Mycorrhizal fungi and environmental change: the need for a mycocentric approach

Mycorrhizal fungi, being symbiotic organisms, have to be studied in association with their host plants, both for reasons of practicality [many of these fungi, especially arbuscular mycorrhizal (AM) fungi, are obligate symbionts] and for our understanding of their basic biology, let alone ecology. However, in many cases this has resulted in mycorrhizal fungi being viewed as mere extensions to the host plant root systems (Fitter et al., 2000). Fitter and colleagues have argued that the mycorrhizal fungal partner needs to be considered as an organism in its own right with its own interests, for example in terms of carbon (C) use (Fitter et al., 1998; Robinson & Fitter, 1999; Fitter et al., 2000; Fitter et al., 2004). This idea that mycorrhizas should be studied from a more ‘mycocentric’ perspective has been evaluated in this issue (pp. 859–868) by Alberton et al. using a meta-analysis approach to compare both mycorrhizal fungal and plant responses to elevated CO₂. This is a thought-provoking attempt at demonstrating the need to consider the two partners in the mycorrhizal association as separate entities with potentially conflicting interests.

‘To understand fully the functioning of mycorrhizas (and their response to environmental change), both partners, albeit intimately linked, must be considered as separate organisms with possible conflicting interests’

As is noted by Alberton et al., certain mycorrhizal parameters are problematic, especially when attempting to separate the fungal response to an environmental variable from that of the host plant. There is also the difficulty associated with comparing the response of mycorrhizal parameters – for example, comparing the response of extraradical mycorrhizal hyphae (normally given in length or biomass per unit soil) to elevated CO₂ with the response of the fraction of root length colonised (i.e. a percentage) to elevated CO₂ (the response of total internal mycorrhizal hyphal length would be more appropriate). The authors note, as others have done, that percentage root length colonised is not an ideal parameter for studying the mycorrhizal association. I concur, but would like to point out that it does, however, especially in combination with data on extraradical mycorrhizal density, give an approximation of changes in carbon allocation pattern between the host plant and the fungus – the value of using percentage root colonisation as a parameter depends on what question is being asked. Nonetheless, the general conclusion of the paper, which I agree with, is that to understand fully the functioning of mycorrhizas (and their response to environmental change), both partners, albeit intimately linked, must be considered as separate organisms with possible conflicting interests (Fig. 1).

Figure 1. Conceptual representation of an (arbuscular) mycorrhizal association between a plant and a fungus. The list of attributes given in italics represent key functions for the organism in question (i.e. plant or fungus). Although intimately linked at the mycorrhizal interface, the mycorrhizal fungal (exchange) structures within the roots, both organisms may behave quite independently in terms of growth and reproduction. In this simplified case of an arbuscular mycorrhiza, the fungus receives all of its carbon from the plant. However, in nature, any given fungus is likely to be receiving carbon from several different plants, which in turn may be in mycorrhizal association with several different fungi.

Carbon allocation pattern at elevated CO₂

A nice finding from the study by Alberton et al. was that the growth response ratios for the plant and fungal partners in the mycorrhizal association's response to elevated CO₂ were very similar, or in other words that the allocation of C between the plant and fungal partners remained relatively unchanged by elevated CO₂. This has also been the conclusion drawn in various reviews on this topic (Staddon & Fitter, 1998; Staddon et al., 2002; Fitter et al., 2004). It would seem to be the case, therefore, that on average there is no alteration to the carbon allocation patterns between mycorrhizal plant and fungal partners as a result of increased C availability at elevated CO₂. This is in many ways counterintuitive because one would expect that as more C is fixed by plants at elevated CO₂, then more should be available for mycorrhizal fungal growth.

Fate of mycorrhizal carbon in AM fungi

In terms of their internal C allocation, mycorrhizal fungi behave like any other organism. AM fungi allocate carbon to intra- or extraradical structures, depending on environmental conditions and their nutritional status (Douds et al., 2000). Structurally, AM fungi may invest in hyphae, arbuscules or vesicles inside the root or in the external mycelial network, which contains hyphae of different diameters and lifespan (Friese & Allen, 1991). Many of these structures, especially the arbuscules (Read, 1991) and much of the hyphal network in the soil (Friese & Allen, 1991; Staddon et al., 2003a) are short-lived (less than a week). These short-lived structures are most likely to be those involved in foraging in and nutrient uptake from the soil, the branched absorbing structures (Bago et al., 1998), and phosphorus transfer to the plant, the arbuscules (Ezawa et al., 2002). The internal hyphae and a ‘backbone’ of larger hyphae in the mycelial network live for considerably longer – the organism can be viewed as having a relatively stable component (located both inside and outside the roots) which has continuously changing short-lived appendages. Indeed, it is known that some mycorrhizal hyphae of the mycelial network in the soil can persist for several months in the field (Friese & Allen, 1991). Depending on the environmental conditions and the level of stress experienced by the fungus, AM fungi invest in storage structures, such as lipid-rich vesicles (Mosse, 1973), or reproduction, i.e. spores.

Mycorrhizal fungi-derived carbon in the soil

In the context of global environmental change, mycorrhizal fungi play a central role in the terrestrial C cycle. There is currently little information on the input of carbon to the soil via the extraradical mycorrhizal mycelium. However, two key aspects of mycorrhizal functioning, namely (a) the direct and rapid acquisition of recent photosynthate (Johnson et al., 2002) and (b) the rapid turnover of the hyphal network in the soil (Staddon et al., 2003a), mean that there is real potential for mycorrhizal fungi to act as a significant pathway for carbon sequestration into the soil. Furthermore, AM fungal biomass, alive and dead, in the soil may account for a very large proportion of the soil microbial biomass (Olsson et al., 1999), and the mycelial network also allows the movement of carbon into the bulk soil. There are several ways in which mycorrhizal carbon may enter the soil: (a) passive carbon losses from the mycelial network (similar to leaching and exudations from roots); (b) grazing of the extraradical hyphae by soil fauna (and subsequent defecation); and (c) hyphal turnover.

Until recently, the rate of extraradical mycorrhizal hyphal turnover in soil was unknown, but thought to be rapid – of the order of days, rather than weeks (Friese & Allen, 1991). Direct measurement, by accelerator mass spectrometry, of the ¹⁴C content of extraradical mycorrhizal hyphae after exposing the host plant to ¹⁴C-dead CO₂ has demonstrated that the majority of hyphae in the mycorrhizal mycelial network live for 5–6 d (Staddon et al., 2003a). This figure can be viewed as an intrinsic value for mycorrhizal hyphal turnover under semisterile conditions – in other words, there were no soil animals present, which could have otherwise speeded up the turnover. As emphasised by Zhu and Miller (2003), this rapid turnover of mycorrhizal hyphae does not preclude a key role for AM fungi in soil carbon sequestration. Decomposition of mycorrhizal hyphae has received very limited research attention (Steinberg & Rillig, 2003), although, in the field, most of the mycorrhizal mycelial network may be dead (Staddon et al., 2003b). The hyphal cell walls contain chitin, which is a very recalcitrant compound (Zhu & Miller, 2003), and, furthermore, AM fungi also produce glomalin, an even more recalcitrant protein (Steinberg & Rillig, 2003), which has been reported to be the most common protein in soil (Wright & Upadhyaya, 1996). It is therefore feasible that glomalin may be a key mycorrhizal compound contributing to the long-term soil carbon pool (Rillig et al., 2003). These issues must be addressed if we are to quantify the role of AM fungi in soil carbon sequestration and the contribution of mycorrhizal-derived carbon to soil carbon storage (Lovelock et al., 2004).

Improved and new stable carbon isotope methods (Staddon, 2004) will be invaluable in obtaining better quantitative and qualitative data on carbon input to the soil via mycorrhizal fungi. A clearer understanding of the role of mycorrhizal fungi in the global carbon cycle is crucial, especially as it is likely that the current and future changes to the global environment will impact upon mycorrhizal functioning (Staddon et al., 2003c), and hence on their role in the soil carbon cycle (Treseder & Allen, 2000). It is also worth emphasising that the feedbacks (Miller & Kling, 2000) which exist between the mycorrhizal community and the wider soil ecosystem and vegetation (van der Heijden, 2002) may also be altered by environmental change, complicating predictions on the role of mycorrhizal fungi in soil carbon sequestration in the future.