13.2 Fungi as recyclers and saprotrophs
We have discussed many aspects of this topic in earlier Chapters (particularly in Chapter 10); we will not repeat them here but will mention them again to bring the strands together here and provide reference to their earlier discussion.
Fungi have been recycling biological remains for at least half a billion years (Taylor et al., 2004, 2006). The earliest fibrous fossils (nematophytes) may well have been large multihyphal fungi that were widespread and dominant terrestrial organisms 440 million years ago. These fungi were presumably creating the ancient ‘soil’, which the first terrestrial animals and plants could invade. Several examples of mycoparasitism have been described in specimens from the Lower Devonian Rhynie chert, and the same material shows vesicular-arbuscular mycorrhizas occurring in the earliest terrestrial plants among these 400 million year old fossils (see the Fossil fungi section of Chapter 2; CLICK HERE to view the page).
A defining characteristic of fungi is that they obtain their nutrients by external digestion of substrates. Technically, all fungi are chemo-organoheterotrophs, meaning that they derive their carbon, energy and electrons (with which they do further chemical work) from a wide variety of organic sources. There are three main sub-groups to this category:
- Saprotrophs are the decomposers, the category probably covers the majority of fungi and is the main topic of this section.
- Necrotrophs invade and kill host (usually plant) tissue rapidly and then live saprotrophically on the dead remains. These tend to be relatively unspecialised pathogens, able to attack any plant tissue if conditions at the tissue surface are favourable for infection; they cause diseases like foot-rots, damping-off in seedlings, and leaf and stem blotch of mature plants because their infection causes tissue necrosis. Examples are diseases caused by Rhizoctonia, Fusarium, Septoria and, among the Oomycota, Pythium (see Chapter 14).
- Biotrophs are found on or in living plants and they do not kill their host plant rapidly. They may have very complex nutrient requirements, so they either cannot be grown in culture or grow only to a limited extent on specialised media. These are the specialised pathogens that are highly host-specific, such as powdery mildew caused by Erysiphe graminis, rice blast caused by Magnaporthe grisea, and animal pathogens like Cryptococcus neoformans (see Chapters 14 and 16).
Saprotrophic fungi decompose many things, and because they can digest and extract nutrients from so many of the materials that exist on, within and under the soil, fungal mycelia act as sinks of organic carbon and nitrogen in the soil. In many ecosystems, a fair proportion of the carbon fixed by photosynthesis ends up in fungal mycelium because of the prevalence of the mycorrhizal symbiotic association between fungus and plant roots (see below).
Something that usually gets much less attention is the fungal involvement in inorganic transformations and element cycling in rocks and minerals (see the Geomycology section of Chapter 1; CLICK HERE to view the page). Several fungi can dissolve and mobilise minerals and metal ions more efficiently than bacteria, and in all soils fungi are involved in scavenging and redistributing minerals and inorganic nutrients (for example, essential metal ions and phosphate). Though this activity is not limited to mycorrhizal fungi, it enables mycorrhizas to make a particularly important contribution to their host as the insoluble salts of minerals (especially phosphates) cannot be absorbed by plant roots but can be solubilised by the mycorrhizal hyphae. Fungi can also accumulate large amounts of metal ions; for example, silver accumulates in Amanita fruit bodies to levels reaching 1 g kg-1 dry weight which was 800-2500 times higher than in the underlying soils (Borovička et al., 2007). Lepp, Harrison & Morrell (1987) give similar information about cadmium and vanadium, and Avila, Johanson & Bergstrom (1999) showed that concentrations of radioactive caesium in roe deer in Sweden, a legacy of fallout from the Chernobyl incident, increased by up to a factor of five specifically during the mushroom season. Perhaps the most important thing overall, is that the mycelial sink keeps the nutrients ‘on site’ and so prevents their loss from the soil by rain-water leaching.
A particularly important ability of fungi is that they are the only organisms that can digest wood; that is, plant secondary cell wall, which is the most widespread substrate on the planet, constituting about 95% of the terrestrial biomass. The lignin, which is complexed with hemicelluloses and cellulose in wood, is extremely difficult to degrade and has evolved in part to be a deterrent to microbial attack on long-lived plant parts. Lignin digestion is restricted to fungi, mostly Basidiomycota but including a few Ascomycota, which between them consume an estimated 4×1011 metric tonnes of plant biomass each year. About 70% of the mass of wood is made up of cellulose, hemicelluloses and pectins and the enzymology of polysaccharide digestion has been described in Chapter 10 (see Breakdown of polysaccharide: cellulose section; CLICK HERE to view the page).
Lignin is a highly branched phenylpropanoid polymer that comprises about 20-25% of wood. Lignin breakdown is an oxidative rather than a hydrolytic process and involves cleavage of ether bonds between monomers, oxidative cleavage of the propane side chain, phenol demethylation and benzene-ring cleavage to ketoadipic acid which is fed into the tricarboxylic acid cycle. It depends on a panel of enzymes including: manganese peroxidase, which catalyses H2O2-dependent oxidation of lignin; lignin peroxidase, a haem [Fe]-containing protein, which also catalyses H2O2-dependent oxidation of lignin; and laccase (a copper-containing protein) that catalyses demethylation of lignin components (see the section on Lignin degradation in Chapter 10; CLICK HERE to view the page, and the Digestion of lignocellulosic residues section of Chapter 17; CLICK HERE to view the page).
The most abundant nitrogen sources available to organisms degrading plant litter are polypeptides in the form of plant protein, lignoprotein and microbial protein. Extracellular proteinase enzymes are produced by many species of fungi to hydrolyse large polypeptide substrates into the smaller molecules that can be absorbed by the cell (see the section on Digestion of protein in Chapter 10; CLICK HERE to view the page). Many pathogenic fungi secrete proteinases as part of their infection process and, of course, they also use host proteins for nutrition. Saprotrophic and mycorrhizal fungi can use protein as a source of both nitrogen and carbon (and sulfur, too) and some ectomycorrhizas (see below) supply nitrogen derived from soil proteins to their plant hosts.
Rather than continuing to expand on details about saprotrophic fungi that appear in other Chapters we will describe here some incidental matters arising out of this mode of growth. These are (a) the way they can make the earth move, (b) fungal toxins, (c) decay of structural timber in dwellings, (d) the potential for using fungi to remediate toxic and recalcitrant wastes, and (e) release of chlorohydrocarbons into the atmosphere by wood decay fungi.
Updated December 17, 2016