Fungi Read online

  3. Scanning electron microscope images of (top) yeast cells of Saccharomyces cerevisiae, and (bottom) filamentous hyphae of Aspergillus niger.

  The beautiful coordination of these cell mechanisms is apparent to anyone watching a hypha grow under a microscope. At high magnification, the tip of a hypha appears to extend at a constant speed while vesicles and other structures whirl around inside the cell. Some sense can be made of this confusing picture using fluorescent dyes linked to antibodies that attach to specific cell proteins. These dyes allow investigators to study the distribution and mobility of nuclei, mitochondria, vacuoles, and the cytoskeleton. One hyphal structure that has been studied for many decades is a cluster of vesicles at the tip of growing cells called the Spitzenkörper, or dark body (Figure 4). The position of this organelle corresponds to the direction of hyphal extension and experiments suggest that its movement controls growth.

  4. Diagram showing the interior of a hyphal tip packed with vesicles that form a structure called the Spitzenkörper whose position governs the direction of growth.

  As hyphae elongate they form branches, creating an interconnected web of cells that expands at its edge (Figure 5). This is the fungal colony or ‘mycelium’, whose circular shape is manifested in the fairy rings of mushrooms and in the disc shape of skin infections caused by ringworm fungi. The expanding mycelium digests materials in its path and uses turgor pressure to push aside obstacles and penetrate solid food. When hyphae encounter sand grains and other hard objects they grow around them and produce branches to explore alternative routes. Rather than sensing traces of chemicals diffusing from potential food materials, mycelia spread outwards in all directions until they strike digestible objects. When this happens, the colony reacts by redirecting growth towards these locations.

  5. Young colony or mycelium of a fungus that has grown outwards from a single spore at the centre of the drawing.

  Hyphae form a continuum of filaments throughout the colony. This interconnected structure allows a mycelium to be highly responsive to the distribution of food in its environment. There is, however, a potential weakness in this organization. Without an efficient repair mechanism, damage to the mycelium in one place—caused by a browsing snail, for example—would affect the whole colony through the rapid loss of turgor pressure as cytoplasm oozed into the soil. This apparent architectural flaw has been countered by the evolution of an elegant substructure to the mycelium. Most fungi produce partitions or septa along their hyphae that divide each cylinder into compartments. Each septum has a closable hole in the middle allowing cytoplasm to flow from one compartment to the next. In one group of fungi, called basidiomycetes, the septa are surrounded with caps formed from perforated membranes. These regulate the passage of organelles along the hyphae, acting as sieves through which larger structures are excluded. And, when damage occurs to one part of the colony, septa on either side of the wound are sealed by the membrane caps to localize ‘bleeding’.

  The succession of compartments that forms the mycelium is regarded as a multicellular structure. Individual hyphal compartments of some fungi contain single nuclei, but other fungi have multiple nuclei in each compartment. This version of multicellularity is unique to the fungi. Some fungi do not form septa along their growing hyphae and develop, instead, as a fluid-filled continuum of cylindrical cells containing multiple nuclei. In these fungi the entire colony is regarded as a single multinucleate cell, also known as a coenocyte.

  The second common growth form of fungi is the yeast. This alternative cell type has a rounded shape and reproduces by forming buds on its surface. Hundreds of species of fungi grow in this fashion and are referred to as yeasts. The noun ‘yeast’ is also used in a narrower sense as the common name for a single fungal species, Saccharomyces cerevisiae, which is used in baking, brewing, and winemaking. Yeasts tend to flourish in fluids rich in nutrients, but they also grow on wet surfaces where they form gooey blobs of multiple cells. Most fungi are aerobes, meaning that they require oxygen to support the respiratory reactions that release energy from their food. Oxygen can become limiting for yeasts submerged in fluid and this stimulates fermentation reactions that release energy from nutrients under anaerobic (oxygen free) conditions. Fermentation is the process that generates alcohol in brewing and winemaking. Many of the fungi that grow on human skin and are found in our guts are yeasts. Candida albicans is a yeast that normally grows in the mouth, vaginal tract, and colon without causing any illness. It causes oral thrush in babies and vaginal irritation in adults when antibiotics upset the normal balance of microorganisms. Candida can also produce serious infections when the immune system is weakened.

  A typical yeast cell is 0.003 to 0.004 millimetres (3 to 4 μm) in diameter, which is three times wider than a bacterium and half the size of a red blood cell. Fungal hyphae vary a lot in width, but most are around the same width as a yeast cell. Hyphae are visible as white threads when they grow in bundles (underneath a plant pot is a good place to look), but a microscope is needed to see an individual hypha or a yeast. This is the reason that we refer to fungi as microorganisms, even though their fruit bodies can be huge. Popular references to fungi as the largest and oldest organisms are based on the estimated size of mycelia of Armillaria solidipes, a ‘honey fungus’ that grows in forest soil and attacks conifers. The current champion has spread over ten square kilometres in Oregon in the last 2,400 years and may weigh as much as 35,000 tons. The largest umbrella shaped mushrooms have a cap diameter of one metre and are produced by colonies of fungi cultivated by termites in Africa and leaf-cutter ants in Central America. Most fungi are microscopic throughout their lives, forming tiny colonies that become dusted with spores.

  The inconspicuous nature of most fungi is one of the reasons that we know so little about them compared with animals and plants. Most of the classical work in mycology concerned mushrooms and there was little attention to the development of the colonies that supported the fruit bodies. The introduction of culture techniques in the 19th century placed the science of mycology on a stronger scientific footing and a great deal was learned from experiments on a small number of species that could be grown easily in the laboratory. Studies on the fine structure of fungal cells using electron microscopy produced a wealth of information on growth mechanisms and cell division in the 1970s, and this work was extended through molecular genetic experimentation beginning in the 1980s.

  The emerging molecular techniques were also applied to the study of phylogeny at this time and today’s fungal biology is informed by the increasingly sophisticated methods for sequencing and characterizing genes. Using modern ‘metagenomic’ methods, for example, investigators are extracting and characterizing genes from the environment without growing fungi in culture. A new group of fungi, called the Cryptomycota, was discovered with these methods in 2011. The genes of these microorganisms have been identified in pond water, soils, marine sediments, and even in chlorinated drinking water. They appear to embrace more genetic diversity than all of the groups of fungi known previously, but almost nothing is known about their biology beyond the fact that they form motile zoospores.

  The diversity evident in today’s fungi has arisen through processes of evolutionary change across the hundreds of billions of generations of fungi that have lived and died since the Precambrian. Sexual reproduction is widespread in the fungi but unknown in some groups. Natural cloning of fungi occurs when a nucleus divides by the process of mitosis and copies of the nucleus are packaged into spores. These asexual spores formed by mitosis are called conidia. Mutations in the genes carried inside conidia are a major source of the variation with which evolution operates and asexual or ‘parasexual’ mechanisms of genetic recombination produce additional novelties. Sexual reproduction occurs when mycelia of two strains of a fungus fuse with each other. Many fungi reproduce asexually and sexually, developing two or more kinds of spore depending upon the method of reproduction.

  Fungal ecology

  Fungi engage in
all manner of close biological associations with other organisms. The scientific term for these interactions is symbiosis and they include relationships that appear to benefit both contributors (mutualism) and interactions in which one participant benefits at the expense of the other (parasitism). Fungal mutualisms include a range of physical connections with plant roots called mycorrhizas, including the arbuscular type preserved in the Ordovician fossil record. Lichens are another kind of fungal mutualism in which the cells of a photosynthetic microorganism—either a cyanobacterium or a single-celled eukaryotic green alga—are embedded in a lattice of fungal hyphae. Thousands of species of fungi form lichens in collaboration with a small number of photosynthetic partners. Fungal mutualisms with animals include symbioses that form inside the guts of invertebrates and vertebrates. Relatively little is known about these interactions, but the fungi participate in the breakdown of food within the digestive system of their hosts. Bucking the aerobic nature of most fungi, species of strictly anaerobic fungi live in the guts of herbivores where they digest plant fibre. Other kinds of fungi live in the human gut where they are thought to interact with resident bacteria and archaea in the metabolism of sugars.

  Fungi are the most important cause of plant disease and are responsible for billions of dollars of crop losses every year. In some of these infections, the fungus feeds on living tissues without killing the plant. Other fungi begin by killing plant cells and feed on their dead contents. In a third disease category, the fungus employs both strategies by minimizing damage to the living plant in the early phases of infection and switching to more destructive behaviour later. All of these fungi can be described as plant parasites or as pathogens. There is some disagreement about the difference between parasites or pathogens, but these terms are usually interchangeable when we refer to fungi that cause disease. Epidemic fungal diseases of trees and staple crops have affected us throughout history, but even the least conspicuous plant is plagued by pathogenic fungi.

  The Irish potato famine of the 1840s is often attributed to the spread of the potato blight ‘fungus’ Phytophthora infestans. This pathogen is not a fungus; it is a species of water mould more closely related to giant kelps and other brown algae than it is to mushrooms and yeasts. Nevertheless, water moulds have been studied by mycologists because they form hyphae that resemble the cells of fungal mycelia. Indeed, water moulds meet the functional definition of fungi as eukaryotes that feed by absorption and reproduce by spore formation. Biologists separate them from fungi on the basis of numerous differences in cell structure and genetics, which show that their resemblance is an example of evolutionary convergence, comparable to the formation of wings by birds and bats.

  Fungi decompose plant tissues in forests and grasslands. They produce enzymes that catalyse the breakdown of lignin polymers that strengthen wood. Other fungi decompose plant tissues in rivers and lakes and produce spores beneath the water that attach to submerged leaves. Breakdown of partly digested plant tissues in herbivore dung is another fungal activity that is a critical process in the carbon cycle. Dispersal of these coprophilous fungi once the nutrients in the dung are exhausted requires the escape of their spores, passage through an animal, and deposition in a fresh deposit of faeces. Evolutionary solutions to this considerable challenge have produced gorgeous contraptions for discharging spores, including the squirt gun of Pilobolus that launches a capsule filled with 90,000 spores at a speed of 32 kilometres per hour over a distance of 2.5 metres (Figure 6). Scaled to human dimensions, this is equivalent to a nine-kilometre flight!

  Some fungal pathogens of plants and wood decomposers may be exclusive vegetarians, but most fungi are very effective at breaking down animal proteins when they are fed them in the laboratory. This omnivory is reflected in the observation that a great variety of fungi are capable of infecting the tissues of animals with weakened immune systems. Infections of this kind are called opportunistic and, in rare cases, even involve fungi that form mushrooms. More prevalent fungal infections are also opportunistic, but they are established by species that show particular adaptations to combating the remaining host defences and colonizing our tissues. Human interactions with fungi can be harmful in other ways including poisonings by highly toxic mushrooms, exposure to ‘mycotoxins’ produced by fungi that cause food spoilage, and allergies stimulated by the inhalation of airborne spores. Human physiology is also affected by psychoactive compounds produced by ‘magic mushroom’ species that are sought by devotees of hallucinatory experiences. Drugs purified from these fungi have also been used in some fascinating neuroscience experiments that have illuminated brain function.

  The yeast Saccharomyces cerevisiae has been used to make bread, ferment wine, and brew beer for millennia and fundamental practices of mushroom growing have changed very little for centuries. Traditional methods of working with fungi have been refined with the use of carefully controlled growth conditions and strains of fungi with specific properties. Genetic engineering has become part of the biotechnology industry in which yeasts and filamentous fungi are used to produce antibiotics and other pharmaceutical agents, industrial enzymes, organic acids, and vitamins.

  6. The stalked sporangium of the dung fungus Pilobolus kleinii. The translucent stalk is a few millimetres tall and filled with pressurized fluid. The swelling at the top serves as a lens that focuses sunlight on pigments that allow the fungus to point towards the sun. Discharge of the black sporangium occurs when it breaks from the stalk and is blasted up to 2.5 metres through the air at a speed of 32 kilometres per hour.

  At a time when fewer and fewer biologists specialize in the broad study of groups of organisms, biologists who call themselves mycologists have become as scarce as professional entomologists and ornithologists. But fungi are studied by many scientists, including cell and molecular biologists who use fungi as ‘model systems’ for exploring fundamental questions about the way cells work. Indeed, fungi have been used in some of the most important experiments in modern biology including research that led to the ‘one gene-one enzyme hypothesis’ in the 1940s, work on the cell cycle in the 1970s and 1980s, and the sequencing of whole genomes in the 1990s. Other scientists who study fungi include plant pathologists who are just as interested in plants as the fungi that attack them, specialists in indoor air quality concerned with the allergens carried by spores, and palynologists who use historical deposits of fungal spores (along with pollen) as indicators of ecosystem and climate change.

  Beyond the academic study of fungi, many people enjoy mushroom hunting and love to cook and eat bronze-capped ceps (porcini), golden chanterelles, honeycomb-headed morels, and other delicious edibles. The yin-yang nature of the mushroom, with the shared pulchritude of the poisonous and the edible, places a premium upon the art and science of mushroom identification. This makes an illustrated guidebook on fungi a viewing pleasure and a potential lifesaver. And with so many mushrooms, there is a great deal to learn. We turn in Chapter 2 to the wider diversity of the fungi as we consider the characteristics of the major groups recognized by biologists.

  Chapter 2

  Fungal diversity

  The range of fungal complexity

  Fungi are more diverse in their structure and behaviour than anyone would imagine from their representation in popular culture. Most people recognize that mushrooms come in a range of sizes and colours, that yeasts are fungi used in baking and brewing, and that other microscopic fungi cause vaginal irritation and athlete’s foot. This snapshot of the fungi does not come close to representing the variety of the mycological world.

  Consideration of three species that span the range of structural complexity among the fungi may be helpful in expanding our survey of this group of organisms. A fungus called Olpidium brassicae is about as simple as a fungus gets. Olpidium is a parasite of cabbage that uses swimming zoospores to infect the root cells of its host (Figure 7). Once inside a root, the fungus grows as a rounded pellet, or thallus, that feeds on its surroundings. Each thallus expels a new gen
eration of zoospores after the nutrients in the infected cell are exhausted. Olpidium uses an intricate mechanism to penetrate the cells of its host but its structure is very plain compared with other fungi. The only deviation from the cycle of swimming zoospores, plant infection, formation of feeding thalli, and return to swimming zoospores, is the formation of angular resting spores that can maintain the fungal population at the end of the growing season.

  7. Olpidium brassicae, an aquatic fungus that infects cabbage roots using zoospores.

  Spirodactylon aureum is a representative of the middle of the range of structural complexity (Figure 8). This fungus grows on rodent dung and forms spores within coiled stalks that project into the air. Each stalk is 1–2 millimetres in height and supports numerous coils. The whole structure gyrates when it is disturbed and looks like a miniature crystal chandelier. It has been suggested that the spores of this fungus are spread on the hairs of rodents that brush past the coils. Although spore formation in this fungus involves the development of this spectacular apparatus, Spirodactylon does not create any kind of larger fruit body comparable to a mushroom for housing the cells that produce its spores.