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  8. Spirodactylon aureum, a zygomycete fungus that grows on rodent dung and forms its spores on stalks with a spectacular coiled structure. The fungus is shown in a variety of magnifications in this illustration. The spores are formed within the coils and are exposed in the drawing at bottom left.

  9. The artillery fungus, Sphaerobolus stellatus, sliced through the centre to show the multiple tissue layers. (Left) unopened fruit body; (middle) open fruit body with black capsule bathed in fluid within cup; and (right) capsule jettisoned from triggered cup.

  The most complex species of the trio is Sphaerobolus stellatus, which has the common name of artillery fungus (Figure 9). Its closest relatives produce earth-stars and phallic mushrooms which will be described shortly. Colonies of Sphaerobolus feed on herbivore dung, mulch, and wet wood chips, and make spherical fruit bodies with a diameter of two millimetres. The anatomy of these little white beads is exceedingly complex. The centre of the fruit body is occupied by a capsule that contains ten million spores. A jacket made from six layers of interwoven hyphae surrounds the capsule and the whole structure looks like a tiny Scotch egg. When the fruit body is mature, the outer layers of the jacket peel open, separate into two cups, and hold the exposed capsule in the centre. Swelling of cells in the inner cup produces a compressive stress which is relieved when this elastic membrane flips outward with an audible ‘pop’, propelling the capsule into the air over a distance of up to six metres.

  The largest structures produced by Olpidium are its thalli inside the cabbage roots. These can be seen with the low-power objective lens of a microscope providing a 100-fold (100×) magnification. The stalks of Spirodactylon are visible with the naked eye, but none of their intricate structure can be seen without a microscope. The fruit bodies of the artillery fungus can be spotted on the ground, and the magnification provided by a 10× hand lens (magnifying loupe) is sufficient to see the glistening capsule bathed in the fluid of the open cup. A microscope is needed to see the multilayered structure of the jacket and the spores inside the capsule. Light microscopes with magnifications between 100× and 1,000× are essential for studies on fungi and can be used to look at living cells. Electron microscopes provide considerably higher magnifications of dead specimens that are placed in a vacuum and bombarded with electrons.

  Classifying fungi

  Until quite recently, the visible characteristics of the fungi served as the only guide to identifying species and for sorting them into different groups. Long before scientists became interested in developing a formal system of fungal classification, illustrated studies of mushrooms were published with the aim of separating poisonous and edible species. Carolus Clusius authored the first detailed study of mushrooms in 1601. His work was extended by a Flemish priest, Franciscus van Sterbeeck, in a very influential book, titled Theatrum Fungorum, published in 1675. Later scholars separated mushrooms by differences in shape, size, and colour and the first schemes for classification assigned these putative species into groups with gills, pores, or teeth beneath their caps.

  In the 19th century, Swedish mycologist Elias Magnus Fries produced a novel system of classification that concentrated upon the colour of spores. Rather than looking at the spores with a microscope, Fries scrutinized ‘spore prints’ that accumulate when a mushroom cap is placed gills downward on a piece of paper. After Darwin elucidated the mechanism of evolution, mycologists, and other biologists, attempted to create natural systems of classification in which groups of species are related by descent from a common ancestor. It turns out that mushroom shape, size, and colour are poor guides for natural classification.

  As we saw in Chapter 1, genetic comparisons are used to tease apart the largest lineages of organisms into supergroups (e.g. Opisthokonta) and kingdoms (e.g. Fungi and Animalia). The sequences of genes also serve as the most objective guide for identifying individual species and unravelling evolutionary relationships between species. The term ‘taxonomy’ describes the identification and naming of organisms and ‘systematics’ refers to the particular study of evolutionary relationships among organisms. The fragment of the complete set of genetic instructions of a fungus that is sequenced for these evolutionary studies is called the ITS region, where ITS stands for Internal Transcribed Spacer. ITS is a region of the gene that encodes part of a cell structure called the ribosome. Ribosomes are the molecular machines that carry out protein synthesis. They are about one million times smaller than cells: a single yeast cell contains 200,000 ribosomes. Mycologists who specialize in the study of fungal systematics amplify all or part of the ITS region from fungi, determine their sequences, and compare the sequences among different fungi to determine their similarity. The ITS region has proven so useful for identifying fungi that the sequence is used in diagnostic kits for the rapid detection of fungi causing human infections, plant disease, and contamination of water-damaged buildings.

  Data produced by genetic comparisons is used to construct evolutionary or phylogenetic trees that display relationships between organisms in the form of branching diagrams. Phylogenetic trees are used as a guide for making sensible decisions about grouping species into a Genus, genera into a Family, families into an Order, and orders into a Class (Table 1).

  Table 1. Taxonomy of three fungal species

  With each step up in this hierarchy of names, we are dealing with greater genetic variation. Related classes are arranged into a Phylum and this is a convenient level for further consideration of the modern classification of the Kingdom Fungi (Table 2). There are some disagreements about the number of phyla and this organization of species is likely to change as more fungi are discovered and more detailed genetic research is completed.

  More than 90 per cent of the more than 70,000 species of fungi that have been described by mycologists are classified within Phylum Basidiomycota (basidiomycetes) and Phylum Ascomycota (ascomycetes). Half of the basidiomycetes produce mushrooms; the others include rusts and smuts that cause plant disease, and a plethora of single-celled yeasts. Ascomycetes include the yeast Saccharomyces cerevisiae, fungi with beautiful cup-shaped fruit bodies, truffles, and morels. Basidiomycetes produce basidiospores and ascomycetes produce ascospores (Figure 10). The number of technical terms used to describe fungi can be an impediment to learning about them. An imposing book titled The Dictionary of the Fungi has been published since the 1940s and lists 21,000 names of fungi and terms that describe their structure. Reliance on this terminology is as limited as possible in this short book without compromising the accuracy of the science.

  Table 2. Major groups or phyla of fungi

  Phylum Common name Examples

  Basidiomycota mushrooms gilled mushrooms, boletes, bracket fungi, jelly fungi, artillery fungus

  Ascomycota cup fungi morels, truffles, baker’s yeast, moulds (Aspergillus, Penicillium)

  Glomeromycota arbuscular mycorrhizal fungi Glomus species

  Zygomycota (informal) bread moulds Mucor, Rhizopus, Spirodactylon

  Chytridiomycota chytrids Batrachochytrium (frog pathogen)

  Blastocladiomycota no common name Allomyces

  Neocallimastigomycota anaerobic rumen fungi Neocallimastix

  Cryptomycota hidden fungi Rozella

  Mushrooms and related fungi

  The apparent stillness of a mushroom belies furious microscopic activity beneath its cap. Gill development provides a mushroom with a twenty-fold larger surface area for spore production than a flat disc of the same diameter. Cells that produce spores are packed on to the gill surface and each spore is launched into the space between neighbouring gills by the motion of a tiny droplet of fluid. This intricate discharge mechanism, called a surface tension catapult, can be observed using a high-speed video camera attached to a microscope. Frame-by-frame viewing of videos captured at 100,000 frames per second shows that the fluid drop slaps on to the spore, sending spore and drop flying from the gills (Figure 11). This happens tens of thousands of times every second, allowing a big mushroom to release three billion s
pores in a day. Large bracket fungi, which are also basidiomycetes, can release trillions of spores every year amounting to a weight of one kilogram.

  10. Fruit bodies of (left) an ascomycete cup fungus and (right) a mushroom-forming basidiomycete. The cup fungus discharges ascospores from multiple asci in synchrony producing a vertical puff. The mushroom discharges basidiospores from its gills, which fall from the cap and are dispersed by wind.

  11. Basidiospore discharge shown in successive images from high-speed video recording captured at 100,000 frames per second. The fluid droplet at the base of the spore in the first frame coalesces with fluid on the adjacent spore surface in the second frame, which makes the spore jump into the air at an acceleration of 10,000 g.

  Umbrella-shaped mushrooms with gills are a common type of basidiomycete fruit body that has developed many times during the evolutionary history of this group of fungi. The repeated emergence of the same basic structure is an example of convergent evolution. This is probably explained by the efficiency of this architecture. Growth of a mushroom draws upon the resources of a large volume of filamentous hyphae that are feeding in the surrounding soil or rotting wood. The development of a mushroom from the colony is an investment in the future of the genes carried by the clouds of spores that will be shed from its gills.

  Mushroom stems and caps are fashioned by millions of branching hyphae. The elongation of the stem allows a fruit body to poke a few centimetres above the ground, or to sprout from a tree, placing the gills in a perfect position for misting the air with spores. Cap formation is also important because it protects the gills from raindrops that would sabotage the mechanism of spore discharge. Given the energy consumed in making a mushroom, it makes sense to release as many spores as possible. Alternatives to gilled mushrooms include fruit bodies with pendulous spines (Hydnum repandum, the hedgehog mushroom, is an example), and others with tightly packed tubes (boletes like the edible cep or porcini produce these ‘poroid’ mushrooms). A variety of basidiomycetes dispense with the protection offered by a cap and release their spores from exposed surfaces when it is not raining. These include coral fungi, with fruit bodies that look like tiny candelabra, jelly fungi, which look like jelly, and various species that form flat crusts on tree bark.

  Wind dispersal of spores from mushrooms is limited to short distances in sheltered locations and insects are thought to assist in spreading spores of some species. Spores stick to the bodies of insects that feed on mushrooms and are carried in their guts. A bioluminescent mushroom species that grows in the Brazilian rainforest lures insects by emitting green light during darkness. This was demonstrated by experiments using acrylic models of fruit bodies illuminated with green light-emitting diodes. It is not known whether other bioluminescent mushrooms work in this fashion, but insect dispersal is probably important for luminescent and non-luminescent mushrooms.

  An assortment of basidiomycetes have abandoned ‘active’ spore discharge entirely in favour of splash discharge by raindrops and dispersal by insects and other animals. Earth-stars form lovely fruit bodies that enclose spores in round bags that are held above the ground on star-shaped platforms. The bags are compressed by raindrops, expelling a jet of spores through a nozzle at the top. After release, the spores drift away on the breeze. Puffballs and earth-balls work in a similar fashion, although some of them split apart and release spores without using a nozzle to concentrate and accelerate their emissions. The giant puffball, Calvatia gigantea, is the most fecund of fruit bodies, with the largest specimens holding an estimated seven trillion spores. Arranged in a line, these ‘dust’ particles would ring the equator.

  Bird’s nest fungi produce very elaborate fruit bodies (Figure 12). These basidiomycetes house their spores inside capsules that nestle in their small cup-shaped fruit bodies. Looking from above, the capsules look like eggs in a nest. Each bird’s nest capsule is bigger (2 mm or more in diameter) than the single capsule discharged by the artillery fungus (less than 1 mm in diameter). The fruit bodies direct falling raindrops into the bottom of the nest, splashing their capsules into the air over a distance of up to one metre. Some species have a cable attached to each capsule that operates as a grabline, attaching the capsules to plant stalks as they fly from the fruit body. This tethering mechanism increases the chance that the capsules will be consumed by herbivores that graze around the bird’s nest fungi. After passage through the gut of the animal, the 100 million spores inside each capsule will be deposited in dung that serves as a fertilizer for the development of a new mycelium.

  12. Structure of the fruit body of the bird’s nest fungus Cyathus striatus. The interior of the fruit body is shown in this illustration to reveal the capsules before they are splashed from the cup. A single capsule is shown on the right with a fully extended grabline.

  Stinkhorns are stranger still. The common stinkhorn, Phallus impudicus, is shaped like an erect human penis and attracts flies to the stinking olive-green slime that covers its head. It emerges from a buried ‘egg’ that looks like a golf ball. The basidiospores of this fantastic organism are embedded in the slime, so that insects consuming the slime transport the spores when they fly away. This reproductive behaviour is comparable to the use of the odour of rotting flesh by corpse flowers to attract the scavenging flies and beetles that act as their pollinators. Relatives of the common stinkhorn form thin red stalks tipped with slime (dog stinkhorn), hang a white network beneath the head that looks like a skirt (veiled stinkhorn), and spread their slime over the ‘bars’ of cages (latticed stinkhorn) and the ‘arms’ of red stars (starfish fungus). Each of these odd structures emerges from its egg stage in a few hours by absorbing water. This rapid inflation mechanism is seen to a greater or lesser extent in other mushrooms and accounts for the sudden appearance of fungi that people find so surprising.

  Molecular phylogenetic research shows that earth-stars, puffballs, earth-balls, bird’s nest fungi, and stinkhorns evolved within different groups of mushrooms with gills and tubes beneath their caps. The loss of the active mechanism of spore discharge was a critical step in this process. The effectiveness of these alternative strategies for spore dispersal is evident from the discovery of fossil representatives of earth-stars and bird’s nest fungi which are tens of millions of years old.

  The rusts and smuts are classified as separate subgroups of the basidiomycetes. Similarities in cell structure between rusts and smuts and the mushroom-forming species unite them within the basidiomycetes. Their evolutionary ties are also apparent from their use of the droplet mechanism of spore discharge. Rusts are specialized plant parasites that attack a wide range of plants including wheat, coffee, and other critical agricultural species. Smuts infect the reproductive organs of flowering plants. In loose smut of barley, for example, a smut fungus infects the open flowers and the damaged flower heads fill with masses of black spores rather than seeds.

  Ascomycetes and other groups

  With a few exceptions, ascomycetes are overlooked more easily than basidiomycete mushrooms. With the exception of morels, truffles, and a handful of rarer species, the beauty of ascomycete fruit bodies is invisible without the aid of a hand lens. The inconspicuous nature of these fungi is no excuse for ignoring them. Ascomycetes are the most important pathogens of plants, cause food spoilage, are a major cause of human allergies, and include the yeast that is our dependable workmate in biotechnology. And, outside the most polluted cities, we see ascomycete colonies everywhere in the form of the fungal components of lichens.

  The ascospores of ascomycetes are formed inside cells called asci. Lacking the drop mechanism of spore discharge used by basidiomycetes, many ascomycetes shoot their spores from asci that operate as pressurized cannons. Ascospore discharge is one of the fastest movements in nature, with a record speed of 100 kilometres per hour, measured using a high-speed video camera running at one million frames per second (Figure 13).

  13. Ascospore discharge in Ascobolus immersus whose asci open via a lid. The spores of this
fungus are connected by mucilage and the whole mass is shot at a speed of 65 kilometres per hour. The fastest of the ascomycetes propel their spores at speeds of up to 100 kilometres per hour.

  Some ascomycetes produce ‘naked’ asci. Taphrina deformans, that causes leaf curl disease in fruit trees, spreads itself from asci that break through the surface of infected leaves and spray their spores into the air. Ascomycetes in the genus Dipodascus form long asci on surfaces and exude their spores through the expansion of mucilage within the ascus. And hundreds of species of ascomycete yeasts transform their single cells into asci and spill their ascospores when the walls of their asci dissolve. But the common name of the phylum, the ‘cup fungi’, refers to a type of ascomycete fruit body called an apothecium.

  Apothecia range in size from tiny blue discs of the bluestain fungus, Chlorociboria, and red discs of the eyelash cup fungus, Scutellinia scutellata, to the pale brown pig’s ear fungus, Peziza badia, that can grow as big as a cereal bowl. The fruit bodies of edible morels and toxic false morels are examples of big apothecia that are pushed into the air on stems like basidiomycete mushrooms. Truffles are modified apothecia whose exposed surfaces have become enclosed during the evolutionary history of these fungi. They form below ground where they use pheromones to attract mammals that consume the fruit bodies and disperse the ascospores in their dung. Other kinds of ascomycete fruit body develop as tiny flasks (perithecia) and balls (cleistothecia). Neurospora crassa is a perithecial ascomycete that is a favourite for cell biological research, and species of Aspergillus produce cleistothecia.