Moving beyond the black‐box: fungal traits, community structure, and carbon sequestration in forest soils

‘… shifts in species traits, both within and among fungal guilds, may be key determinants of carbon sequestration in forest soils.’ The researchers use a natural island-based successional gradient to show that younger soils in the chronosequence (i.e. on larger islands) had a higher abundance of ectomycorrhizal (ECM) fungal species that produce rhizomorphic exploration types (Agerer, 2001) vs older soils (i.e. on smaller islands), which had more ECM fungi that produce diffuse mycelial exploration types. They also document shifts in fungal guild prevalence across islands, with a change from larger islands being dominated by ECM fungi to smaller islands having a greater proportional abundance of ericoid mycorrhizal (ERM) fungi. Combining these results with the increased soil C accumulation observed on smaller islands (Clemmensen et al., 2013), Clemmensen et al. (2015) suggest that the shifts in fungal community structure may in fact be driving the sequestration of C in SOM. Their argument is based on two aspects of the observed changes. First, they reason that ECM fungi with rhizomorphic exploration types, which dominate on larger islands, produce mycelia where the hyphae at the leading fronts are highly ephemeral and rapidly decompose after turnover. Furthermore, rhizomorphic ECM fungi may be particularly efficient in recycling their own biomass. Together, these traits would lead to fast turnover of ECM fungal tissues and reduced C input into SOM pools. Conversely, ECM fungi producing more diffuse exploration types have less efficient recycling of their tissues, resulting in a relatively larger contribution of necromass into soil C cycles after their death. Although there is evidence showing that rhizomorphic wood-rot fungi are quite efficient recyclers of their own biomass (Boddy, 1999), to our knowledge, trade-offs among exploration type, decomposition rate, and biomass recycling for ECM fungi have yet to be demonstrated. The second part of their logic is that ERM fungi, which dominate on smaller islands, frequently possess heavily melanized hyphae, a fungal trait that appears to be particularly important in determining the decomposability of fungal necromass. Research in other systems has shown that fungal necromass decomposition is strongly negatively affected by increasing melanin concentration (Fernandez et al., 2013; Fernandez & Koide, 2014). Clemmensen et al. (2015) provide additional support to this pattern by showing significant correlations between the abundance of melanized fungi and C accumulation in SOM. While the authors correctly acknowledge that the correlative nature of their study does not allow causation to be inferred (i.e. whether fungal traits drive C sequestration or vice versa), taken together, the shifts in these key fungal traits provide intriguing evidence about the directionality of this relationship. There are a number of possible explanations for why soil fungal community composition and soil C sequestration may be causally linked (Fig. 1). Clemmensen et al. (2015) focus on the potential effects of chemical recalcitrance of mycorrhizal fungal necromass on the accumulation of fungal derived carbon in SOM. With regard to melanized fungal necromass, the physiochemical properties of melanized hypae have also been noted to have higher bonding interaction with soil mineral components compared to hyaline hyphae (Fomina & Gadd, 2003). This latter factor may result in physiochemical protection of this C, which would also result in increased incorporation into stable SOM. Along with these direct effects on C accumulation through mycorrhizal inputs, fungal hyphae are directly involved in the stabilization of soil C through soil aggregate formation and stabilization (Rillig et al., 2015, this issue of New Phytologist, pp. 1385–1388). Soil particles are aggregated through the activity of fungi (and fine roots) and as a result the C contained in these aggregates is protected from decomposition processes (Schmidt et al., 2011; Rillig et al., 2015). Given the importance that morphological traits of fungal mycelia have on the likelihood of encountering and interacting with soil particles (Rillig et al., 2015), shifts in community structure from mycorrhizal fungi with rhizomorphic to diffuse exploration strategies likely have strong effects on these processes as well. ECM fungi exhibiting a diffuse and medium distance exploration types have been shown to have greater coverage per area of soil occupied than long distance rhizomorphic exploration types (Weigt et al., 2011). This greater coverage of a given volume of soil may increase C protected through aggregate formation and stabilization. ‘ERM fungi and diffuse exploration type ECM fungi generally increase in abundance with soil depth across the chronosequence.’ While this new study provides exciting insight into the influence of mycorrhizal fungi on C sequestration in soils, the generality of its findings remain to be tested. Plant C allocation to fungal symbionts may differ greatly across ecosystems (as has already been demonstrated for ECM fungi; Hobbie, 2006), which may alter the importance of root associated fungal C that enters into stable SOM fractions. Utilization of chronosequences like the one used in Clemmensen et al. (2013, 2015) is a powerful approach to understand processes that occur on longer timescales (Dickie et al., 2013; Martínez-García et al., 2015, this issue of New Phytologist, pp. 1565–1576) and comparing similar temperate and tropical chronosequences is one promising direction for assessing the robustness of their findings. In addition to correlative approaches, manipulative experiments involving long-term soil incubations of isotopically-labeled fungal necromass coupled with high-resolution analytical chemistry techniques will be key to providing a mechanistic understanding of sequestration of mycorrhizal fungal C in soils. In particular, experiments examining the relative roles of chemical, physical, and physiochemical protection of mycorrhizal fungal C from decomposition will greatly enhance our understanding of mycorrhizal influence on C sequestration in soils. Finally, the incorporation of fungal necromass inputs into global C cycle models will also be an important next step, given the large amount of C entering the soils as mycorrhizal fungal biomass (Clemmensen et al., 2013) and the differences in the biochemical and morphological traits of these inputs depending on ecosystem age (Clemmensen et al. (2015). The authors thank L. Lofgren for the digital rendition of Figure 1 and M. Öpik for helpful input on an earlier version of this commentary.