Tree girdling provides insight on the role of labile carbon in nitrogen partitioning between soil microorganisms and adult European beech

Dannenmann, Michael; Simon, Judy; Gasché, Rainer; Holst, Jutta; Naumann, Pascale S.; Kögel‐Knabner, Ingrid; Knicker, Heike; Mayer, Helmut; Schloter, Michael; Pena, Rodica; Polle, Andrea; Rennenberg, Heinz; Papen, H.

doi:10.1016/j.soilbio.2009.04.024

Cited by 179 publications

(186 citation statements)

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“…Soil nitrogen was relatively stable (total N, 7.7 Ϯ 0.7 and 8.6 Ϯ 0.6 mg g Ϫ1 soil [dry weight] on girdled and control plots, respectively; dissolved organic N, 29 Ϯ 6 and 32 Ϯ 6 g g Ϫ1 soil [dry weight] on girdled and control plots, respectively), whereas dissolved organic carbon was lower in soil from the girdled plots than in that from nongirdled plots (16). HЈ was positively correlated with DOC/DON (Fig.…”

Section: Resultsmentioning

confidence: 99%

Girdling Affects Ectomycorrhizal Fungal (EMF) Diversity and Reveals Functional Differences in EMF Community Composition in a Beech Forest

Pena

Offermann

Simon

et al. 2010

Appl Environ Microbiol

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The relationships between plant carbon resources, soil carbon and nitrogen content, and ectomycorrhizal fungal (EMF) diversity in a monospecific, old-growth beech (Fagus sylvatica) forest were investigated by manipulating carbon flux by girdling. We hypothesized that disruption of the carbon supply would not affect diversity and EMF species numbers if EM fungi can be supplied by plant internal carbohydrate resources or would result in selective disappearance of EMF taxa because of differences in carbon demand of different fungi. Tree carbohydrate status, root demography, EMF colonization, and EMF taxon abundance were measured repeatedly during 1 year after girdling. Girdling did not affect root colonization but decreased EMF species richness of an estimated 79 to 90 taxa to about 40 taxa. Cenococcum geophilum, Lactarius blennius, and Tomentella lapida were dominant, colonizing about 70% of the root tips, and remained unaffected by girdling. Mainly cryptic EMF species disappeared. Therefore, the Shannon-Wiener index (H) decreased but evenness was unaffected. H was positively correlated with glucose, fructose, and starch concentrations of fine roots and also with the ratio of dissolved organic carbon to dissolved organic nitrogen (DOC/DON), suggesting that both H and DOC/DON were governed by changes in belowground carbon allocation. Our results suggest that beech maintains numerous rare EMF species by recent photosynthate. These EM fungi may constitute biological insurance for adaptation to changing environmental conditions. The preservation of taxa previously not known to colonize beech may, thus, form an important reservoir for future forest development.In temperate and boreal forest ecosystems, most tree species form ectomycorrhizal fungal (EMF) associations. EM fungi ensheathe the root tip, forming characteristic mantlelike structures (1). The presence and lengths of hyphae emanating from the mantle are characteristic of different EMF species and establish different soil exploration types (2). It has been assumed that EMF communities are adapted specifically to mobilize sparse soil nutrient resources in boreal and temperate forests (11, 50). Current estimates indicate that about 80% of all nitrogen and phosphorus present in plants has been taken up via mycorrhizas (30,41,63).Unlike free-living soil microbes, EM fungi have direct access to reduced carbon from their host plants. More than 50 years ago, Melin and Nilsson (46) showed that 14 C applied to leaves was recovered within one day in EM fungi, suggesting a strong dependence of fungal metabolism on host photosynthesis. Subsequent isotopic studies corroborated tight connections between current photosynthate and EM fungi (28,42). EMF hyphae constitute the main path of plant-derived carbon into the soil (24, 29). Furthermore, EMF hyphae contribute substantially to soil respiration (25% from hyphae and 15% from roots) (27). As hyphal respiration decreases strongly in response to girdling of trees, a tight metabolic link between extramatrical mycelia and host ...

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Section: Resultsmentioning

confidence: 99%

Girdling Affects Ectomycorrhizal Fungal (EMF) Diversity and Reveals Functional Differences in EMF Community Composition in a Beech Forest

Pena

Offermann

Simon

et al. 2010

Appl Environ Microbiol

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122

105

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“…In our experiment, we used an NH 4 þ concentration similar to that found in the Tuttlingen forest (Dannenmann et al, 2009), where the soil for beech mycorrhizal inoculation was sampled. The beech trees in the Tuttlingen forest are colonized by a characteristic EMF flora, including all species present in this study (Buée et al, 2005;Pena et al, 2010;.…”

Section: Discussionmentioning

confidence: 99%

“…A total of 120 mycorrhizal and 120 non-mycorrhizal beech seedlings were transplanted without adherent soil individually into 660 ml pots with a sand-peat mixture and supplied daily with 56 ml of nutrient solution containing 0.4 mM NH 4 þ as the sole N source. This concentration was chosen because it was similar to that in forest soil of the Tuttlingen site (Dannenmann et al, 2009) Jongbloed et al, 1991;Eltrop and Marschner, 1996) and because preceding analysis with attached beech roots at the Tuttlingen site showed saturation of NH 4 þ uptake at concentrations above 0.05 mM (Gessler et al, 2005). The seedlings were grown either in full light (200 mmol PAR m À 2 s À 1 ) or in the shade (35-40 mmol PAR m À 2 s À 1 at plant height).…”

Section: Plant Cultivation and Experimental Treatmentsmentioning

confidence: 99%

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

Pena

Polle

2013

The ISME Journal

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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.

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“…Hö gberg et al (2007) observed a tendency towards higher inorganic N levels in girdled plots of a boreal forest, whereas Ekberg et al (2007) detected a decrease in total organic C in girdled plots of temperate spruce stand. It is thus likely that girdling-related changes in soil chemistry, in particular labile C and N pools have considerable effects on the soil microbial community structure (Dannenmann et al, 2009;Weintraub et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Seasonality and resource availability control bacterial and archaeal communities in soils of a temperate beech forest

et al. 2010

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It was hypothesized that seasonality and resource availability altered through tree girdling were major determinants of the phylogenetic composition of the archaeal and bacterial community in a temperate beech forest soil. During a 2-year field experiment, involving girdling of beech trees to intercept the transfer of easily available carbon (C) from the canopy to roots, members of the dominant phylogenetic microbial phyla residing in top soils under girdled versus untreated control trees were monitored at bimonthly intervals through 16S rRNA gene-based terminal restriction fragment length polymorphism profiling and quantitative PCR analysis. Effects on nitrifying and denitrifying groups were assessed by measuring the abundances of nirS and nosZ genes as well as bacterial and archaeal amoA genes. Seasonal dynamics displayed by key phylogenetic and nitrogen (N) cycling functional groups were found to be tightly coupled with seasonal alterations in labile C and N pools as well as with variation in soil temperature and soil moisture. In particular, archaea and acidobacteria were highly responsive to soil nutritional and soil climatic changes associated with seasonality, indicating their high metabolic versatility and capability to adapt to environmental changes. For these phyla, significant interrelations with soil chemical and microbial process data were found suggesting their potential, but poorly described contribution to nitrification or denitrification in temperate forest soils. In conclusion, our extensive approach allowed us to get novel insights into effects of seasonality and resource availability on the microbial community, in particular on hitherto poorly studied bacterial phyla and functional groups.

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Tree girdling provides insight on the role of labile carbon in nitrogen partitioning between soil microorganisms and adult European beech

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Cited by 179 publications

References 57 publications

Girdling Affects Ectomycorrhizal Fungal (EMF) Diversity and Reveals Functional Differences in EMF Community Composition in a Beech Forest

Girdling Affects Ectomycorrhizal Fungal (EMF) Diversity and Reveals Functional Differences in EMF Community Composition in a Beech Forest

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

Seasonality and resource availability control bacterial and archaeal communities in soils of a temperate beech forest

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