Australia: The Land Where Time Began

A biography of the Australian continent 

Nutrient mobilisation from SOM

SOM as a source of nutrients

Ectomycorrhizal fungi can produce a wide range of extracellular and wall-bound hydrolytic and oxidative enzymes which digest N- and P-compounds that are present in the SOM, and more particularly in proteins, ligno-cellulose and polyphenol-protein complexes, in addition to their contribution of the cycling of C that was discussed above (Leake & Read, 1990; Hodge et al., 1996; Gramms et al., 1998; Tibbett et al., 1999; Burke & Cairney, 2002; Leake et al., 2002). The activities of these fungal enzymes play an important role in the dynamics of geochemical cycles and in mobilising and transferring nutrients from SOM to forest trees.

Mobilising of N and P from SOM

The release of smaller organic molecules, which are potential sources of N or P for ectomycorrhizal fungi and other organisms in the soil, are the direct consequences of decomposition of the SOM by extracellular enzymes. The N organic compounds from humified material, plant litter or dead microbial cells, range from simple amino acids, amino sugars and nucleotides to chitin and polypeptides complexed with polyphenols (Leake & read, 1990; Lindahl & Taylor, 2004; Nygren et al., 2007). A wide range of aminoacids and a large proportion of the N that has been assimilated that is transmitted to the host plant is utilised by the ectomycorrhizal fungi (Plassard et al., 2000; Taylor et al., 2004). Many studies have therefore, focused on the production of extracellular proteases by ectomycorrhizal fungi (El Badaoui & Botton, 1989; Bending & Read, 1995; Tibbett et al., 1999; Nehls et al., 2001b; Nygren et al., 2007). It has been usual to infer protease activity from the ability of the ectomycorrhizal fungi to grow in pure culture with protein as the only source of N (Yamanaka, 1999; Lilleskov et al., 2002) or by the quantification the production of protease by the use of fluorescent substrates such as FITC-BSA (Leake & Read, 1989; Bending & Read, 1995; Tibbett et al., 1999). The production of enzymes is repressed or reduced under natural conditions by many environmental factors. It has been found in many fungi, particularly in Hebeloma crustuliniforme, that the production of extracellular protease is repressed by ammonium (Zhu et al., 1994). This variability in forest soils of extracellular enzymes that mobilise N and reflect the adaptation to high or low availability of inorganic N. Fungi that colonise sites that contain a highly available N (nitrate or ammonium) may indeed be less likely to use complex organic forms of N such as proteins (Lilleskov et al., 2002). The secretion of proteases is also regulated by pH, as has been demonstrated by 2 aspartic proteases from Amanita muscaria (Nehls et al., 2001b). Direct effects of pH and temperature on the activity of protease have been reported in the enzyme fraction that is secreted by birch roots that are colonised by Paxillus involutus (Bending & Read, 1995) of the mycelium of Hebeloma in pure culture (Tibbett et al., 1999). In this respect, informative data is provided by the genome sequence of the ectomycorrhizal fungus L. Bicolor. The number of putative proteases (116 members) that were identified, for instance, is comparatively large compared with other fungi that have been sequenced such as Coprinopsis cinerea and Cryptococcus neoformans Martin et al., 2008). A role may be played in the degradation of decomposing litter by aspartyl-, metallo- and serine proteases (Lindahl et al., 2007). That L. bicolor seems to be able to use N of organic matter from plant or animal `origin is supported by this recent genomic data.

In forest soils most of the total P present is in the form of complex molecules such as inositol phosphate, nucleotides and phospholipids (Criquet et al., 2004). Orthophosphate ions, the only form in which it is taken up by microorganisms and plants (Rao et al., 1996) are released into the soil solution as a result of the activities of phosphatase. Phosphate has been classified in different groups, such as phosphomonoesterases, which have been studied extensively in soil, litter (Dinkelaker & Marschner, 1992; Turner et al., 2002), and ectomycorrhizal fungi (Eleanor & Lewis, 1973; Tibbett et al., 1998a; Buée et al.,, 2005). The regulation of these extracellular and surface bound phosphatases by inorganic P (Pi) in pure culture of fungi (Antibus et al., 1996; Mousain & Salsac, 1986, Tibbett et al., 1998b, c) and the root tips of ectomycorrhizas (Alexander & Hardy, 1981; Jentschke et al., 2001). The hypothesis of the active role and ecological importance of ectomycorrhizal fungal hyphae and mycorrhizas in the acquisition of P under conditions of P deficiency, have been supported by these studies. It appears that ectomycorrhizal phosphatases have an optimum pH that approaches that of the native soil of the fungus (Antibus et al., 1986; Tibbett et al., 1998b; Pritsch et al., 2004) and phosphomonoesterase activity is contributed to the soil at the same rate as saprotrophic fungi (Colpaert & Van Laere (1996). Moreover, temperature controls strongly phosphomonoesterase production and activity (Tibbett et al., 1998b,c).

Diversity of ECM species for their ability to mobilise nutrients from SOM

Ectomycorrhizal communities are frequently rich in species of fungi (Buée et al., 2005; Izzo et al., 2005). Possibilities are opened for functional complementarity and, therefore, greater resilience of the host trees that are facing environmental stresses, by differences in their capacities to mobilise nutrients from SOM. It is difficult, however, to discuss the functional diversity of ectomycorrhizal fungal communities because of the low number of studies that have been carried out in situ at the forest stand scale. Several authors have, nevertheless, described that under controlled conditions the specific or intraspecific variations of the use of nutrient from different organic sources by ectomycorrhizal fungi. Only a small number of species of ectomycorrhizal fungi (about 50) have been studied for their capacities to mobilise organic N (Nygren et al., 2007), but the important variability of these proteolytic abilities has been demonstrated (Lilleskov et al., 2002; Nygren et al., 2007). The majority of species that have been examined have been grown because of the easiness to grow them in pure culture, though the genera that are most rich in species in ectomycorrhizal communities (such as Cortinarius, Lactarius, Russula or Tomentella sp.) are very difficult to isolate and culture in vitro. As a consequence, the enzymatic capabilities of these fungi are to a large extent unknown. Some authors have developed bioassays to measured metabolic activities of different mycorrhizal morphotypes directly from root tips that were collected in situ and corresponding to the actual species richness of the ectomycorrhizal community, in order to circumvent this problem (Pritsch et al., 2004; Courty et al., 2005, 2007; Buée et al., 2007). The intraspecific functional diversity for proteolytic capacity has also been evaluated for a few species (Anderson et al., 1999; Sawyer et al., 2003; Guidot et al., 2005). E.g., there were important intraspecific variations in the use of different sources of inorganic N among 22 different haploid strains of H. cylindrosporum growing in pure culture. Different studies have found evidence (Taylor et al., 2000; Peter et al., 2001; Avis et al., 2008) that the diversity and proteolytic capabilities of ectomycorrhizal fungi are greater in the podzolic boreal soils with mor-type humus, where mineralisation of N is poor, than in soils with mull-type humus of temperate forests. The production of extracellular phosphatases can vary depending of the species of fungus, and even on the strain (Meyselle et al., 1991; Cairney & Burke, 1996; Tibbett et al., 1998b, 1998c; Buée et al., 2005; Courty et al., 2005), as has also been shown for N mobilisation.

Trophic interactions between ECM fungi and other soil microbes

Between symbiotic fungi within ectomycorrhizal communities the interactions extend to larger fungal communities which include species that are saprophytic, as has been reported by Lindahl et al. (1999), who demonstrated the translocation of ³²P in a microcosm system between mycelia that were interacting of a wood-decomposing and ectomycorrhizal fungi. Moreover, some strains of soil prokaryotes could have the ability to catalyse the oxidation of various phenolic substances (Claus, 2003; Claus & Decker, 2006). Finally, the ability to degrade organic matter that was detected in mycorrhizal roots may also be a reflation of the complexity of the whole ectomycorrhizosphere microflora (Frey-Klett et al., 2007).

Courty, P.-E., et al. (2010). "The role of ectomycorrhizal communities in forest ecosystem processes: New perspectives and emerging concepts." Soil Biology and Biochemistry 42(5): 679-698.