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Keywords:

  • carbon allocation;
  • fungal communities;
  • molecular identification;
  • nitrogen isotopes;
  • Pinus;
  • radiocarbon

With improvements in molecular techniques, identification of taxa in mycorrhizal ecology has expanded from fruitbodies to mycorrhizal roots to extraradical hyphae (Anderson & Cairney, 2004). These molecular techniques are, in general, equally applicable to saprotrophic fungi, although this important functional group has received relatively little focus in community studies (Allmer et al., 2006). Only a few studies have examined the spatial patterns of ectomycorrhizal fungi in soil profiles, and no studies have examined similar patterns for saprotrophic fungi. In this issue of New Phytologist (pp. 611–620), Lindahl et al. reported on the spatial patterns of ectomycorrhizal and saprotrophic fungi from soil profiles in a Pinus sylvestris forest in Sweden, and compared those patterns with patterns of bulk carbon:nitrogen ratios, 15N content and radiocarbon (as a proxy for age). As expected, each of these parameters increased with depth in soil profiles. The authors also reported a striking separation of the ectomycorrhizal and the saprotrophic communities, with the surface litter layer strongly dominated by saprotrophic fungi and the deeper horizons strongly dominated by ectomycorrhizal fungi. This physical separation implies that these fungal types also play separate roles in the carbon and nitrogen cycles by exploiting discrete pools of litter.

‘… these observations are the best evidence to date that the ectomycorrhizal transfer of 15N-depleted N may be a primary driver for 15N enrichment in soil profiles’

Inputs to the soil profile

  1. Top of page
  2. Inputs to the soil profile
  3. 15N as a marker of nitrogen cycling
  4. Identifying the players
  5. Acknowledgements
  6. References

The two overlapping fungal communities (ectomycorrhizal and saprotrophic) surveyed by Lindahl et al.. primarily consume carbohydrates for their metabolic requirements. Their relative abundance through the soil profile partly reflects the pattern of fresh carbon input through two main sources. Saprotrophic fungi, because of their extensive capabilities to degrade lignin, predominate where above-ground litterfall is the primary input. In contrast, the peak of relative abundance of ectomycorrhizal taxa in the F and H layers presumably reflects a related peak in below-ground carbon input via roots. The unexpected increase in the C:N of organic matter from the F layer to the lower H layer may reflect these inputs, but could also indicate that soil N is sufficiently available in the lower organic horizon to be mobilised and removed by mycorrhizal fungi. Thus, carbon inputs into boreal forest soils can be spatially separated into a discrete above-ground input to the litter surface via litterfall of foliage, twigs, and wood, and a broad zone of below-ground input that peaks in the F and H layers of the organic horizon (Fig. 1). The relative contribution of below-ground inputs and above-ground inputs, and the subsequent turnover and release of a portion of those inputs in respiration, determine patterns of radiocarbon and carbon accumulation. High inputs of recent photosynthate at depth via roots and mycorrhizal fungi may accordingly alter the assumed monotonic increase in carbon age with depth in soil profiles.

image

Figure 1. Input rates, with depth of above-ground litter, roots and mycorrhizal fungi influencing the patterns of available substrates for decomposition and the soil 15N patterns. Major chemical classes of inputs are given in italics with relative 15N content.

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From work with 13C-enriched litter in pine forests in California, Bird & Torn (2006) suggest that carbon cycling in litter is largely divorced from carbon cycling in deeper horizons, which concurs with the key role of two separate input pathways in determining carbon cycling patterns, as suggested by Lindahl et al. If the carbon flux below ground to fine roots and mycorrhizal fungi equals or exceeds the flux via litter to the soil surface, the question left by the community analysis of Lindahl et al. is this: where is the saprotrophic community to decay below-ground inputs? Is there a saprotrophic fungal community on dead roots equivalent to the one on above-ground litter? Although we know little about the saprotrophic capabilities of many ectomycorrhizal taxa, an intriguing possibility is that ectomycorrhizal fungi may have evolved good abilities to degrade the structural macromolecules (e.g. suberin) found in fine roots but not in above-ground litter. The loss of the outer cortex and the carbonized form in ectomycorrhizas of some taxa of mat-forming ectomycorrhizal fungi suggests some saprotrophic capabilities (Agerer, 1987–2006; Agerer, 1993; Lefevre & Müller, 1998). Because the fine roots colonized by ectomycorrhizal fungi are low in lignin (e.g. oak; Soukup et al., 2004) compared with above-ground litter, it is plausible that the enzymes necessary to degrade fine roots are poorly adapted for degrading lignin-rich above-ground litter.

The relative importance of above-ground inputs, roots and mycorrhizal fungi as sources for soil organic matter is a contentious topic. The best current estimates for total below-ground allocation use the carbon balance technique, in which litterfall and CO2 efflux from the soil are measured. Below-ground inputs are then estimated as the difference between CO2 efflux and litterfall (Davidson et al., 2002). Using this approach, below-ground inputs appear to be about double the above-ground litterfall globally. The partitioning of below-ground allocation between roots and mycorrhizal fungi is poorly known (Hobbie, 2006). However, improved independent estimates of allocation to roots or mycorrhizal fungi are appearing on the horizon. For roots, emphasizing root order as an important determinant of carbon allocation holds considerable promise for assessing carbon flux (Guo et al., 2004), whereas the in-growth core technique pioneered by Wallander et al. (2001) provides at least relative measures of growth of ectomycorrhizal hyphae using an easily repeatable method. However, more work is needed to put these new measurements of root and mycorrhizal allocation into an ecosystem framework. Such work would encourage ecosystem modelers to at last devote as much energy to understanding and tracking below-ground processes as is currently devoted above-ground.

15N as a marker of nitrogen cycling

  1. Top of page
  2. Inputs to the soil profile
  3. 15N as a marker of nitrogen cycling
  4. Identifying the players
  5. Acknowledgements
  6. References

The potential of natural abundance stable isotope measurements of 15N content to reveal new insights into plant-mycorrhizal functioning can be traced as far back as 1977, when Bardin et al. reported that pines colonized by ectomycorrhizal fungi were depleted by 2‰ relative to nonmycorrhizal pines. In 1996, Högberg et al.suggested that high 15N content in ectomycorrhizal fungi could account for the consistently reported 15N enrichment of soil, relative to litter, in many forest ecosystems. Subsequent field and laboratory studies (reviewed in Hobbie, 2005) indicated that fractionation against 15N during the formation of transfer compounds, such as amino acids, leads to the transfer of 15N-depleted N to ectomycorrhizal plants and the retention of 15N-enriched N in ectomycorrhizal fungi, with an intrinsic fractionation against 15N of ≈ 10‰.

Lindahl et al. reported that soil 15N content changed little before the F layer, that the relative abundance of ectomycorrhizal fungi peaked in the F and H layers, and that saprotrophic taxa dominated in the litter layer. Taken together, these observations are the best evidence to date that the ectomycorrhizal transfer of 15N-depleted N may be a primary driver for 15N enrichment in soil profiles, and that earlier suggestions of soil 15N enrichment, primarily resulting from discrimination against 15N during decomposition (Nadelhoffer & Fry, 1988), were overstated. It also suggests that little stable soil organic nitrogen is derived from inputs of root nitrogen without first being processed by mycorrhizal fungi, as such direct inputs of 15N-depleted N would decrease the 15N enrichment between litter and deeper soil horizons. This may be particularly true in ectomycorrhizal systems, where fungi colonize > 90% of the feeder roots in most communities.

Identifying the players

  1. Top of page
  2. Inputs to the soil profile
  3. 15N as a marker of nitrogen cycling
  4. Identifying the players
  5. Acknowledgements
  6. References

Lindahl et al. linked changes in C and N dynamics with the fungi found in the soil horizons. The molecular techniques they used allowed them to observe the fungi present in soil (as hyphae and with mycorrhizal roots, but potentially as spores and sclerotia; see Avis et al., 2006). Identifying the players involved allowed Lindahl et al. to assign them to broad functional groups with great confidence. Regardless of the names or taxonomic level, those fungi that could be assigned to mycorrhizal or saprotrophic functional groups were clearly separated (Figs 1 and 2, Lindahl et al.), following the changes in soil depth, age, C:N ratio, and 15N. Less clear is how this spatial separation is maintained and whether this spatial separation promotes or retards nutrient cycling and decomposition. Manipulative experiments should now be directed towards answering these questions (see Leake et al., 2002).

We know that fungal communities can be very complex, even when focusing on one group such as ectomycorrhizal fungi (Horton & Bruns, 2001). Lindahl et al. accessed the broader fungal community, with sequences from saprotrophic, ectomycorrhizal, ericoid and arbuscular mycorrhizal taxa. Perhaps as a result, many of the taxa from this study are poorly represented in the GenBank/EMBL/DDBJ databases, despite over a decade of sequence submissions of nuclear ribosomal DNA (nrDNA) internal transcribed spacer (ITS). Using the ITS region to identify unknown fungi from vegetative structures remains a powerful tool for diagnostic purposes, but we need to continue submitting sequences to the databases as new taxa are identified. Interestingly, Lindahl et al. did not include two samples of thelephoroid taxa in their multivariate analysis because they were outliers in terms of their dominant presence as mats; this type of patchy dominance is often observed when sampling ectomycorrhizal roots within small volumes of soil, even with taxa that do not form mats, such as species of Russula. The lesson here is that accessing the broader fungal community in soils will not overcome the sampling issues encountered when root tips alone are sampled (Taylor, 2002). However, these issues do not detract from the results of this important study. Combining molecular and ecosystem approaches in integrated studies, as carried out here, provide exciting opportunities for fertile collaborations between ecosystem scientists and mycologists.

Acknowledgements

  1. Top of page
  2. Inputs to the soil profile
  3. 15N as a marker of nitrogen cycling
  4. Identifying the players
  5. Acknowledgements
  6. References

We thank Ian Dickie, Adam Langley and Peter Kennedy for critical comments on the manuscript. This work was supported by the US National Science Foundation, awards DEB-0614384, DEB-0614266, and DEB-0235727.

References

  1. Top of page
  2. Inputs to the soil profile
  3. 15N as a marker of nitrogen cycling
  4. Identifying the players
  5. Acknowledgements
  6. References
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