Australia: The Land Where Time Began

A biography of the Australian continent 

Ectomycorrhizas and carbon cycling

Origin of carbon content in ectomycorrhizal fungi

Ectomycorrhizal fungi have 2 major sources of carbon that are potentially available to them, photosynthates from tree hosts and soil organic matter (SOM), Phloem vessels carry sucrose from the leaves to the roots. Carbon from the soil is sequestered in various compounds, such as carbohydrates, proteins, nucleic acids, chitin, fatty acids or complex phenolic molecules such as lignin. Many phytocentric models regard ectomycorrhizal fungi as extensions of the roots, and research on mycorrhizas has often been centred on the plants (Fitter et al., 2000). Courty et al. chose, in contrast, a mycocentric view for this paper, assuming that carbon is allocated between the intraradical and extraradical mycelia according to the carbon demand of the fungus rather than according the demand of the carbon autotrophic host (Fitter et al., 1998; Robinson & Fitter, 1999).

Ectomycorrhizas as a sink for photosynthates

Ectomycorrhizal fungi depend mostly on their hosts for the supply of carbon they need to complete their lifecycle under symbiotic conditions. There are 2 steps that are encompassed in the transfer of carbon from the host tree to the fugal symbiont; C exchange at the root-fungus interface and allocation from intra- to extraradical mycelium (Leake et al., 2001). It was estimated with a high uncertainty that in controlled conditions as much as 30% of the net primary production can be allocated to the Ectomycorrhizal fungal symbionts (Nehls & Hampp, 2000; Söderström, 2002; Hobbie, 2006). In forest trees sucrose is the major transport form of photoassimilates. Sucrose is hydrolysed to glucose and fructose at the root-fungus interface by acid invertases that are derived from the plant that are bound to the cell wall (Salzer & Hager, 1991). The fungal partner then takes up the monosaccharides that result from the common apoplastic interface. The transfer of glucose and fructose to the fungus is allowed by fungal hexose transporters and enables its growth (Schaeffer et al., 1995; Nehls et al., 1998, 2010a, b; Nehls & Hampp, 2000). A gradient is also generated by the fungus by converting glucose and fructose into compounds that are not used by the host plant (Hampp & Schaeffer, 1999) such as mannitol, arabitol, glycerol, and saccharides that are not reducing such as trehalose, which are the main soluble carbohydrates that are present in ectomycorrhizal fungi (Söderström et al., 1988; Martin et al., 1998). Trehalose and mannitol play the role in fungi of reserve carbohydrates and osmoprotectants (Niederer et al., 1992; Shi et al., 2002). It has been suggested that these substances contribute to the selection of particular bacterial populations in the ectomycorrhizosphere as they are exuded into the soil (Frey-Klett et al., 2005).

In ectomycorrhizal fine roots the proportions of fungal biomass ranges between 10% and 40% (Harley & McCready, 1952; Vogt et al., 1991; Kinoshita et al., 2007). This proportion depends on the C that is allocated by the plant to the fungus and on the specific requirements of C of the plant and the fungus (Bidartondo et al., 2001; Hobbie, 2006; Hobbie & Hobbie, 2006). Ectomycorrhizal fine roots on the same root system are a mixture of roots that are highly active, which are strong sinks of C of photosynthates, and ones that are less active (Högberg et al., 2008). The ectomycorrhizal biomass at the forest scale (including the ectomycorrhizal mantle) can reach up to 5,000 kg/ha in a mixed forest (Wallander et al., 2004).  The total amount of ectomycorrhizal mycelium that is produced each year can reach 600 kg/ha (Wallander et al., 2001; Nilsson et al., 2005). According to Courty et al. it appears to be possible that it could reach as high as ⅓ of the microbial biomass in coniferous forests (Högberg & Högberg, 2002). The extraradical mycelium, which is important for exploration of the soil, depends less on the growth of root responses than intraradical than does intraradical mycelium (Ceulemans et al., 1999). Ectomycorrhizal extraradical mycelial growth rates of up to 10 mm/day have been measured (Donnelly et al., 2003; Leake et al., 2004; Wallander, 2006). It is concentrated near the surface of the soil (Read et al., 2004; Querejeta et al., 2007) and contributes to the formation of fruiting bodies         (Högberg, 1999). The production of fruiting bodies depends to a large extent on the photosynthetic rate of the trees, because fruiting bodies are connected to the roots through the extraradical mycelium (Högberg et al., 2001; Kuikka et al., 2003).

About 60% of the efflux of CO₂ from the soil that results from respiration is derived from heterotrophic respiration (free-living microorganisms and soil fauna), 25% from the respiration of ectomycorrhizal mycelium (up to 35% during the period of fruiting body formation) and 15% from the respiration of root tissue (Heinemeyer et al., 2007). Ectomycorrhizal respiration, which depends on the host, fungal species and the availability of nitrogen, corresponds to 3.5-15% of the total photosynthates (Bidartondo et al., 2001; Heinemeyer et al., 2006). Dead mycorrhizas are an important component of SOM (Johnson et al., 2001; Godbold et al., 2006), and it has been shown that the ectomycorrhizal fine roots decompose more slowly than non-mycorrhizal ones (Langley & Hungate, 2003; Langley et al., 2006; Millard et al., 2007). However, the reason for this difference remains unknown to date.

Heterotrophic origin of a part of ECM carbon

Part of the C that is used by ectomycorrhizal fungi can be derived directly from SOM (Treseder et al., 2005). The use of the natural abundance of ¹³C, for instance, has been shown by Hobbie & Hobbie (2006) that soil C may contribute as much as 43% of the total C in fruiting bodies of ectomycorrhizal fungi. It was demonstrated by Durall et al., (1994) using ¹⁴C labelling that ectomycorrhizas that were formed by different species of fungi displayed different abilities to respire C from hemicellulose, cellulose, humic polymers or conifer needles. As ectomycorrhizal fungi evolved from saprophytic ancestral forms of fungi on several independent occasions, this is not surprising (Hibbett et al., 2000). This is well illustrated by the presence the presence of a broad range of genes that code for enzyme degrading complex organic compounds (i.e., lignin peroxidases, manganese peroxidases, laccases, and tyrosinases) in basidiomycetous fungi that represent several different phylogenetic clades (Chambers et al., 1999; Nehls et al., 2001a; Chen et al., 2003; Lindahl & Taylor, 2004; Luis et al., 2005; Bodeker et al., 2009). The diversity of these genes is, however, lower than in species that are exclusively saprophytic. Some species, such as L. bicolor and Amanita bisporingera are even deprived of genes that code cellulose- and hemicellulose-degrading hydrolytic enzymes and are also reduced in enzymes that degrade polyphenol (Martin et al., 2008; Courty et al., 2009; Nagendran et al., 2009). Many ectomycorrhizal fungi possess, correspondingly, extracellular and oxidative and cellulolytic activities (Bending & Read, 1995; Gramms et al., 1998), though compared with those of litter decomposing fungi these are marginal (Colpaert & Van Laerae, 1996; Koide et al., 2008). Recent studies that were based on the measurement of enzymatic activities on the tips of individual ectomycorrhizas have revealed variable laccase, β-glucosidase and the cellobiohydrolase activities that depend on the species of fungus (Courty et al., 2005, 2006; Buée et al., 2007). Nevertheless, the genome analysis of the ectomycorrhizal fungus L. bicolor, compared with that of saprotrophic basidiomycetes, showed extreme reduction of the number of enzymes that are involved in the degradation of plant cell wall; for instance, only the GH5 cellulase family was found but not sGH6 and GH7, (Martin et al.,  2008; Martin & Nehls, 2009), even if the cellulolytic capacity may be particularly well developed among some ectomycorrhizal fungi, such as Pezizales (Egger, 2006) or Tricholoma matsutaki (Kusuda et al., 2006). Also, similar loss or reduction of hemicellulose and pectin degrading enzymes were reported.

Biotic (tree phenology) and abiotic (climate) influence the activities of soil enzymes (Kang & Freeman, 1999; Fenner et al., 2005) and they seasonally fluctuate. The quality of oak litters were found, similarly, to modify the structure of the community and enzymatic capacities of ectomycorrhizas (Conn & Deighton, 2000). It is suggested by these observations that the ability of ectomycorrhizal fungi to degrade SOM might be a more fundamental trait of these species than had traditionally been inferred from their symbiotic status. There are 2 recent publications that have confirmed convincingly this viewpoint. It was found by the first one (Cullings et al., 2008) that 7 enzyme activities that were involved in the decomposition of organic matter were enhanced in the dominant ectomycorrhizal type (due to Suillus granulatus) in a pine forest in response to artificial, partial defoliation. The significance of these results might, however, be limited somewhat by the analytical procedure used homogenised ectomycorrhizas, with the result that intracellular, as well as secreted, enzymatic activities. The second work (Courty et al., 2007), addressed the fact that, in deciduous oak (Quercus) species, the quantity of carbohydrates that are nonstructural (starch and soluble sugars) in the sapwood is not sufficient in spring to support fine root respiration and elongation, bud break, and cambial activity, at the same time. Indeed, in deciduous oaks, cambial activity begins prior to bud break and continues when the leaves are not yet mature and photosynthetically active (Hinckley & Lassoie, 1981; Barbaroux et al., 2003). Working in a stand of Quercus petraea it was demonstrated (Courty et al., 2007)  that the activities of some enzymes that had been secreted were enhanced dramatically in the ectomycorrhizas formed by L. quietus, which was the dominant symbiont in the stand being studied (during this period), which suggests that the fungus responded to the shortage of carbon in the tree and, therefore, in its own mycelium, by a temporary saprotrophic lifestyle, i.e., by upregulating enzymatic activities that were capable of obtaining labile carbohydrates.

An event that is an even more challenging point of view concerning the C budget of the symbiosis is led to by these recent findings. The host tree provides the fungus with carbohydrates and the fungus provides the tree with water and mineral nutrients (bidirectional exchanges) in the typical ectomycorrhizal symbiosis (Allen, 1991; Trappe, 1994; Smith & Read, 1998). There is another type of symbiotic relation, however, plants that are non-photosynthetic and mycorrhizal fungi, in which C flows in the opposite direction (Alexander & Hadley, 1985; Molina et al., 1992; Smith & Read, 2008). It may be speculated, therefore, that some deciduous trees – such as oaks discussed above – may derive some extrastructural carbon from the fungal symbionts at peak periods of their own development, when their storage compartments are emptied. In order to test this hypothesis and demonstrate not only that such transfer can occur, but also to evaluate whether it is significant in terms of quantity of carbon is transferred, more research is needed.

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.