The Role of Mushrooms in Nature
The Mycorrhizal Gourmet Mushrooms
Parasitic Mushrooms: Blights of the Forest?
Saprophytic Mushrooms: The Decomposers
The Global Environmental Shift
Mushrooms and Toxic Wastes
Mushroom Mycelium and Mycofiltration
About the Author
Related Editions of The Overstory
Fungi have vital roles in ecosystem health. There are numerous fungi that produce fleshy fruiting bodies known as mushrooms, many of which are prized for their edible and medicinal uses. In this edition of The Overstory, special guest author Paul Stamets explores the role of mushroom-producing fungi (commonly referred to as mushrooms) in the health of forests and other landscapes.
The article covers three basic ecological groups of mushrooms: those that form a symbiosis with host plants called mycorrhizal mushrooms; those that act on living plants called parasitic mushrooms; and those that recycle dead plant material, the saprophytic mushrooms.
The Mycorrhizal Gourmet Mushrooms
Mycorrhizal mushrooms form a mutually dependent, beneficial relationship with the roots of host plants, ranging from trees to grasses. "Myco" means mushrooms, while "rhizal" means roots. The collection of filament of cells that grow into the mushroom body is called the mycelium. The mycelia of these mycorrhizal mushrooms can form an exterior sheath covering the roots of plants and are called ectomycorrhizal. When they invade the interior root cells of host plants they are called endomycorrhizal. In either case, both organisms benefit from this association. Plant growth is accelerated. The resident mushroom mycelium increases the plant's absorption of nutrients, nitrogenous compounds, and essential elements (phosphorus, copper, and zinc). By growing beyond the immediate root zone, the mycelium channels and concentrates nutrients from afar. Plants with mycorrhizal fungal partners can also resist diseases far better than those without.
Most ecologists now recognize that a forest's health is directly related to the presence, abundance, and variety of mycorrhizal associations. The mycelial component of topsoil within a typical Douglas fir forest in the Pacific Northwest approaches 10% of the total biomass. Even this estimate may be low, not taking into account the mass of the endomycorrhizae and the many yeast-like fungi that thrive in the topsoil.
The nuances of climate, soil chemistry, and predominant microflora play determinate roles in the cultivation of mycorrhizal mushrooms in natural settings. Species native to a region are likely to adapt much more readily to designed habitats than exotic species. I am much more inclined to spend time attempting the cultivation of native mycorrhizal species than to import exotic candidates from afar.
One method for inoculating mycorrhizae calls for the planting of young seedlings near the root zones of proven Truffle trees. The new seedlings acclimate and become "infected" with the mycorrhizae of a neighboring, parent tree. In this fashion, a second generation of trees carrying the mycorrhizal fungus is generated. After a few years, the new trees are dug up and replanted into new environments. This method has had the longest tradition of success in Europe.
Another approach, modestly successful, is to dip exposed roots of seedlings into water enriched with the spore-mass of a mycorrhizal candidate. First, mushrooms are gathered from the wild and soaked in water. Thousands of spores are washed off the gills, resulting in an enriched broth of inoculum. A spore-mass slurry coming from several mature mushrooms and diluted into a 5-gallon bucket can inoculate a hundred or more seedlings. The concept is wonderfully simple. Unfortunately, success is not guaranteed.
Broadcasting spore-mass onto the root zones of likely candidates is another venue that costs little in time and effort. Habitats should be selected on the basis of their parallels in nature. For instance, Chanterelles can be found in oak forests of the Midwest and in Douglas fir forests of the West. Casting spore-mass of Chanterelles into forests similar to those where Chanterelles proliferate is obviously the best choice. Although the success rate is not high, the rewards are well worth the minimum effort involved. Bear in mind that tree roots confirmed to be mycorrhized with a gourmet mushroom will not necessarily result in harvestable mushrooms. Fungi and their host trees may have long associations without the appearance of edible fruit bodies. (For more information, consult Fox, 1983.)
On sterilized media, most mycorrhizal mushrooms grow slowly, compared to the saprophytic mushrooms. Their long evolved dependence on root by-products and complex soils makes media preparation inherently more complicated. Some mycorrhizal species, like Pisolithus tinctorius, a puffball favoring pines, grow quite readily on sterilized media. A major industry has evolved providing foresters with seedlings inoculated with this fungus. Mycorrhized seedlings are healthier and grow faster than non-mycorrhized ones. Unfortunately, the gourmet mycorrhizal mushroom species do not fall into the readily cultured species category. The famous Matsutake may take weeks before its mycelium fully colonizes the media on a single petri dish! Unfortunately, this rate of growth is the rule rather than the exception with the majority of gourmet mycorrhizal species.
Given the huge hurdle of time for honing laboratory techniques, I favor the "low-tech" approach of planting trees adjacent to known producers of Chanterelles, Matsutake, Truffles, and Boletus. After several years, the trees can be uprooted, inspected for mycorrhizae, and replanted in new environments. The value of the contributing forest can then be viewed, not in terms of board feet of lumber, but in terms of its ability for creating satellite, mushroom/tree colonies. When industrial or suburban development threatens entire forests, and is unavoidable, future-oriented foresters may consider the removal of the mycorrhizae as a last-ditch effort to salvage as many mycological communities as possible by simple transplantation techniques, although on a much grander scale.
Parasitic Mushrooms: Blights of the Forest?
Parasitic fungi are the bane of foresters. They do immeasurable damage to the health of resident tree species, but in the process create new habitats for many other organisms. Although the ecological damage caused by parasitic fungi is well understood, we are only just learning of their importance in the forest ecosystem. Comparatively few mushrooms are true parasites.
Parasites live off a host plant, endangering the host's health as it grows. Of all the parasitic mushrooms that are edible, the Honey mushroom, Armillaria mellea, is the best known. One of these Honey mushrooms, known as Armillaria gallica, made national headlines when scientists reported finding in Michigan a single colony covering 37 acres, weighing at least 220,000 pounds, with an estimated age of 1,500 years! Washington State soon responded with reports of a colony of Armillaria ostoyae covering 2,200 acres and at least 2,400 years old. With the exception of the trembling Aspen forests of Colorado, this fungus is the largest known living organism on the planet. And, it is a marauding parasite!
In the past, a parasitic fungus has been looked upon as biologically evil. This view is rapidly changing as science progresses. Montana State University researchers have discovered a new parasitic fungus attacking the yew tree. This new species is called Taxomyces andreanae and is medically significant for one notable feature: it produces minute quantities of the potent anti-carcinogen Taxol, a proven treatment for breast cancer (Stone, 1993). This new fungus was studied and now a synthetic form of this potent drug is available for cancer patients. Recently, a leaf fungus isolated in the Congo has been discovered that duplicates the effect of insulin, but is orally active. Even well known medicines from fungi harbor surprises. A mycologist at Cornell University (Hodge et al. 1996) recently discovered that the fungus responsible for the multibillion dollar drug, cyclosporin, has a sexual stage in Cordyceps subsessilis, a parasitic mushroom attacking scarab beetle larvae. Of the estimated 1,500,000 species of fungi, approximately 70,000 have been identified (Hawksworth et al. 1995), and about 10,000 are mushrooms. We are just beginning to discover the importance of species hidden within this barely explored genome.
Many saprophytic fungi can be weakly parasitic in their behavior, especially if a host tree is dying from other causes. These can be called facultative parasites: saprophytic fungi activated by favorable conditions to behave parasitically. Some parasitic fungi continue to grow long after their host has died. Oyster mushrooms (Pleurotus ostreatus) are classic saprophytes, although they are frequently found on dying cottonwood, oak, poplar, birch, maple, and alder trees. These appear to be operating parasitically when they are only exploiting a rapidly evolving ecological niche.
Saprophytic Mushrooms: The Decomposers
Most of the gourmet mushrooms are saprophytic, wood-decomposing fungi. Saprophytic fungi are the premier recyclers on the planet. The filamentous mycelial network is designed to weave between and through the cell walls of plants. The enzymes and acids they secrete degrade large molecular complexes into simpler compounds. All ecosystems depend upon fungi's ability to decompose organic plant matter soon after it is rendered available. The end result of their activity is the return of carbon, hydrogen, nitrogen, and minerals back into the ecosystem in forms usable to plants, insects, and other organisms. As decomposers, they can be separated into three key groups. Some mushroom species cross over from one category to another depending upon prevailing conditions.
Primary Decomposers: These are the fungi first to capture a twig, a blade of grass, a chip of wood, a log or stump. Primary decomposers are typically fast-growing, sending out ropy strands of mycelium that quickly attach to and decompose plant tissue. Most of the decomposers degrade wood. Hence, the majority of these saprophytes are woodland species, such as Oyster mushrooms (Pleurotus species), Shiitake (Lentinula edodes), and King Stropharia (Stropharia rugosoannulata). However, each species has developed specific sets of enzymes to break down lignin-cellulose, the structural components of most plant cells. Once the enzymes of one mushroom species have broken down the lignin-cellulose to its fullest potential, other saprophytes utilizing their own repertoire of enzymes can reduce this material even further.
Secondary Decomposers: These mushrooms rely on the previous activity of other fungi to partially break down a substrate to a state wherein they can thrive. Secondary decomposers typically grow from composted material. The actions of other fungi, actinomycetes, bacteria, and yeasts all operate within compost. As plant residue is degraded by these microorganisms, the mass, structure, and composition of the compost is reduced, and proportionately available nitrogen is increased. Heat, carbon dioxide, ammonia, and other gases are emitted as by-products of the composting process. Once these microorganisms (especially actinomycetes) have completed their life cycles, the compost is susceptible to invasion by a select secondary decomposer. A classic example of a secondary decomposer is the Button Mushroom, Agaricus brunnescens, the most commonly cultivated mushroom. Another example is Stropharia ambigua, which invades outdoor mushroom beds after wood chips have been first decomposed by a primary saprophyte.
Tertiary Decomposers: An amorphous group, the fungi represented by this group are typically soil dwellers. They survive in habitats that are years in the making from the activity of the primary and secondary decomposers. Fungi existing in these reduced substrates are remarkable in that the habitat appears inhospitable for most other mushrooms. A classic example of a tertiary decomposer is Aleuria aurantia, the Orange Peel Mushroom. This complex group of fungi often poses unique problems to would-be cultivators. Panaeolus subbalteatus is yet another example. Although one can grow it on composted substrates, this mushroom has the reputation of growing prolifically in the discarded compost from Button mushroom farms. Other tertiary decomposers include species of Conocybe, Agrocybe, Pluteus, and some Agaricus species.
The floor of a forest is constantly being replenished by new organic matter. Primary, secondary, and tertiary decomposers can all occupy the same location. In the complex environment of the forest floor, a "habitat" can actually be described as the overlaying of several, mixed into one. And, over time, as each habitat is being transformed, successions of mushrooms occur. This model becomes infinitely complex when taking into account the interrelationships of not only the fungi to one another, but also the fungi to other microorganisms (yeasts, bacteria, protozoa), plants, insects, and mammals.
Primary and secondary decomposers afford the most opportunities for cultivation. To select the best species for cultivation, several variables must be carefully matched. Climate, available raw materials, and the mushroom strains all must interplay for cultivation to result in success. Native species are the best choices when you are designing outdoor mushroom landscapes.
The Global Environmental Shift and the Loss of Species Diversity
Studies in Europe show a frightening loss of species diversity in forestlands, most evident with the mycorrhizal species. Many mycologists fear many mushroom varieties, and even species, will soon become extinct. As the mycorrhizal species decline in both numbers and variety, the populations of saprophyric and parasitic fungi initially rise as a direct result of the increased availability of deadwood debris. However, as woodlots are burned and replanted, the complex mosaic of the natural forest is replaced by a highly uniform, mono-species landscape. Because the replanted trees are nearly identical in age, the cycle of debris replenishing the forest floor is interrupted. This new "ecosystem" cannot support the myriad fungi, insects, small mammals, birds, mosses, and flora so characteristic of ancestral forests. In pursuit of commercial forests, the native ecology has been supplanted by a biologically anemic woodlot. This woodlot landscape is barren in terms of species diversity.
With the loss of habitat of the mycorrhizal gourmet mushrooms, market demands for gourmet mushrooms should shift to those that can be cultivated. Thus, the pressure on this not-yet-renewable resource would be alleviated. I believe the judicious use of saprophytic fungi by homeowners as well as foresters may well prevent widespread parasitic disease vectors. Selecting and controlling the types of saprophytic fungi occupying these ecological niches can benefit both forester and forestland.
Mushrooms and Toxic Wastes
In heavily industrialized areas, the soils are typically contaminated with a wide variety of pollutants, particularly petroleum-based compounds, polychlorinated biphenols (PCBs), heavy metals, pesticide-related compounds, and even radioactive wastes. Mushrooms grown in polluted environments can absorb toxins directly into their tissues, especially heavy metals (Bressa, 1988; Stijve 1974, 1976, 1992). As a result, mushrooms grown in these environments should not be eaten. Recently, a visitor to Ternobyl, a city about 60 miles from Chernobyl, the site of the world's worst nuclear power plant accident, returned to the United States with a jar of pickled mushrooms. The mushrooms were radioactive enough to set off Geiger counter alarms as the baggage was being processed. Customs officials promptly confiscated the mushrooms. Unfortunately, most toxins are not so readily detected.
A number of fungi can, however, be used to detoxify contaminated environments, in a process called "bioremediation." The white rot fungi (particularly Phanerochaete chrysosporium) and brown rot fungi (notably Gloephyllum species) are the most widely used. Most of these wood-rotters produce lignin peroxidases and cellulases, which have unusually powerful degradative properties. These extracellular enzymes have evolved to break down plant fiber primarily lignin-cellulose, the structural component in woody plants, into simpler forms. By happenstance, these same enzymes also reduce recalcitrant hydrocarbons and other manufactured toxins. Given the number of industrial pollutants that are hydrocarbon-based, fungi are excellent candidates for toxic waste cleanup and are viewed by scientists and government agencies with increasing interest. Current and prospective future uses include the detoxification of PCB (polychloralbiphenols), PCP (penrachlorophenol), oil, and pesticide/herbicide residues. They are even being explored for ameliorating the impact of radioactive wastes by sequestering heavy metals.
Bioremediation of toxic waste sites is especially attractive because the environment is treated in situ. The contaminated soils do not have to be hauled away, eliminating the extraordinary expense of handling, transportation, and storage. Since these fungi have the ability to reduce complex hydrocarbons into elemental compounds, these compounds pose no threat to the environment. Indeed, these former pollutants could even be considered "fertilizer," helping rather than harming the nutritional base of soils.
The higher fungi should not be disqualified for bioremediation just because they produce an edible fruitbody. Indeed, this group may hold answers to many of the toxic waste problems. Mushrooms grown from toxic wastes are best not eaten, as residual heavy metal toxins may be concentrated within the mushrooms.
Mushroom Mycelium and Mycofiltration
The mycelium is a fabric of interconnected, interwoven strands of cells. One colony can range in size from a half-dollar to many acres. A cubic inch of soil can host up to a mile of mycelium. This organism can be physically separated, and yet behave as one.
The exquisite lattice-like structure of the mushroom mycelium, often referred to as the mycelial network, is perfectly designed as a filtration membrane. Each colony extends long, complex chains of cells that fork repeatedly in matrix-like fashion, spreading to geographically defined borders. The mushroom mycelium, being a voracious forager for carbon and nitrogen, secretes extracellular enzymes that unlock organic complexes. The newly freed nutrients are then selectively absorbed directly through the cell walls into the mycelial network.
In the rainy season, water carries nutritional particles through this filtration membrane, including bacteria, which often become a food source for the mushroom mycelium. The resulting downstream effluent is cleansed of not only carbon/nitrogen-rich compounds but also bacteria, in some cases nematodes, and legions of other microorganisms. The voracious Oyster mushrooms been found to be parasitic against nematodes (Thorn and Barron, 1984; Hibbett and Thorn, 1994). Extracellular enzymes act like an anesthetic and stun the nematodes, thus allowing the invasion of the mycelium directly into their immobilized bodies.
The use of mycelium as a mycofilter is currently being studied by this author in the removal of biological contaminants from surface water passing directly into sensitive watersheds. By placing sawdust implanted with mushroom mycelium in drainage basins downstream from farms raising livestock, the mycelium acts as a sieve, which traps fecal bacteria and ameliorates the impact of a farm's nitrogen-rich outflow into aquatic ecosystems.