae and cords that can explore a wider area of the forest floor in search of food. Because fusion between hyphae in one location does not result in the immediate spread of nuclei of both mating types throughout the whole colony, large mycelia can grow as patchworks of genetic variation. Mycelia can also divide into two or more individuals when, for example, distant sections of a colony become detached from the older part of a mycelium and its mushrooms. All of these processes occur during the lives of the largest fungal colonies, including the enormous mycelia of Armillaria solidipes in Oregon described in Chapter 1.

  Saprotrophic fungi utilize some of the same mechanisms of wood decay in forests to rot timber in buildings. Damage to timber frames in European homes is caused by the dry rot fungus, Serpula lacrymans, and Coniophora puteana, which causes wet rot. Another basidiomycete fungus, Meruliporia incrassata, is responsible for dry rot in the Western United States. The dry rot fungi grow from wet masonry or from soil outside buildings and can transport water and dissolved nutrients to the sites of wood decay through their cords. The cords of Meruliporia can be as fat as a garden hosepipe and grow for several metres. Once a mycelium of a dry rot fungus has colonized a wood beam, it forms long flattened fruit bodies that shed basidiospores into the air. These spores can initiate wood decay in other locations within a building. Wet rot is different because Coniophora shows a preference for growth on wood that is soaked with water. All three species cause the brown rot form of wood decay and are related to boletes whose mushrooms have pores rather than gills.

  Indoor fungi, food spoilage, and decomposition of manufactured products

  Many other saprotrophic fungi grow in buildings on shower curtains, plumbing fittings, and in drains and dishwashers. Diligent cleaning reduces the growth of fungi and other microorganisms in our homes, but they can never be abolished completely. A few of the fungi identified in buildings can cause serious illnesses, but it is important to recognize that their spores are common, if not ubiquitous, in the outdoor air. This means that the indoor environment does not pose any special danger. Ascomycetes are the commonest of the indoor fungi. When buildings are flooded, they grow on a wide range of surfaces including wallpaper and drywall, carpeting, and furniture. Under these circumstances fungal growth can cover large areas and produce high concentrations of spores in the indoor air. Spores carry proteins on their surface that can cause allergic responses that can be a serious problem for asthmatics. Allergies to fungi are featured in Chapter 7.

  Saprotrophs also cause food spoila
ge in our homes, rotting fresh fruits and vegetables, and putrefying dairy and meat products. Species of the ascomycete Penicillium cause blue and green moulds of citrus fruits, blue mould of apples and pears, and spoil cheeses that are kept too long in a refrigerator. There is an irony with cheese spoilage because blue cheeses are flavoured by the growth of Penicillium species that differ from those associated with spoilage (Chapter 8). Penicillium is also responsible for the blue colonies that develop on mouldy bread. Black bread mould is caused by Rhizopus stolonifer, which is a zygomycete. The black dots that speckle the spoiled bread are sporangia filled with asexual spores. With a hand lens the sporangia are visible at the top of translucent stalks that project from the surface of the mycelium.

  Other common ascomycetes that cause food spoilage are species of Aspergillus and Alternaria. Aspergillus niger contaminates baked goods, dairy products, and fruit juices. Alternaria alternata produces dark spots on tomatoes and other fruits and vegetables. Some of the fungi that cause food spoilage produce toxins, called mycotoxins, which can pose food safety concerns. Aflatoxins produced by Aspergillus flavus and Aspergillus parasiticus are the most significant mycotoxins from the perspective of human health. These cancer-causing compounds can reach potentially dangerous levels in cereals, peanuts, and other crops stored under hot, humid conditions. They can also be found in milk from cows that have eaten contaminated cattle feed.

  More surprising than food spoilage is the growth of saprotrophic fungi on oil-based products. Hormoconis resinae is a filamentous ascomycete that can decompose hydrocarbons in aviation fuel. The fungus, accompanied with bacteria, grows at the interface between water droplets and the hydrocarbons in fuel. This microbial community damages rubber and plastic components in fuel systems and causes corrosion of the metal parts through the release of acidic compounds. Fuel contamination can also clog filters and damage fuel pumps. The problem was identified in the 1960s, when investigators found the fungus in a high percentage of several types of military and commercial aircraft. A solution came from the discovery that anti-icing fuel additives inhibited the growth of Hormoconis. These compounds are standard components of fuel used in aircraft today. Hormoconis is also known as the creosote fungus for its ability to grow on this toxic wood preservative. Neolentinus lepideus is another creosote-tolerant fungus. This species is a basidiomycete that forms mushrooms with scaly caps. It is called the train wrecker for its growth on old railway sleepers (ties), but there is no evidence that it has caused any accidents.

  Compared with these acts of metabolic virtuosity, fungal damage to books seems rather facile. After all, most paper is made from wood pulp. Fungi grow on the page edges of closed books and are responsible for some of the foxing stains visible on open pages. Prints and paintings are also vulnerable to spoilage by fungi. These alarming phenomena are controlled by maintaining low humidity in libraries and museums. Tiny fungal colonies spot the emulsion on the surface of old photographic slides and their filamentous nature is apparent when they are magnified by projection. This anecdote may not make much sense to younger readers, but it provides another example of the relentless growth of fungi on man-made products.

  Global significance of saprotrophic fungi

  The global significance of saprotrophic fungi is apparent when we consider their overall contribution to the carbon cycle. Lignocellulose decomposition is the largest source of CO2 emissions, exceeding the quantity of CO2 released by burning fossil fuels by a factor of ten. This statistic does not diminish the importance of fossil fuel consumption in the modern disturbance of atmospheric chemistry. The release of CO2 from decomposition has always been balanced by the uptake of the gas by plants and photosynthetic microbes. The consumption of ancient deposits of coal, oil, and gas since the industrial revolution, and at an accelerating pace, has provided a new source of CO2 that is poorly accommodated by the natural carbon cycle. It is responsible for the 25 per cent increase in atmospheric CO2 levels in the last fifty years.

  The largest coal deposits were formed in the Carboniferous Period (360–290 million years ago), with the burial of immense quantities of the woody tissues of giant clubmosses, horsetails, and seed ferns that flourished in tropical wetland forests. An intriguing explanation for the fossilization of these plants is that the white rot fungi capable of destroying their remains did not evolve until the end of the Carboniferous. According to genetic investigations using a molecular clock calibrated with fossils (Chapter 1), there was a lag between the evolution of woody plants and the emergence of fungi that could decompose them. The first mycelia that secreted lignin-degrading enzymes enjoyed an abundance of food in the coal forests and their success is written in the decline in coal formation in the Permian Period. No other organisms have ever mastered the chemistry of lignin breakdown. We turn in Chapter 7 to fungi that feed on the less resilient tissues of the human body.

  Chapter 7

  Fungi in animal health and disease

  Our microbiome

  Yeasts are budding in the sebaceous oil on your scalp as you read this chapter. Fungi are growing on other parts of your skin too and in your mouth and nasal passages. They are thriving in the openings from your reproductive, urinary, and digestive systems, and they live in astonishing numbers inside your gut. These fungi that live on and inside us are part of the galaxy of microorganisms called the human microbiome. We interact with fungi in a more casual way too, by inhaling their spores from first breath to last gasp. Most of our associations with fungi cause no problems and some of them support our well-being. These harmless or supportive relationships can be upset, however, when the skin is damaged by a severe burn or if fungi are introduced into the body during surgery. Serious fungal diseases or ‘mycoses’ also develop when our immune defences are weakened by viruses, immune therapy after an organ transplantation, or by cancer treatments. The resulting infections can be difficult to treat. This chapter considers the fungi that populate the healthy human microbiome and the nature of fungal infections. We will also look at mushroom poisoning, and the effects of magic mushrooms on perception.

  Skin and hair

  The scalp offers food for fungi in the form of sebum, which is the fatty secretion from hair follicles, and keratin in hair and skin flakes. Metagenomic studies show that species of Malassezia are the dominant fungi on our heads, torso, and arms, and in our ears and noses. These yeasts are harmless residents and they probably help us by controlling the growth of other microorganisms. Our relationship with Malassezia is secured by the dependence of the fungus on fatty acid molecules in sebum. Other fungi manufacture their own fatty acids, but Malassezia lacks the enzyme that strings together small molecules into these storage fats. Malassezia causes dandruff and a more extreme inflammatory condition called seborrhoeic dermatitis. Both skin conditions can be treated with simple antifungal compounds containing zinc or selenium. Malassezia can also block skin follicles causing more widespread skin irritation and is responsible for pityriasis, displayed as a rash of discoloured skin patches.

  Other kinds of skin disease are caused by filamentous fungi rather than yeasts. Ringworm is an umbrella term for superficial infections caused by dermatophytes. Dermatophytes are ascomycetes that invade skin, hair, and nails, breaking down keratin and triggering inflammation. The hyphae of dermatophytes grow in the outer layer of the skin where they feed on dead skin cells and rarely penetrate deeper layers. Trichophyton species are the commonest dermatophytes. In athlete’s foot their colonies grow between the toes and can spread over the skin on the top and bottom of the foot in severe cases. On the scalp, hyphae invade the hair shaft and feed on the keratin filaments. When the fungus produces its spores, the hair shaft bursts and breaks off at the base leaving a black dot in the empty follicle. Ringworm occurs on other parts of the body and all of these infections are contagious, spreading from person to person via spores.

  The cause of ringworm was not recognized until the 19th century when Robert Remak, a Polish investigator, examined infected skin cr
usts with a microscope and observed oval bodies (spores) and connecting threads (hyphae). He went on to use himself as an experimental animal by sticking an infected skin crust to his forearm. After two weeks, he developed an active skin infection that contained fungal cells. This act of self-sacrifice went a long way towards proving that ringworm was caused by a fungus. It is interesting that Remak’s conclusions were published in the 1840s, predating Louis Pasteur’s experiments on the Germ Theory of Disease by twenty years. But Remak was not the first scientist to demonstrate the causal link between microorganisms and disease. This honour goes to a French investigator, Bénédict Prévost, who published a series of radical experiments in 1807 showing that the smut fungus, Tilletia caries, causes ‘bunt’ or ‘stinking smut’ of wheat.