Organic Matter Degradation and Biogeochemical Cycling

Most attention has been given to carbon and nitrogen cycles, and the ability of fungi to utilize a wide spectrum of organic compounds is well known. These range from

simple compounds such as sugars, organic acids, and amino acids which can easily be transported into the cell to more complex molecules which are first broken down to smaller molecules by extracellular enzymes before cellular entry. Such compounds include natural substances such as cellulose, pectin, lignin, lignocellulose, chitin and starch to anthropogenic products like hydrocarbons, pesticides, and other xenobiotics.

Table 1 Summary of some of the important roles and activities of fungi in biogeochemical processes

Fungal role and/or activity Biogeochemical consequences

Growth

Growth and mycelium Stabilization of soil structure; soil particulate aggregation; penetration of pores, fissures, and development grain boundaries in rocks and minerals; mineral tunneling; biomechanical disruption of solid substrates; plant colonization and/or infection (mycorrhizas, pathogens, parasites); animal colonization and/or infection (symbiotic, pathogens, parasites); translocation of inorganic and organic nutrients; assisted redistribution of bacteria; production of exopolymeric substances (serve as nutrient resource for other organisms); water retention and translocation; surfaces for bacterial growth, transport, and migration; cord formation (enhanced nutrient translocation); mycelium acting as a N reservoir of N and/or other elements (e.g., wood decay fungi)

Metabolism

Carbon and energy metabolism Organic matter decomposition; cycling and/or transformations of component elements of organic compounds and biomass: C, H, O, N, P, S, metals, metalloids, radionuclides (natural and accumulated from anthropogenic sources); breakdown of polymers; altered geochemistry of local environment, e.g., changes in redox, O2, pH; production of inorganic and organic metabolites, e.g., H+, CO2, organic acids, with resultant effects on the substrate; extracellular enzyme production; fossil fuel degradation; oxalate formation; metalloid methylation (e.g., As, Se); xenobiotic degradation (e.g., PAHs); organometal formation and/or degradation (note: lack of fungal decomposition in anaerobic conditions caused by waterlogging can lead to organic soil formation, e.g., peat)

Inorganic nutrition Altered distribution and cycling of inorganic nutrient species, e.g., N, S, P, essential and inessential metals, by transport and accumulation; transformation and incorporation of inorganic elements into macromolecules; alterations in oxidation state; metal(loid) oxido-reductions; heterotrophic nitrification; siderophore production for Fe(iii) capture; translocation of N, P, Ca, Mg, Na, K through mycelium and/or to plant hosts; water transport to and from plant hosts; metalloid oxyanion transport and accumulation; degradation of organic and inorganic sulfur compounds

Mineral dissolution Rock and mineral deterioration and bioweathering including carbonates, silicates, phosphates, and sulfides; bioleaching of metals and other components; MnO2 reduction; element redistributions including transfer from terrestrial to aquatic systems; altered bioavailability of, e.g., metals, P, S, Si, Al; altered plant and microbial nutrition or toxicity; early stages of mineral soil formation; deterioration of building stone, cement, plaster, concrete, etc.

Mineral formation Element immobilization, including metals, radionuclides, C, P, and S; mycogenic carbonate formation; limestone calcrete cementation; mycogenic metal oxalate formation; metal detoxification; contribution to patinas on rocks (e.g., 'desert varnish'); soil storage of C and other elements

Physicochemical properties

Sorption of soluble and particulate Altered metal distribution and bioavailability; metal detoxification; metal-loaded food source for metal species invertebrates; prelude to secondary mineral formation

Exopolysaccharide production Complexation of cations; provision of hydrated matrix for mineral formation; enhanced adherence to substrate; clay mineral binding; stabilization of soil aggregates; matrix for bacterial growth; chemical interactions of exopolysaccharide with mineral substrates

Symbiotic associations

Mycorrhizas Altered mobility and bioavailability of nutrient and inessential metals, N, P, S, etc.; altered Cflow and transfer between plant, fungus, and rhizosphere organisms; altered plant productivity; mineral dissolution and metal and nutrient release from bound and mineral sources; altered biogeochemistry in soil-plant root region; altered microbial activity in plant root region; altered metal distributions between plant and fungus; water transport to and from the plant

Lichens Pioneer colonization of rocks and minerals; bioweathering; mineral dissolution and/or formation;

metal accumulation and redistribution; metal accumulation by dry or wet deposition, particulate entrapment; metal sorption; enrichment of C, N, etc.; early stages of mineral soil formation; development of geochemically active microbial populations; mineral dissolution by metabolites including 'lichen acids'; biophysical disruption of substrate

(Continued )

Table 1 (Continued)

Fungal role and/or activity Biogeochemical consequences

Insects and invertebrates Fungal populations in gut aid degradation of plant material; invertebrates mechanically render plant residues more amenable for decomposition; cultivation of fungal gardens by certain insects (organic matter decomposition and recycling); transfer of fungi between plant hosts by insects (aiding infection and disease)

Pathogenic effects

Plant and animal pathogenicity Plant infection and colonization; animal predation (e.g., nematodes) and infection (e.g., insects);

redistribution of elements and nutrients; increased supply of organic material for decomposition; stimulation of other geochemically active microbial populations

Such activities take place in aquatic and terrestrial ecosystems, as well as in artificial and man-made systems, their relative importance depending on the populations present and physicochemical factors that affect activity. Clearly, the terrestrial environment is the main locale of fungal-mediated biogeochemical change, especially in mineral soils and the plant root zone, and on exposed rocks and mineral surfaces. There is rather a limited amount of knowledge on fungal biogeochemistry in freshwater and marine systems, sediments, and the deep subsurface. Fungal roles have been arbitrarily split into categories based on growth, organic and inorganic metabolism, physicochemical attributes, and symbiotic relationships. However, it should be noted that many, if not all, of these are inter-linked, and almost all directly or indirectly depend on the mode of fungal growth (including symbiotic relationships) and accompanying heterotrophic metabolism, in turn dependent on a utilizable carbon source for biosynthesis and energy, and other essential elements, such as N, O, P, S, and many metals, for structural and cellular components. Mineral dissolution and formation are outlined separately although these processes clearly depend on metabolic activity and growth form.

Some fungi have remarkable degradative properties, and lignin-degrading white rot fungi, such as Phanerochaete chry-sosporium, can degrade several xenobiotics including aromatic hydrocarbons, chlorinated organics, polychlori-nated biphenyls, nitrogen-containing aromatics and many other pesticides, dyes, and xenobiotics. Such activities are of potential in bioremediation where appropriate ligninolytic fungi have been used to treat soil contaminated with substances like pentachlorophenol (PCP) and polynuclear aromatic hydrocarbons (PAHs), the latter being constituents of creosote. In many cases, xenobiotic-transforming fungi need additional utilizable carbon sources because although capable of degradation, they cannot utilize these substrates as an energy source for growth. Therefore, inexpensive utilizable lignicellulosic wastes such as corn cobs, straw, and sawdust can be used as nutrients to obtain enhanced pollutant degradation. Wood-rotting and other fungi are also receiving attention for the bleaching of dyes and industrial effluents, and the biotreatment of various agricultural wastes such as forestry, pulp and paper byproducts, sugar cane bagasse, coffee pulp, sugar beet pulp, apple and tomato pulp, and cyanide.

Fungi are also important in the degradation of naturally occurring complex molecules in the soil, an environment where the hyphal mode of growth provides several advantages, and also in aquatic habitats. Since 95% of plant tissue is composed of carbon, hydrogen, oxygen, nitrogen, phosphorus, and sulfur, the decomposition activities of fungi clearly are important in relation to redistribution of these elements between organisms and environmental compartments. In addition to C, H, O, N, P, and S, another 15 elements are typically found in living plant tissues -K, Ca, Mg, B, Cl, Fe, Mn, Zn, Cu, Mo, Ni, Co, Se, Na, and Si. However, all 90 or so naturally occurring elements may be found in plants, most at low concentrations although this may be highly dependent on environmental conditions. These include Au, As, Hg, Pb, and U, and there are even plants that accumulate relatively high concentrations of metals like Ni and Cd. In fact, plant metal concentrations may reflect environmental conditions and provide an indication of toxic metal pollution or metalliferous ores. Such plants are also receiving attention in bioremediation contexts (=phytoremediation). Animals likewise contain a plethora of elements in varying amounts. For example, the human body is mostly water and so 99% of the mass comprises oxygen, carbon, hydrogen, nitrogen, calcium, and phosphorus. However, many other elements are present in lower amounts including substances taken up as contaminants in food and water. A similar situation occurs throughout the plant, animal, and microbial world and therefore, any decomposition, degradative, and pathogenic activities of fungi must be linked to the redistribution and cycling of all these constituent elements, both on local and global scales (Figure 2).

Organometals (compounds with at least one metal-carbon bond) can also be attacked by fungi with the organic moieties being degraded and the metal compound undergoing changes in speciation. Degradation of organo-metallic compounds can be carried out by fungi, either by direct biotic action (enzymes) or by facilitating abiotic degradation, for instance, by alteration of pH and excretion of metabolites. Organotin compounds, such as tributyltin oxide and tributyltin naphthenate, may be degraded to mono- and dibutyltins by fungal action, inorganic Sn(ii) being the ultimate degradation product. Organomercury compounds may be detoxified by conversion to Hg(ii) by fungal organomercury lyase, the

Figure 2 Simplified elemental biogeochemical cycle in a vegetated ecosystem where organic matter decomposition processes, and therefore a prime fungal role, leads to cycling of many other elements besides C. The cycle depicted could be of Ca or K for example. Organic matter could also arise from anthropogenic sources.

Figure 2 Simplified elemental biogeochemical cycle in a vegetated ecosystem where organic matter decomposition processes, and therefore a prime fungal role, leads to cycling of many other elements besides C. The cycle depicted could be of Ca or K for example. Organic matter could also arise from anthropogenic sources.

Hg(n) being subsequently reduced to Hg(0) by mercuric reductase, a system broadly analogous to that found in mercury-resistant bacteria.

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