These authors contributed equally to this work.
Arbuscular mycorrhizal fungi – short-term liability but long-term benefits for soil carbon storage?
Article first published online: 23 NOV 2012
© 2012 The Authors. New Phytologist © 2012 New Phytologist Trust
Volume 197, Issue 2, pages 366–368, January 2013
How to Cite
Verbruggen, E., Veresoglou, S. D., Anderson, I. C., Caruso, T., Hammer, E. C., Kohler, J. and Rillig, M. C. (2013), Arbuscular mycorrhizal fungi – short-term liability but long-term benefits for soil carbon storage?. New Phytologist, 197: 366–368. doi: 10.1111/nph.12079
- Issue published online: 18 DEC 2012
- Article first published online: 23 NOV 2012
- arbuscular mycorrhizal fungi (AMF);
- elevated CO2;
- soil carbon sequestration
The interaction between plants and mycorrhizal fungi represents a major link between atmospheric and soil-contained carbon (C). In order to estimate the fate of atmospheric CO2 under the projected increases in the upcoming century, ranging from an increase of 20% to > 200% compared with current concentrations (Pachauri & Reisinger, 2007), it is crucial to understand how plants and mycorrhizal fungi either buffer or exacerbate atmospheric CO2 rises through their effects on soil C sequestration.
Indirect evidence suggests that arbuscular mycorrhizal fungi (AMF) generally stimulate soil carbon pools (Wilson et al., 2009), and experience enhanced growth under elevated CO2 (eCO2) (Antoninka et al., 2011), leading to the assumption that they will buffer atmospheric CO2 increases. However, long-term experiments under eCO2 show both increased carbon storage (Iversen et al., 2012) and accelerated decomposition (negating the effect of the increase of soil carbon inputs; Phillips et al., 2012), leaving the question as to whether soils will buffer against CO2 increases wide open. While there is a dearth of direct empirical evidence regarding the involvement of AMF in soil C storage processes under conditions of global change, there is uncertainty about how component processes leading to soil C storage will be affected.
Recently, Cheng et al. (2012) presented a compelling body of evidence to suggest that AMF may diminish rather than enhance soil C pools in the topsoil. Their findings are based on the observation that, in the presence of AMF, fresh above-ground plant litter decomposes faster, in particular at eCO2 and increased nitrogen (N) concentrations (Cheng et al., 2012). This observation suggests that AMF can accelerate decomposition and can even lead to a loss of soil C pools, at least in the short term. However, we feel that other parts of the soil C equation will need to be resolved in order to fully understand how AMF affect long-term soil C-sequestration potential. This is because short-term experiments do not account for potential increases in organic matter (OM) of plant or microbial origin triggered by increased decomposition; long-term (decadal scale) effects of soil biota such as AMF can be qualitatively different from short-term effects; and pulse increases of CO2 and N affect soils in a way that may not represent a system where CO2 and N are at consistently higher concentrations.
Soil C sequestration is the net build-up of C in the entire soil profile through accumulation of OM from plant, fungal (and other microbial) and animal origins. Decomposition of OM is an ongoing process, and snapshot rate assessments must therefore be interpreted with caution. If a particular nutrient (e.g. C or N) is elevated, this may lead to accelerated decomposition, but conclusions about soil C gain or loss can only be drawn if the effect of biomass increases of all biota is also incorporated into the equation (Fig. 1a). This becomes apparent in a simple model where AMF are allowed to produce recalcitrant compounds (such as various polysaccharides (Kögel-Knabner, 2002) and glomalin, in line with experimental observations; Rillig, 2004) that contribute to the future OM fraction (see Fig. 1b). In the short term, an AMF-mediated increase in decomposition of labile plant litter may lead to a reduction of soil C. However, the C balance is offset by a long-term gain in recalcitrant compounds (Fig. 1a). Contributions of AMF are likely to be further amplified through physically protecting OM from decomposition by means of soil aggregation (Rillig, 2004) and via a general increase in plant productivity and hence significantly higher litter input (Hoeksema et al., 2010).
The principal mechanism by which AMF are proposed to stimulate soil C efflux is through priming of decomposers, which is a commonly observed soil-biotic response to increased (labile) OM deposition (de Graaff et al., 2010). However, whether this stimulation of soil saprobes is a permanent effect will require further study: C pulses and the resulting soil fungal community responses are a well-appreciated side-effect of sudden-onset CO2 exposure designs, which disappear when CO2 is gradually increased (Klironomos et al., 2005). Such sudden increases in atmospheric CO2 concentration are unlikely to happen in the near future. By contrast, other parameters will likely change under permanently altered amounts of resources, for instance litter quality. Decomposability of plant litter is known to decrease following plant exposure to eCO2 (Norby et al., 2001), and has the potential to buffer soil C concentrations against effects predicted from short-term experiments. Thus the magnitude of priming effects through AMF under permanent eCO2 (as opposed to pulse elevation) must be scaled against indirect effects on litter quality to fully appreciate the contribution of AMF to plant-derived soil C concentrations.
A way in which short-term experimental studies could control for some of these effects is to include additional treatments where soil and OM (thus controlling for factors such as soil aggregation and quantity and quality of litter) have been preconditioned, to the extent feasible, according to experimental treatments of interest (e.g. ambient vs eCO2; low vs high N; + vs −AMF) in a factorial manner. Another highly useful addition might be a treatment where plant roots but not AMF can access plant litter generated under ambient vs eCO2 concentrations (a true nonAMF treatment). Even though these approaches do not resolve all fundamental issues arising from predicting long-term processes with short-term experiments, decomposition in the eCO2 and AMF treatments can be compared between ‘uniform’ and ‘preconditioned’ (according to treatment) plant and soil material. This way we can test whether a lower C : N ratio of AMF litter than of plant litter, or other potential mechanisms discussed in Cheng et al. (2012), will negate the general increase of OM input, recalcitrant compound production, and soil stabilization effects of AMF. This would yield a crucial insight into transient and permanent effects of eCO2 and AMF.
The arbuscular mycorrhiza is clearly a multifunctional symbiosis, whose other services from a plant host perspective include plant pathogen protection (Wehner et al., 2010), phosphorus uptake and mediation of water status (Querejeta et al., 2006) (in addition to ecosystem-level services; Rillig, 2004). To base recommendations for the management of this organism group (e.g. in agriculture) on just one functional axis, such as soil C sequestration (Kowalchuk, 2012), may therefore be leading us down the wrong path. As we argue here, the detrimental influences of AM fungi on soil carbon storage presented by Cheng et al. (2012) may not be as grim as first appears. Future studies need to consider fungal-mediated processes that lead to long-term C gains (plant growth promotion effects, soil aggregation, recalcitrant mycelium products), some of which will only unfold in the decadal timescale.
We would like to thank Shuijin Hu for valuable comments on the manuscript. I.C.A. acknowledges receipt of a collaboration fellowship from the German Federal Ministry of Education and Research, and T.C. was supported by the Alexander von Humboldt Foundation.
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