This chapter deals with fungal co-operative ventures, including ant agriculture, termite gardeners and agriculture in beetles. An important co-evolutionary story is that linking anaerobic fungi, the evolution of grasses and the rise of the ruminants. It is a fascinating story that links with human evolution since humans use cereal grasses as staple foods and selected their main food animals from among the ruminants. Finally, we look at the predatory nematode-trapping fungi.

Fungi have coexisted with animals and plants throughout the whole of the evolutionary time since these three groups of higher organisms originally separated from one another. Living together closely for this length of time has given rise to many co-operative ventures. We have already seen how many fungi have combined with plants as partners in mutually beneficial relationships such as mycorrhizas and lichens. In these symbiotic or mutualistic associations the partners each gain something from the partnership so that the association is more successful than either organism alone. The organisms concerned (often two but sometimes more) live in such close proximity to each other that their cells may intermingle and may even contribute to the formation of joint tissues, as they do in the lichen thallus, which is one of the most ancient mutualistic associations of all and found in some of the most inhospitable environments.

When early humans gave up their nomadic hunter–gatherer existence and turned to agriculture to solve their food problem they would quickly have been challenged by the fungi. Early farmers must have learned very rapidly that crops are very uncertain resources, prone to variations in weather, fire, floods, weeds, insect pests, and those troubles that came to be referred to collectively as ‘blights’ which were due to various sorts of plant disease.

Great plant losses, caused by any of these factors, can be suffered in natural ecosystems but by bringing the crops together into fields in the first place, the early agriculturalists created ideal conditions for the spread of plant disease. And the more selective their farming, the closer their crops came to being true monocultures, the greater the extent of agricultural losses due to any single agency like a particular plant disease, so in this chapter we look at fungi as pathogens of plants.

Fungi are the main disease organisms of plants, being responsible for major losses of world agricultural production. Because of the number that exist, we can only give a few specific examples, so we limit these to the headline crop diseases: the rice blast fungus (Magnaporthe grisea), the bootlace or honey fungus (Armillaria), rusts, mildews and smuts (pathogens that produce haustoria which penetrate the plant cells), leaf spot (Cercospora), Dutch elm disease (Ophiostoma) and black stem rust of wheat (Puccinia graminis).

In Chapter 9 we showed how fungal hyphae are capable of a wide range of cell differentiation, and in other chapters (particularly Chapters 3 and 8) we have mentioned and illustrated some of the variety of multicellular fruiting structures (sexual and asexual) that fungi can produce. It must be evident, therefore, that a fungal mycelium has a number of alternative developmental pathways open to it:

• continuation of hyphal growth

• production of asexual structures

• progress into the sexual cycle.

These are not strict alternatives, because a mycelium of even modest size may express all of these possibilities at the same time, so we can deduce that whatever control of genetic expression is involved must be local.

In this chapter we explain the nature of development and morphogenesis in fungi and the formal terminology of developmental biology. Observations and experiments on fungal developmental biology lead to the conclusion that there are ten ways to make a mushroom, depending on different arrangements of competence and regional patterning. As specific examples we show how the Coprinopsis fruit body makes hymenia, and how Coprinopsis and Volvariella make gills (not forgetting how polypores make tubes). The Coprinopsis fruit body also provides examples of the construction of mushroom stems and the coordination of cell inflation throughout the maturing fruit body; which leads us to consider the mechanics of the mushroom fruit body.

In this chapter we will give you an overview of the organisms that make up Kingdom Fungi. We'll try to emphasise a more ecosystem-oriented approach because we want to avoid rambling taxonomy-driven species lists, but there may be as many as 1.5 million species of fungi currently present on Earth (see below), so we need to know some by name and understand the natural classification of fungi. A natural classification is the arrangement of organisms into groups on the basis of their evolutionary relationships.

To begin with we will describe enough of the taxonomic structure to provide a foundation for understanding the breadth of the group we are studying, and the major phyla that make up the kingdom: Chytridiomycota, Blastocladiomycota, Glomeromycota, Microsporidia (for which see Section 16.2), Zygomycota, Ascomycota and the Basidiomycota. We will then discuss what the word (or, better, concept) ‘species’ means in fungi and the ways in which a fungal species might be defined. In the final sections of the chapter we will examine those fungus-like organisms, which we call the ‘untrue fungi’, and which have some of the characteristics of fungi without being closely related in an evolutionary sense. In our final section we draw a few key aspects about fungi in the natural environment and in their natural communities from this overview of Kingdom Fungi that we will develop more fully in later chapters about ecosystem mycology.

The following classification is adapted from the 9th and 10th editions of The Dictionary of the Fungi (Kirk et al., 2001, 2008), but it has been amended to adopt the phylogenetic arrangement emerging from the AFTOL (Assembling the Fungal Tree of Life) project funded by the US National Science Foundation (visit: http://www.aftol.org/; and see Blackwell et al., 2006), as set out by Hibbett et al. (2007).

The AFTOL project is a work in progress and uncertainties remain about the exact relationships of many groups. These are indicated in the annotated classification below with the abbreviation ‘inc. sed.’, which stands for incertae sedis, meaning ‘of uncertain position’, this being the standard term for a taxonomic group of currently unknown or undefined relationship. Some of the material contained in this section is sourced from the ‘Classification of the fungi’ entry (written by David Moore) in the Encyclopaedia Britannica and is used with permission, by courtesy of Encyclopaedia Britannica, Inc.© 2008.

In this chapter we study fungi as pathogens of animals, including humans. There are many pathogens of insects amongst the fungi and fungus-like organisms: Microsporidia, Trichomycetes, Laboulbeniales and entomogenous fungi. Inevitably, discussion of insect disease eventually turns to thoughts of the potential for biological control of arthropod pests. In other animals, cutaneous chytridiomycosis is an emerging disease of amphibians; so, too, is aspergillosis disease of coral, and both have potential lessons to teach about the emergence of new diseases from organisms that have long, but benign, associations with the host.

Our main concern, though, are the mycoses that are the fungus diseases of humans. We describe the clinical groupings set up for human fungal infections; fungi within the home, and their effects on health through production of allergens and toxins.

In the penultimate section we attempt a comparison of animal and plant pathogens and briefly discuss the essentials of epidemiology. We finish with a short discussion of mycoparasitic and fungicolous fungi; that is, fungi that are pathogenic on other fungi.

Pathogens of insects

Insects are the most diverse group of animals on Earth, occurring in most terrestrial environments, though only a few species are found in marine habitats, as these are dominated by the crustaceans. Over a million species of insects have been described, which is more than half of known living organisms, and taking into account estimates of the number of species that are yet to be described, the Class Insecta probably includes about 90% of all species on the planet.

Wikipedia points out that ‘biodiversity’ is a new portmanteau word made up from ‘biology’ and ‘diversity’ that probably arrived in the English language in 1985. Wikipedia defines ‘biodiversity’ as ‘the variation of taxonomic life forms within a given ecosystem, biome or for the entire Earth. Biodiversity is often used as a measure of the health of biological systems’ (see http://en.wikipedia.org/wiki/Biodiversity). As an aside to this Wikipedia definition of biodiversity: given the fact that in the fossil record fungal biodiversity greatly increases during major extinction events (see Section 2.8) we are not convinced that fungal biodiversity is a good measure of the health of non-fungal biological systems!

In this Chapter 9 we will explain the meaning of the word ‘diversity’ in the context of the fungi, and then deal with its different aspects as they bear upon cells and tissues: mycelial differentiation and the different ways that fungi use for making spores. We describe Aspergillus conidiophores in some detail because something is known about the molecular regulation of Aspergillus sporulation. This is then compared with conidiation in Neurospora crassa. Finally, we make some general points about the nature and construction of fungal tissues and organs by describing conidiomata, and then linear structures like strands, cords, rhizomorphs and stipes; finishing off with the globose structures called sclerotia, stromata, ascomata and basidiomata.

Fungi make crucial contributions to all ecosystems because of their abilities as decomposers. One of the most important kingdom-specific characteristic of fungi is that they obtain their nutrients by external digestion of substrates. In the real world, though there is some digestion of inorganic substrates (see Section 1.7), the bulk of the substrates that fungi recycle are the remains of animals and, most particularly, plants. In this chapter we give an account of the ways in which fungal hyphae obtain, absorb, metabolise, reprocess and redistribute nutrients.

In doing this, fungi obviously contribute to recycling and mineralisation of nutrients and in what follows we will describe the enzyme systems that enable this activity. Our description is relatively brief and more details can be found in the premier text on fungal physiology (Jennings, 2008). For clarity we have to describe separately the enzyme systems involved, and in an order that we have chosen for descriptive purposes. This introduction is intended to convey the impression that for most fungi in most circumstances the initial nutritional step is the excretion of enzymes able to convert polymers to the simple sugars, amino acids, carboxylic acids, purines, pyrimidines, etc., that the cell can absorb. Also, in most circumstances most fungal mycelia will be carrying out all of these biochemical changes simultaneously.

Fungal biomass is a high-quality food source because it contains a good content of protein (typically 20% to 30% crude protein as a percentage of dry matter), which contains all of the amino acids that are essential to human and animal nutrition. Add characteristically low fat content, a chitinous wall as a source of dietary fibre, useful vitamin content, especially of B vitamins, and carbohydrate in the form of glycogen, and fungal biomass can be considered an ideal food. Judging from archaeological and similar finds, mushrooms, toadstools and bracket fungi have been used by humans since before recorded history for both food and medicinal purposes.

We currently depend on fungi and fungal products every hour of every day and this chapter will concentrate on the human fungal foodstuffs in current use (Moore, 2001). However, before turning to this aspect we want to deal with the ways that other animals exploit fungi for food. Fungi feature prominently in food webs, and wild fungi are picked commercially, too. But it's not solely a matter of ‘picking mushrooms’; fungal cells and mycelium are used as human food, and fungi are used to prepare many commonly used fermented foods, so there is a need to consider several different industrial cultivation methods. Finally, to make the point that we are not the only animals that cultivate fungi, we will discuss the relationship between gardening insects and their fungi, though we will describe these mutualisms in detail in Chapter 15.

Although their mode of nutrition is important in defining members of Kingdom Fungi, the fundamental aspect of cell biology that sets the majority of fungi apart from most members of the other major kingdoms is the apical extension of their tubular hyphae. These possess controls which ensure that hyphae normally grow away from one another to form the typical ‘colony’ with an outwardly migrating growing front. Extension growth of the hypha is limited to the apex and this pattern of growth makes the vegetative fungal mycelium an exploratory, invasive organism; and exploration and invasion is the fundamental lifestyle of fungi. This lifestyle allows filamentous fungi to dominate their ecosystems because it gives them the tools they need to find and colonise new substrates rapidly. The success of this growth habit can be judged from the extraordinary diversity of fungal species, their distribution in virtually every habitat on the planet and the parallel evolution of a similar growth strategy by other important soil microorganisms, the prokaryotic streptomycetes and some of the Oomycota in Kingdom Chromista (e.g. Saprolegnia and Achlya).

In this chapter we will discuss the hyphal mode of growth in some detail, explaining how hyphae emerge during spore germination and how hyphae contribute to colony formation. Mycelium growth kinetics is a key topic in understanding the nature of fungi; here we show how that understanding has been built from experiments with living fungi.

The fungal wall can justifiably be described as a sophisticated cell organelle because of the range of functions for which it is responsible.

In this chapter we will discuss the fungal wall as a working organelle, and then consider the fundamental aspects of wall structure, function and architecture. We will describe each of the main components in detail; the chitin component, the glucan and the glycoprotein. Wall synthesis and remodelling is also described, although you should already be aware of some of the mechanisms that may be involved (discussed in Section 5.15) and that the dynamic nature of the fungal cell wall is also mentioned during discussions of hyphal and spore differentiation (Section 9.3), hyphal branching (Section 4.11), septation (Sections 4.12 and 5.17) and hyphal anastomosis (Section 5.16).

In the final two sections of this chapter we give consideration to two aspects that are often overlooked: what happens on the outside of the wall is contemplated in the section entitled ‘On the far side’; and finally we look, briefly, at the fungal wall as a clinical target (although antifungal agents that target the wall are dealt with in detail in Chapter 18).

In this chapter we examine the biotechnology that uses intact living organisms to produce commercially important products. In the main this means fungal fermentations in submerged liquid cultures, so we describe in detail the essential aspects of cultivating fungi: media, oxygen demand and supply, and fermenter engineering. We describe fungal growth patterns in liquid cultures; fermenter growth kinetics; growth yield; the stationary phase; and growth as pellets.

Beyond the batch culture, we discuss fed-batch methods, chemostats and turbidostats. Then we look towards the industrial scene and examine the uses of submerged fermentations, with the specific examples: alcoholic fermentations; citric acid biotechnology; penicillin and other pharmaceuticals; enzymes for fabric conditioning and processing, and food processing; steroids and use of fungi to make chemical transformations; the Quorn™ fermentation and evolution in fermenters; and the production of spores and other inocula. We hark back to ruminant digestion to consider the ‘engineering aspects’ of natural digestive fermentations in herbivores, and try to work out just how many anaerobic fungi we are cultivating in our livestock.

Many of the most important commercial (particularly food) fermentations take place in the solid state. So we look in a little more detail at the digestion of lignocellulosic residues, and then turn to our major foods: bread, cheese and salami manufacture; and soy sauce, tempeh and other food products, with a few comments about products like chocolate, coffee and even tea, which, though few people realise this, all depend on fermentation processes.

Why write a textbook? That's a question we've asked ourselves several times over the past few years; sometimes with exasperation, often in dismay at the mountain of tasks that remained to be completed. The authors have taught a general mycology course in the University of Manchester for many years. From the year 2000 increasing emphasis was given to Internet/Intranet-delivered modules for this course, providing students with yearly-enhanced resources in the form of PDF downloads of lecture notes, PowerPoint presentations as Flash movies, broadcast video and audio files streamed to the registered student end-user, and an extensive resource of reference material provided as full-text PDF for download from the Faculty Intranet. By the 2008/9 session these resources were distilled into a completely new online textbook: the first draft of 21st Century Guidebook to Fungi.

So we didn't actually make a decision to write a textbook; rather it emerged from our everyday (and every year) teaching. For something like 20 years our course portrayed Kingdom Fungi as a major eukaryotic Kingdom in its own right. Fungi have their own unique cell biology, their own unique developmental biology and their own unique lifestyle, and play critical roles in every ecosystem and every food web, and we thought it essential that biology undergraduates should be given the opportunity to understand all this.

In this book we aim to provide a broad understanding of the biology of fungi and the biological systems to which fungi contribute. Our scope ranges from the evolutionary origins of fungi and other eukaryotes more than a billion years ago (though the discussion covers all of time), through to the many contributions that fungi make to our present, everyday, lives. The book provides an all-round view of fungal biology, including ecology, evolution, diversity, cell biology, genetics, biochemistry, molecular biology, biotechnology, genomics and bioinformatics.

Our book emphasises interactions between fungi and other organisms to bring out the functions and behaviours of biological systems:

• we concentrate on integration rather than reduction, which satisfies those who would see systems biology as a paradigm of the scientific method;

• we include computational modelling and bioinformatics for those who view systems biology in terms of operational research protocols;

• and we bring together data about biological systems from diverse interdisciplinary sources.

In this chapter we examine present-day communities; starting with the essential terrestrial habitat and the nature and formation of soil. We emphasise the contributions made by fungi to soil structure and chemistry; and particularly what has come to be called geomycology. We also discuss the diversity of organisms in soil and illustrate interactions between bacteria, amoebae (including slime moulds), fungi, nematodes, microarthropods and larger animals. The origins of agriculture are briefly mentioned and our dependence on fungi illustrated.