Belowground Ectomycorrhizal Fungal Community Change Over a Nitrogen Deposition Gradient in Alaska

Abstract

Nitrogen availability may be a major factor structuring ectomycorrhizal fungal communities. Atmospheric nitrogen (N) deposition has been implicated in the decline of ectomycorrhizal fungal (EMF) sporocarp diversity. We previously characterized the pattern of decreased sporocarp species richness over an anthropogenic N deposition gradient in Alaska (USA). To determine whether this change in sporocarp community structure was paralleled below ground, we used molecular and morphological techniques to characterize the ectomycorrhizal community of white spruce (Picea glauca) over this gradient. We then related patterns of richness and relative abundance of taxa to various N-affected environmental parameters. Species richness of EMF declined dramatically with increasing N inputs. Over 30 taxa were identified at the low-N sites, compared with nine at the high-N sites. Low-N site dominants (Piloderma spp., Amphinema byssoides, Cortinarius spp., and various dark-mantled Tomentella spp.) disappeared completely at the high-N sites, where they were replaced by Lactarius theiogalus, Paxillus involutus, Tylospora fibrillosa, Tomentella sublilacina, Thelephora terrestris, and an unidentified species. Lactarius theiogalus accounted for 44-68% of the root tips at the high-N sites, compared with 7-20% of tips at the low-N sites. Organic horizon mineral N and foliar nutrient ratios (N:P, P:Al) were excellent predictors of taxonomic richness (r 2 Ͼ 0.93). Organic horizon NO 3 Ϫ availability was the best predictor of abundance of many taxa. These patterns suggest that long-term N deposition can lead to decline in EMF species richness, and dramatic changes in EMF community structure. The consequences of these changes for plant nutrition and ecosystem function depend on how EMF community function changes as community structure changes. We speculate that as N inputs increase, the EMF community shifts from taxa specialized for N uptake under low-N conditions (e.g., Cortinarius, Piloderma), toward taxa specialized for high overall nutrient availability (e.g., Tomentella sublilacina, Thelephora terrestris) and finally toward taxa specialized for P uptake under high-N, low-P, acidified conditions (e.g., Paxillus involutus, Lactarius theiogalus).

Nitrogen fertilization reduces diversity and alters community structure of active fungi in boreal ecosystems

“…The vast majority of information about fungal responses to N deposition focuses on mycorrhizal (especially ectomycorrhizal) fungi (Treseder, 2004). In general, studies show that ectomycorrhizal diversity declines with N deposition (Lilleskov et al, 2001(Lilleskov et al, , 2002Frey et al, 2004), and our data indicate that this pattern may be generalizable to broader groups of fungi. Although diversity studies on non-mycorrhizal taxa are rare, there is evidence that wood-decaying fungi compete poorly under high-N conditions (Fog, 1988).…”

“…Therefore, predicting N deposition and/or climate warming effects on ecosystem processes depends on understanding fungal responses to increasing N availability. There is evidence that N deposition decreases the diversity of ectomycorrhizal fungi in white spruce forests of Alaska (Lilleskov et al, 2001(Lilleskov et al, , 2002, and a recent meta-analysis indicated that N fertilization reduces mycorrhizal abundance by 15% (Treseder, 2004). However, mycorrhizal fungi are not believed to play a major role in organic carbon decomposition (Read, 1991;Dighton, 2003), and the responses of decomposer fungi to N deposition remain largely untested.…”

Effects of nitrogen deposition and fertilization on N transformations in forest soils: a review

“…For instance, in a highly acidic spruce forest soil, the amounts of dissolved organic C (DOC) and dissolved N were found to be very low (Bárta et al 2010). It is well accepted that mycorrhizal fungi exert strong controls over belowground C allocation in forest ecosystems, greatly affecting microbial turnover in the rhizosphere (Janssens et al 2010;Kuzyakov and Xu 2013;Lilleskov et al 2001Lilleskov et al , 2002Tietema 1998;Treseder 2008). Here, we further conjecture that the change in mycorrhizal fungi, resulting from Al 3 + release in the process of soil acidification, is likely to play a role in the decreased N mineralization.…”

Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe

“…Furthermore, increased nitrogen loadings can affect ecosystem phosphorus cycling, as observed in a wide variety of terrestrial ecosystems 54 , by favouring higher plant phosphorus uptake e.g. through enhanced activity of soil phosphatases 55 , root phosphatases 56 or changing symbiotic fungi 57 . Nonetheless, in the long term, these mechanisms seem quantitatively insufficient to deliver enough phosphorus to alleviate phosphorus limitation 58 .…”