Fungi Page 7
The presence of massive quantities of leaf pulp in the ant nests provides an opportunity for the growth of other kinds of fungi. The ants groom their gardens, removing foreign spores and chunks of mycelium infected by these intruders. An ascomycete called Escovopsis specializes in attacking the fungal mycelium rather than competing with it for access to the leaf pulp. Spores of this damaging ‘mycoparasite’ are collected by the ants, pressed into a pocket inside their mouths, and regurgitated outside the nest. Before they are dumped, the spores are sterilized by antibiotics produced by bacteria that grow on the surface of the ants.
The cultivation of fungi is quite widespread among other kinds of ants. One group of ant species farms coral fungi in small nests containing fewer than one hundred workers. Another group cultivates colonies of fungi growing as yeasts rather than filaments. Ants feed coral fungi and yeasts with a mixture of organic materials including wood particles, seeds, plant sap, nectar, dead flowers, and insect excrement. All of the types of ant agriculture evolved from a common ancestor that lived fifty million years ago by farming a variety of fungi, rather than a single mushroom species. Leaf-cutter agriculture is the most recent innovation, which began about ten million years ago.
Termites engage in a comparable form of fungal agriculture in Africa and Asia. Colonies of one or two million insects build mounds of mud and tend mycelia grown on macerated plant matter. Foraging termites chew and swallow grass and wood and deposit this as faeces when they return to the nest. Workers inside the nest fashion this undigested slurry into spongy masses called combs. Mycelia of the symbiotic fungi decompose the plant tissues in the combs, producing sugars and proteins that nourish the colony. The fungi in these relationships are species of Termitomyces, including the West African mushroom, Termitomyces titanicus, whose enormous gilled fruit bodies have a diameter of up to a metre. Young workers eat fungal nodules on the surface of the combs that could otherwise develop into mushrooms. Once a mound is abandoned, the fruit bodies emerge from the combs and plough their way through the wall. The cathedral mounds built by some termite species can exceed five metres in height. Airflow along a central shaft in the mound and through the porous mud walls maintains a relatively constant temperature that optimizes decomposition by the fungus. The combination of climate control and careful husbandry of the fungus by the termites is comparable to the methods of industrial mushroom cultivation by humans.
Mutualisms with plants: mycorrhizas and endophytes
Mycorrhizas are, seemingly, less lively kinds of fungal symbioses than those associated with social insects. Lacking the visible bustle of an insect colony, more imagination is needed to appreciate the flurry of molecular communication that maintains these fungal connections with plant roots. This chemical dialogue is needed to modulate the defences of the plant and to quell tissue damage by the fungus. In some mycorrhizal symbioses it is impossible to be sure which, if either, organism benefits from the interaction. The issue is complicated by the fact that the behaviour of a fungus can sometimes shift from mutualism to parasitism. The edible matsutake mushroom, Tricholoma matsutake, performs this switch. Its mycelia form mycorrhizas with young roots, then turn nasty and attack the host plant, and, finally, live as saprotrophs by decomposing the dead tissues of their former collaborators.
Fungi establish many kinds of mycorrhizal relationships with plants (Figure 21). Orchid mycorrhizas illustrate the complexity of these associations. The Orchidaceae is one of the largest families of flowering plants, comprising 25,000 to 30,000 species. Orchid seeds are microscopic and do not contain sufficient nutrients to support germination and early seedling development. Nourishment for these critical stages in development is provided by fungi that grow as knots of convoluted hyphae inside the cells of the swelling embryo. These knots are digested by the orchid, furnishing the little plant with food until it turns green and can start supporting itself by photosynthesis. The advantage of this connection to the fungus is unknown and it seems plausible that it is the victim of parasitism by the orchid. As the plant grows, however, a more hospitable relationship develops, with the fungus providing the plant with phosphorus and nitrogen and the orchid contributing sugars. The nutrients supplied by the fungus are absorbed from the soil by its mycelium. Mycorrhizal fungi operate as accessory root systems for plants.
21. Two types of mycorrhizal association between fungi and plant root systems.
The fungi in orchid mycorrhizas can connect with the roots of other kinds of plants to create ‘common mycorrhizal networks’ that support nutrient flow between trees, fungi, and orchids. Pale orchid species that do not produce chlorophyll exploit these networks by obtaining all of their food from the continuous digestion of the knots of fungal hyphae in their cells. These orchids are called mycoheterotrophs, referring to their fungal diet, and mycorrhizal cheaters for their unusual parasitic lifestyle. Photosynthesis by the trees is the ultimate source of the food that sustains these mycoheterotrophs, with the fungus being exploited as the go-between. Other kinds of plants, including species of Ericaceae that lack chlorophyll, engage in similarly manipulative relationships with fungi.
Fungi that form mycorrhizas with orchids are basidiomycetes. Many of these species are called jelly fungi because they produce fruit bodies with a rubbery or gelatinous texture on rotting wood. Basidiomycetes with umbrella-shaped mushrooms establish a different kind of mycorrhiza with trees and shrubs. Hyphae of these ‘ectomycorrhizal’ fungi wrap around the tips of rootlets forming a tight glove, or mantle, and grow between cells in the outer layers of the root tissue creating a structure called the Hartig net. Dissolved minerals are delivered to root cells through the Hartig net and sugars flow to the fungus in the opposite direction. Ectomycorrhizal fungi include boletes, with pores beneath their caps, and many of the gilled mushrooms common in forests. Species of Amanita (including the fly agaric and death cap), Cortinarius (webcaps), Laccaria, Lactarius (milk-caps), and Russula are common ectomycorrhizal fungi with a global distribution. Ectomycorrhizas are formed with only 3 per cent of plant species, but their ecological and economic importance is enormous because these plants include conifers that dominate the northern boreal forests and rainforest trees called dipterocarps in SouthEast Asia.
Broadleafed trees in temperate forests and the rainforests of Africa and South America are also supported by ectomycorrhizas. Ectomycorrhizal mushrooms are so plentiful in the Amazon basin that clouds of their spores accumulate in the atmosphere above the tree canopy. Arbuscular mycorrhizas are also essential for the health of these forests and these are the commonest type of mutualism between fungi and plants. Arbuscular mycorrhizas are formed between fungi classified in the Glomeromycota and 70–90 per cent of plant species including liverworts, ferns, gymnosperms, and flowering plants. Physical contact between fungi and plants in these mergers is provided by arbuscules, which are finely branched connectors between fungal mycelia and the interior of root cells. Arbuscules provide a large surface area for nutrient exchange. Experiments have shown that these symbioses increase plant productivity by as much as 20 per cent. Arbuscular mycorrhizas have huge agricultural significance because they are formed with wheat, corn, rice, potato, and other crops.
If a mushroom is fruiting beneath a healthy tree it is tempting to assume that it is formed by a mycorrhizal fungus that is connected to the tree. DNA fingerprinting can be used to test this idea and often reveals an unexpected level of fungal diversity. In one experiment in Scotland, investigators found that individual pine trees were associated with the mycelia of up to nineteen different mushroom colonies. The mycelia of ectomycorrhizal fungi are formed by branched hyphae, and thicker assemblages of hyphae called ‘cords’ help fungi negotiate dry soil patches and bridge areas where nutrients are scarce. The mycelium connected to every metre of root length can thread its way through hundreds of metres of surrounding soil. This spreading growth pattern is a good tactic for finding soil patches that are rich in nutrients. The protein in the carcass of a dead insect, for
example, offers a dense source of nitrogen for the mycelium. Digestion of the insect is followed by distribution of nitrogen to distant parts of the mycelium and transmission to the plant root. Mycorrhizal fungi can also access essential mineral nutrients by penetrating rock surfaces and secreting organic acids that dissolve calcium, magnesium, and other elements.
Ectomycorrhizas and arbuscular mycorrhizas create mycorrhizal networks like those associated with orchids. By linking adjacent root systems, the fungi support populations of a single plant species and communities of multiple plant species. Experiments show that plants warn one another about pest attack by passing signalling molecules through their common mycorrhizal networks. This allows plants to produce defence compounds before they are attacked by aphids or caterpillars. By operating as an underground communication system for plants, mycorrhizal networks help to protect their hosts and thereby maintain their personal supply of sugars.
The functions of individual mycorrhizas and common mycorrhizal networks in the ecology of forests, grasslands, and other habitats makes it essential for ecologists to consider the activities of fungi in models of plant productivity. The attention to plants as isolated ecological entities was one of the reasons that the study of ecology progressed so slowly and answered few fundamental questions in the 20th century. Mycorrhizas are no longer an afterthought for scientists who develop models of the flow of energy through ecosystems. Mycorrhizas are also an important consideration in the evolution of land plants. Fossils of spores produced by arbuscular mycorrhizal fungi suggest that these symbioses were formed with early land plants. The first of these relationships may have resembled the arbuscles found in today’s liverworts, which are among the most ‘primitive’ plants. Life on land could not have arisen without mycorrhizal fungi and remains dependent on continuing mutualisms between fungi and plants.
Fungi called endophytes form a very different kind of mutualism from mycorrhizas by housing themselves inside plant tissues without any connection to an external mycelium. Endophytes live in the stems and leaves of plants and do not enter their roots. They grow in spaces between plant cells and along the walls of adjacent cells, but do not form structures that resemble the Hartig net or penetrate plant cells with anything like an arbuscle. Endophytes are ascomycetes that appear to have evolved from pathogenic fungi that infect plants and insects. The resemblance between the genomes of a fungus that destroys rice and a rice endophyte is one example of an obvious connection. Neotyphodium species, which are endophytes that live in grasses, are related to insect pathogens. The presence of Neotyphodium in a plant results in faster growth rates, greater tolerance to drought, and resistance to other fungi that cause disease. These endophytes also produce toxic alkaloids that act as natural pesticides that deter insect damage. Some of these compounds are poisonous to horses and cattle, causing the constriction of blood vessels in the animals’ extremities and producing a condition called fescue lameness. These symptoms are similar to ergotism in humans and other mammals, which is caused by the fungus Claviceps purpurea. This is not surprising because the ergot fungus is another close relative of endophytic species of Neotyphodium.
Neotyphodium has lost the ability to reproduce sexually and its hyphae are dispersed inside the seeds of its host plants. This ‘vertical transmission’ allows the fungus to move directly between generations of plants. (In medicine, vertical transmission is used to describe a bacterial or viral infection transferred by a pregnant mother to her foetus.) Related endophytes produce sexual ascospores as well as asexual conidia and use these to sweep across a population of grasses. This form of airborne transfer is referred to as horizontal transmission, and is comparable to the way that a cold virus is spread in an office. Horizontal transmission is very common among endophytes that colonize trees and woody shrubs. Endophytes that protect plants from diseases caused by other microorganisms can switch to the decomposition of leaf tissues towards the end of a growing season. Other endophytes living in the sapwood of trees can begin the active breakdown of wood as its host ages or is damaged. These are additional instances of the plasticity of associations between fungi and plants that allow mutualistic fungi to become parasites.
Lichens
Lichens are the best-known mutualisms involving fungi. They are composite organisms consisting of a fungus and a single-celled alga or cyanobacterium. Algal and cyanobacterial partners in lichens provide the fungus with food produced by photosynthesis. Swiss biologist Simon Schwendener made this discovery in the 19th century. The nature of lichens as coalitions between different organisms was a controversial idea at a time when scientists tended to regard species as isolated entities whose interactions were limited to eating and being eaten. Beatrix Potter, the famous author of children’s books, became interested in lichens and was one of the people who resisted Schwendener’s proposal. (Potter conducted experiments on spore germination, but her modest contributions to mycology have been hyped to an absurd degree when the work of so many other women scientists deserves greater recognition.)
Despite this opposition, many eminent biologists of this period recognized that lichens were ‘dual organisms’ and discovered other mutualistic relationships including ectomycorrhizas, root nodules (bacteria and legumes), and corals (algae and animals). Scientists that specialize in the study of lichens are called lichenologists and they tend to work alongside bryologists who study bryophytes (mosses, liverworts, and hornworts). This intellectual alliance makes sense because lichens and bryophytes often grow in the same habitats, which means that experts on one group of organisms are always finding species of the other group. In the polar tundra, for example, where there are few vascular plants, miniature forests of lichens and bryophytes are the primary producers. Arctic lichens serve as important winter forage for caribou (reindeer).
The Latin names of lichens refer to the species of fungus rather than the photosynthetic companion. This makes a lot of sense because lichens are formed by 18,000 species of ascomycetes (40 per cent of all ascomycetes) with only 150 species of green algae and bacteria. While the fungi in lichens cannot grow without their photosynthetic symbionts, the green algae and bacteria certainly thrive outside lichens. They are recruited from the environment by the fungi and become cradled within a tough fabric of interwoven hyphae in the body, or thallus, of the lichen. This ‘fungus first’ mechanism explains how a single lichen thallus contains one fungus but can incorporate multiple strains of the photosynthetic partner.
Lichens are categorized by shape as crustose (thin crusts), fruticose (shrubby), and foliose (leafy). Rhizocarpon geographicum is a crustose lichen that grows on rocks in the form of a mosaic of yellow patches separated by cracks. With a little imagination, the yellow patches look like regions on a map with the cracks serving as boundaries. This explains the common name of yellow map lichen. In the temperate rainforests of the Oregon Cascades, long grey-green strands of the Methuselah’s beard lichen, Dolichousnea longissima, hang from the branches of Douglas firs. Growth of this fruticose lichen is very sensitive to atmospheric pollution and it has disappeared from much of its original range in Europe. Other lichens flourish under unpromising conditions of industrial and agricultural pollution. Xanthoria parietina is an orange or yellow foliose lichen that grows on roofing in urban areas and covers farm buildings where it is exposed to nitrogen fertilizers. Its natural preference for high nitrogen levels is also shown in its appearance in coastal areas on rocks fertilized by bird guano. Variations in the sensitivity of lichens to nitrates, sulphates, and other chemicals make them very useful as indicators of industrial and agricultural pollution.
Most lichens contain green algae, but 15 per cent of species involve cyanobacteria. In addition to the formation of sugars by photosynthesis, the cyanobacteria in lichens absorb nitrogen gas (N2) from the atmosphere to produce ammonia (NH3). The ammonia is used by the bacterium and the fungus as a source of nitrogen for the synthesis of proteins and nucleic acids. This is crucial for lichens living in places where nitr
ogen is scarce. Species of Peltigera, called dog or pelt lichens, form large grey, green, or brown lobes on wet soil and other mossy locations. Some species of these foliose lichens are three-way combinations of fungus, green alga, and cyanobacterium. Fungi absorb sugars and exchange other nutrients with ‘their’ algae through slender branches that protrude into the green cells. Contact with cyanobacteria is achieved by forming tight connections with the cell surface without penetrating the bacterial wall.
Lichens reproduce by releasing spores of the fungus and rely upon young colonies of the fungus to associate with their photosynthetic partners soon after spore germination. This is only effective, of course, when the appropriate algae or cyanobacteria are prevalent in the environment. Ascospores are produced in fruit bodies that develop on the surface of lichens. The red-tipped branches of a lichen called British soldiers, Cladonia cristatella, are fruit bodies displaying a layer of asci and intervening cells that contain globules of red pigment. The common name of this lichen refers to the ‘Redcoats’ who fought against the Continental Army during the American Revolutionary War. A minority of lichens are produced by basidiomycetes rather than ascomycetes. These lichens reproduce by forming tiny mushrooms. In addition to the release of sexual ascospores and basidiospores, lichens reproduce asexually by dispersing small parcels of fungal hyphae wrapped around algal cells. These form as a powdery coating on the thallus and reformulate exactly the same symbiosis in a new location.