Attributing functions to ectomycorrhizal fungal identities in assemblages for nitrogen acquisition under stress

Abstract

Mycorrhizal fungi have a key role in nitrogen (N) cycling, particularly in boreal and temperate ecosystems. However, the significance of ectomycorrhizal fungal (EMF) diversity for this important ecosystem function is unknown. Here, EMF taxon-specific N uptake was analyzed via 15 N isotope enrichment in complex root-associated assemblages and non-mycorrhizal root tips in controlled experiments. Specific 15 N enrichment in ectomycorrhizas, which represents the N influx and export, as well as the exchange of 15 N with the N pool of the root tip, was dependent on the fungal identity. Light or water deprivation revealed interspecific response diversity for N uptake. Partial taxonspecific N fluxes for ectomycorrhizas were assessed, and the benefits of EMF assemblages for plant N nutrition were estimated. We demonstrated that ectomycorrhizal assemblages provide advantages for inorganic N uptake compared with non-mycorrhizal roots under environmental constraints but not for unstressed plants. These benefits were realized via stress activation of distinct EMF taxa, which suggests significant functional diversity within EMF assemblages. We developed and validated a model that predicts net N flux into the plant based on taxon-specific 15 N enrichment in ectomycorrhizal root tips. These results open a new avenue to characterize the functional traits of EMF taxa in complex communities.

Ectomycorrhizal Communities on the Roots of Two Beech (Fagus sylvatica) Populations from Contrasting Climates Differ in Nitrogen Acquisition in a Common Environment

“…Internal 15 N reallocation from ectomycorrhizal to nonmycorrhizal root tips is unlikely because previous studies showed higher N uptake by nonmycorrhizal beech trees than by ectomycorrhizal beech trees (59) and that 15 N enrichment in the nonmycorrhizal root tips of mycorrhizal trees was similar to that of the nonmycorrhizal root tips of nonmycorrhizal trees (12). Assuming that the NO 3 Ϫ and NH 4 ϩ levels found per kilogram of dry soil in the present study were completely dissolved in the soil solution, the N concentrations were 290 to 360 M for NH 4 ϩ and 39 to 44 M for NO 3 Ϫ in the substrates of NE and SW trees.…”

“…14 N, 15 N, 12 C, and 13 C isotope analyses were conducted at the service unit Kompetenzzentrum für Stabile Isotope (KOSI; University Göttingen, Göttingen, Germany) on a Delta Plus mass spectrometer (Finnigan MAT, Bremen, Germany) with a Conflo III interface (Finnigan MAT, Bremen, Germany) and an NA2500 elemental analyzer (CE Instruments, Rodano, Milan, Italy (dry mass) of the soil, and the soil dry mass in the container was 5,520 g. ␦ 13 C values were determined as [(amount of 13 C/amount of 12 C in the sample)/(amount of 13 C/ 12 C in VPDB)] ϫ 1,000; VPDB is the Vienna Pee Dee belemnite standard, and 13 C APE ϭ atom% for the sample -atom% for natural abundance, where atom% ϭ [amount of 13 C/(amount of 12 C ϩ amount of 13 C)] ϫ 100. Quantification of microbes driving N turnover.…”

“…Because preceding field studies showed reduced N uptake of trees at the dry site (21), we anticipated reduced 15 N enrichment in the ectomycorrhizal communities of trees originating from the dry forest compared with that of communities originating from the moist forest even after 2 months of incubation under comparable conditions. We have previously shown that the level of 15 N enrichment in ectomycorrhizal root tips is proportional to the level of flux of 15 N into the plant (12,23). Therefore, we hypothesized, in addition, that reduced 15 N enrichment in ectomycorrhizal communities results in reduced 15 N enrichment in plant tissues and reduced wholeplant N uptake.…”

“…The control of N flux by EMF is complex because, on the one hand, a decreased host carbon supply results in decreased N delivery by EMF, whereas high N availability leads to enhanced C transfer to the EMF (8)(9)(10). On the other hand, EMF are instrumental to maintenance of the host N supply under drought stress and for access to organic N from leaf litter (11,12).…”

Ectomycorrhizal Fungi and Their Applications

“…However, this extensive metabolic reprogramming is repressed in incompatible interactions where more defensive compounds are produced or retained (Tschaplinski et al 2014 ). Moreover, Pena and Polle ( 2014 ) have demonstrated, using 15 N isotope enrichment, that ECM assemblages provide advantages for inorganic N uptake mainly under environmental constraints with respect to unstressed plants, thus suggesting a stress activation of specifi c ECM taxa.…”