Introduction

1.1 The Last 25 Years

The British Mycological Symposium, volume Decomposer Basidiomycetes (Frankland et al., 1982), identified lines of enquiry into basidiomycete biology and ecology that proved immensely fruitful in the following 25 years. Three chapters in that volume are still particularly relevant to current questions in basidiomycete nutrient uptake and translocation, and its importance in ecosystems. Quantitative investigation (Frankland, 1982) established the abundance of basidiomycete mycelium and its significance in wood decomposition in ecosystems. A conceptual basis was established with Swift's (1982) model of the decomposer subsystem of woodland ecosystems, in which basidiomycetes are primary in the detrital food web, utilizing lignocellulose in carbon/energy capture, and collecting mineral nutrients. The fundamental importance of population genetics was established as a determining factor in the physical structuring of basidiomycete mycelial individuals in populations, affecting their ecosystem function (Rayner and Todd, 1982).

1.2 Translocation through Mycelial Cords Underlies Key Ecosystem Functions of Basidiomycetes

Since 1982, we have come to recognize the importance of basidiomycete mycelia, particularly species that form conducting cords or rhizomorphs, as conduits for nutrients through soil (Cairney, 2005). Although fungal translocation had been well described physiologically, a breakthrough in appreciating its ecological significance was the publication (Simard et al., 1997) of results of a field experiment that demonstrated net carbon flow between ectomycorrhizal tree seedlings in the field. This led the editors of Nature to coin the phrase 'wood-wide web' for the concept of an underground fungal resource network that could be tapped by plants, and could have important effects on aboveground productivity and diversity. The path of carbon and nitrogen through cords of ectomycorrhizal mycelium has been mapped using imaging techniques including real-time radioisotope digital imaging (Leake et al., 2004). The notion of basidiomycete mycelium as an underground infrastructure for ecosystems, implied by the metaphor of the 'wood-wide web', is further supported by the finding that achlorophyllous plants, formerly believed to be parasitic on plants, are myco-heterotrophic (Leake, 2005). They 'cheat' the fungal wood-wide web, drawing off carbon/energy instead of supplying it by photosynthesis. Some mycohetero-trophs rely on specific mycelium for seedling establishment as well as for sustained growth (Bidartondo and Bruns, 2001). Thus, the basidiomycete networks of woodland contribute to plant diversity as well as productivity.

Fungal networks conduct mineral nutrients, including nitrogen, phosphorus, potassium, calcium and magnesium (Jentschke et al., 2001), as well as carbon compounds—'the energy currency of the ecosystem' (Read, 1997). Cords channel bidirectional flows (Lindahl et al., 2001), though the mechanism and pathways remain obscure. They extend the resource-gathering range of individual fungi, enabling individual mycelia to extend over areas of metres, inferred in woodland from the pattern of clonal distribution (Rayner and Todd, 1982; Burnett, 2003), and directly visible in cord-formers that grow over the surface of masonry in buildings (Ramsbottom, 1953; Money, 2007). Translocation of both carbon and mineral nutrients, including amino acids, has been shown in both ectomycor-rhizal (He et al., 2003) and saprotrophic cords (Tlalka et al., 2007; Watkinson et al., 2006; Bebber et al., 2007). By mobilizing resources and information gathered over the whole network, and deploying accumulated resources at a localized site of biosynthesis such as sites of colonization, attack or sporophore construction, cords confer 'network-enabled capability' (Smith, 2006) on the mycelium. Because of these adaptive movements of their resources through mycelial networks, fungi contribute significantly to carbon sequestration by importing carbon into the soil from plants (Leake et al., 2004) and from decomposing lignocellulosic litter (Frey et al., 2003).

1.3 The Translocation Mechanism is likely to be Similar in Saprotrophic and Ectomycorrhizal Basidiomycetes

The functional overlap between symbiotic and saprotrophic networks has only recently been recognized (Read and Perez-Moreno, 2003). Species with both strategies for carbon capture from plants—utilizing dead remains and living roots—co-exist in forest organic horizons and litter layers (Tedersoo et al., 2003). Experiments with isotope markers in microcosms show that nutrient exchange can occur between mycelium of decomposers and symbionts (e.g. Lindahl et al., 1999).

Although species that exploit plant litter for minerals are in a minority of ectomycorrhiza, they are among the most abundant fungi in nitrogen-limited forests (Read and Perez-Moreno, 2003). Interestingly, it is in these podsolized boreal forest soils that the most marked spatial separation of saprotrophic and ectomycorrhizal basidiomycete species and their associated nutrient cycling functions has been reported (Lindahl et al., 2007).

It is now appropriate to consider the physiology and underlying cellular machinery of both ectomycorrhizal and saprotrophic basidiomycete translocation together, because we know from molecular phylogeny that the difference between symbiotic and saprotrophic biology does not correspond with a fundamental taxonomic or phylogenetic separation in basidiomycetes. Ectomycorrhizal symbiosis is an evolutionarily unstable relationship that has been both gained and lost (Hibbett et al., 2000). Recently published basidiomycete phylogenies (Hibbett et al., 2000; Binder and Hibbett, 2002; Hibbett and Binder, 2002; Mon-calvo et al., 2002) indicate that the saprotrophs Coniophora and Serpula are in the Boletales clade with the ectomycorrhizal Suillus and Paxillus, while another pair of sister taxa is the ectomycorrhizal Tomentella and saprotrophic Phanerochaete. Tomentella, which produces resupinate sporophores on dead wood, has been shown only recently by molecular analysis of root tips, to be an ectomycorrhizal genus (Koljalg et al., 2000). Some mycorrhizal basidiomycetes that decompose litter also have the ability to obtain mineral nutrients saprotrophically. For example, Paxillus involutus can obtain nitrogen and phosphorus from tree leaf litter and return it, via mycelial cords connected to the ectomycorrhizal mantle, to roots of tree seedlings (Perez-Moreno and Read, 2000).

Translocation mechanisms in ectomycorrhizal basidiomycetes can be interpreted from experiments with similar networks in the more experimentally tractable saprotrophic basidiomycetes. Microcosm studies of the physiology and mycelial topology of foraging cord formers show similar context-cued cord development and network organization centred on rich unit carbon sources (roots or pieces of dead wood). These form the hubs from which mycelium grows out to sweep the surrounding area for further resources. Mineral nutrients are acquired by diffuse assimilatory mycelium which is both supplied by and feeds back into the mass flow cord system (Olsson et al., 2002; Boddy and Jones, 2007).

1.4 Translocation might Function as a Homeostatic Mechanism in Fungi Adapted to Utilize Spatially and Temporally Separate Carbon and Nitrogen Resources

In boreal and temperate forests carbon and nitrogen sources may be spatially separate, and limiting nitrogen must be gathered where and when it becomes available, from soil, canopy through-fall, lea litter or other detritus. Biogeo-graphical data (Read, 1991) show that plants with basidiomycete ectomycor-rhizas predominate in nitrogen-limited forest biomes, and that ectomycorrhizal symbionts with cord-forming mycelium (Agerer, 2001) capable of acquiring nitrogen in organic form are common in such ecosystems (Read and Perez-Moreno, 2003). Basidiomycete nitrogen-scavenging networks adapt host plants to growing in slow-mineralizing acid soils, where almost all available nitrogen is held in the biota or in very slowly turning over tannic compounds in humus (Richter and Markewitz, 2001; Dighton, 2003; Bardgett, 2005). Wood decomposing bas-idiomycetes of such habitats are mainly brown rot fungi. These generate humus by a decay process that leaves a slow-turnover lignin-rich residue, with which nitrogen becomes bonded. Up to 30% of carbon sequestered in boreal forest is in this form (Ryvarden and Gilbertson, 1993). Nitrification hardly occurs (Davidson et al., 1992; Stark and Hart, 1997), and when any available nitrogen is released it is immediately absorbed by competing plants and microbes (Kaye and Hart, 1997).

The rapid uptake and directed translocation of amino acid, observed by realtime radioisotope imaging in corded mycelia of Phanerochaete velutina (Tlalka et al., 2002; Watkinson et al., 2006; Bebber et al., 2007), may be adaptive to competitive nitrogen capture by the fungal network (Ettema and Wardle, 2002). It confers spatial advantage for enabling the fungus to remove captured nitrogen to wood resources where competition may be less. Similar preferential phosphorus allocation to carbon-rich resources has been shown with isotope labelling in microcosms (Wells et al., 1999).

A conceptual model of nitrogen dynamics in such environments (Lindahl et al. , 2002) places fungal mycelium as a central controlling network for all the major mineral nutrient fluxes between soil, ectomycorrhizal and saprotrophic mycelial networks. The conducting activity of such mycelial networks is critical to exploiting their heterogeneous environment, in which, in the authors' words, 'carbon and nitrogen resources are spatially uncoupled'. The implication is that fungi in these habitats are adapted to gather carbon and energy from one part of their mycelial networks and nitrogen from another. By translocation within the network, a mycelium is enabled to reconcile these two essential resources for biosynthesis. Fungal nitrogen translocation can have a rate-determining effect on ecosystem carbon flux. Nitrogen import through mycelium to N-poor lignocellulose carbon resources results in faster decomposition rates (Beare et al., 1992; Frey et al., 2000). This occurs as a side-effect of the fungal adaptation which enables the individual mycelium to import nitrogen scavenged from soil into newly acquired carbon resource in the form of plant litter at the soil surface. In other words, fungi are adapted by natural selection, not to perform ecosystem services, but to maximize their own fitness. We do not know how translocation is regulated for metabolic home-ostasis, but it evidently requires a coordinated network-wide response to differences in internal levels of different nutrients. A requirement to sense and respond to spatial differences in internal carbon and nitrogen levels offers an explanation for the widespread morphogenetic sensitivity of fungi to intracel-lular C:N ratio (Watkinson, 1999).

Cords developing secondarily in an established mycelial network, as occurs in Serpula lacrymans and Coniophora puteana, form by linear aggregation and differentiation of hyphae around a central low resistance channel, with surrounding tissue of which the anatomy and function is still obscure, embedded in accretions of extracellular matrix material (Jennings and Watkinson, 1982). Cords are elicited under conditions of N limitation or when hyphae themselves become the main source of nutrients. On uniformly nutrient-rich media, and when assimilating or invading cellulosic resources, mycelium takes the form of separate hyphae. Under nitrogen limitation in initially defined media, and in mycelium connecting two separate cellulose resources, cords differentiate. Nutrient perfusion prevents the cord development. Physiological evidence points to intracellular amino acid as a cord-inducing signal (Watkinson, 1999). Nitrate as sole nitrogen source induces early autolysis and cord formation, and suppresses secondary metabolism.

Metabolic fungal adaptations to nitrogen limitation include amino acid uptake transporters with a range of substrate preferences and affinities for scavenging uptake from dilute solutions or nitrogen-rich resource. Global metabolic regulation of transcription of genes is also involved in nitrogen assimilation or dissimilation, to adapt to local or transient nitrogen starvation or repletion (Caddick, 2004).

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