Root-derived carbon and nitrogen from beech and ash trees differentially fuel soil animal food webs of deciduous forests

Zieger, Sarah L.; Ammerschubert, Silke; Polle, Andrea; Scheu, Stefan

doi:10.1371/journal.pone.0189502

Cited by 20 publications

(17 citation statements)

References 72 publications

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“…Other soil animal taxa such as Onychiuridae (Collembola) also might feed on ECM, but in addition feed on other resources such as root hairs, i.e. are not specialized in feeding on ECM [9, 40]. The fact that the density of Protura typically is low as compared to other mesofauna groups, contrasts the high biomass of ECM in temperate forest ecosystems.…”

Section: Discussionmentioning

confidence: 99%

“…For analysing the importance of root-derived C and N for A. gallicum, samples from a pulse labelling experiment conducted in 2012 were used (for details see [40]). In May 2012 beech ( Fagus sylvatica L.) and ash ( Fraxinus excelsior L.) seedlings were excavated with intact surrounding soil and litter from a beech forest near the city of Göttinger (Reyershausen, Germany).…”

Section: Methodsmentioning

confidence: 99%

“…The seedlings were transferred into a plant-growth chamber and pulse-labelled with 13 CO 2 . Further, leaves were immersed into a 15 N ammonium chloride solution for 3 days (for details see [40]). After 5 and 20 days, animals from litter and soil were extracted by heat [47].…”

Section: Methodsmentioning

confidence: 99%

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Protura are unique: first evidence of specialized feeding on ectomycorrhizal fungi in soil invertebrates

et al. 2019

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Background Ectomycorrhizal fungi (ECM) play a central role in nutrient cycling in boreal and temperate forests, but their role in the soil food web remains little understood. One of the groups assumed to live as specialised mycorrhizal feeders are Protura, but experimental and field evidence is lacking. We used a combination of three methods to test if Protura are specialized mycorrhizal feeders and compared their trophic niche with other soil invertebrates. Using pulse labelling of young beech and ash seedlings we analysed the incorporation of 13 C and 15 N into Acerentomon gallicum. In addition, individuals of Protura from temperate forests were collected for the analysis of neutral lipid fatty acids and natural variations in stable isotope ratios. Results Pulse labelling showed rapid incorporation of root-derived 13 C, but no incorporation of root-derived 15 N into A. gallicum . The transfer of 13 C from lateral roots to ectomycorrhizal root tips was high, while it was low for 15 N. Neutral lipid fatty acid (NLFA) analysis showed high amounts of bacterial marker (16:1ω7) and plant marker (16:0 and 18:1ω9) fatty acids but not of the fungal membrane lipid 18:2ω6,9 in A. gallicum . Natural variations in stable isotope ratios in Protura from a number of temperate forests were distinct from those of the great majority of other soil invertebrates, but remarkably similar to those of sporocarps of ECM fungi. Conclusions Using three in situ methods, stable isotope labelling, neutral lipid fatty acid analysis and natural variations of stable isotope ratios, we showed that Protura predominantly feed on mycorrhizal hyphae via sucking up hyphal cytoplasm. Predominant feeding on ectomycorrhizal mycelia by Protura is an exception; the limited consumption of ECM by other soil invertebrates may contribute to carbon sequestration in temperate and boreal forests. Electronic supplementary material The online version of this article (10.1186/s12898-019-0227-y) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Protura are unique: first evidence of specialized feeding on ectomycorrhizal fungi in soil invertebrates

et al. 2019

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“…It has been assumed for long that mainly bacteria benefit from labile C in the rhizosphere [31,32], but this view has been challenged by recent studies documenting that also fungi benefit from labile C input and may exploit it even faster than bacteria [33–35]. This has major implications for the whole soil community as root C is incorporated into higher trophic levels of the soil food web via the fungal and bacterial energy channel [13,36,37]. By manipulating the input of rhizosphere resources their role in structuring microbial communities and energy channels in soil food webs as well as their effects on ecosystem functioning can be investigated.…”

Section: Introductionmentioning

confidence: 99%

Deprivation of root-derived resources affects microbial biomass but not community structure in litter and soil

et al. 2019

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The input of plant leaf litter has been assumed to be the most important resource for soil organisms of forest ecosystems, but there is increasing evidence that root-derived resources may be more important. By trenching roots of trees in deciduous and coniferous forests, we cut-off the input of root-derived resources and investigated the response of microorganisms using substrate-induced respiration and phospholipid fatty acid (PLFA) analysis. After one and three years, root trenching strongly decreased microbial biomass and concentrations of PLFAs by about 20%, but the microbial community structure was little affected and the effects were similar in deciduous and coniferous forests. However, the reduction in microbial biomass varied between regions and was more pronounced in forests on limestone soils (Hainich) than in those on sandy soils (Schorfheide). Trenching also reduced microbial biomass in the litter layer but only in the Hainich after one year, whereas fungal and bacterial marker PLFAs as well as the fungal-to-plant marker ratio in litter were reduced in the Schorfheide both after one and three years. The pronounced differences between forests of the two regions suggest that root-derived resources are more important in fueling soil microorganisms of base-rich forests characterized by mull humus than in forests poor in base cations characterized by moder soils. The reduction in microbial biomass and changes in microbial community characteristics in the litter layer suggests that litter microorganisms do not exclusively rely on resources from decomposing litter but also from roots, i.e. from resources based on labile recently fixed carbon. Our results suggest that both bacteria and fungi heavily depend on root-derived resources with both suffering to a similar extent to deprivation of these resources. Further, the results indicate that the community structure of microorganisms is remarkably resistant to changes in resource supply and adapts quickly to new conditions irrespective of tree species composition and forest management.

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“…Total carbon and nitrogen contents as well as the 15 N and 13 C abundances were determined using an elemental analyzer (NA 2500CE Instruments, Milan, Italy) coupled via a Conflo II interface to an isotope ratio mass spectrometer (Delta Plus, Thermo Finnigan MAT GmbH, Bremen, Germany). Alternatively, samples were analyzed with an elemental analyzer NA 1108, Fisons-Instruments, Rodano, Milan, Italy and a mass spectrometer (Delta C, Finnigan MAT, Bremen, Germany) coupled by a ConFlo III interface (Thermo Electron Corporation, Bremen, Germany) (Zieger et al, 2017). A working standard (glutamic acid) was calibrated against the primary standards of the United States Geological Survey 40 (USGS 40; glutamic acid δ 13 CPDB = -26.39‰) and USGS 41 (glutamic acid δ 13 CPDB = 37.63‰) for δ 13 C, and USGS 40 (glutamic acid δ 15 N air = -4.5‰) and USGS 41 (glutamic acid δ 15 N air = 47.600‰) for δ 15 N. Standards were analyzed after every tenth sample to account for potential instrument drift over time as described by Dannenmann et al (2009) and Simon et al (2011).…”

Section: Methodsmentioning

confidence: 99%

ATP as Phosphorus and Nitrogen Source for Nutrient Uptake by Fagus sylvatica and Populus x canescens Roots

et al. 2019

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The present study elucidated whether roots of temperate forest trees can take up organic phosphorus in the form of ATP. Detached non-mycorrhizal roots of beech ( Fagus sylvatica ) and gray poplar ( Populus x canescens ) were exposed under controlled conditions to 33 P-ATP and/or 13 C/ 15 N labeled ATP in the presence and absence of the acid phosphatase inhibitor MoO 4 2- . Accumulation of the respective label in the roots was used to calculate 33 P, 13 C and 15 N uptake rates in ATP equivalents for comparison reason. The present data shown that a significant part of ATP was cleaved outside the roots before phosphate (P i ) was taken up. Furthermore, nucleotide uptake seems more reasonable after cleavage of at least one P i unit as ADP, AMP and/or as the nucleoside adenosine. Similar results were obtained when still attached mycorrhizal roots of adult beech trees and their natural regeneration of two forest stands were exposed to ATP in the presence or absence of MoO 4 2- . Cleavage of P i from ATP by enzymes commonly present in the rhizosphere, such as extracellular acid phosphatases, ecto-apyrase and/or nucleotidases, prior ADP/AMP/adenosine uptake is highly probable but depended on the soil type and the pH of the soil solution. Although uptake of ATP/ADP/AMP cannot be excluded, uptake of the nucleoside adenosine without breakdown into its constituents ribose and adenine is highly evident. Based on the 33 P, 13 C, and 15 N uptake rates calculated as equivalents of ATP the ‘pro and contra’ for the uptake of nucleotides and nucleosides is discussed. Short Summary Roots take up phosphorus from ATP as P i after cleavage but might also take up ADP and/or AMP by yet unknown nucleotide transporter(s) because at least the nucleoside adenosine as N source is taken up without cleavage into its constituents ribose and adenine.

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Root-derived carbon and nitrogen from beech and ash trees differentially fuel soil animal food webs of deciduous forests

Cited by 20 publications

References 72 publications

Protura are unique: first evidence of specialized feeding on ectomycorrhizal fungi in soil invertebrates

Protura are unique: first evidence of specialized feeding on ectomycorrhizal fungi in soil invertebrates

Deprivation of root-derived resources affects microbial biomass but not community structure in litter and soil

ATP as Phosphorus and Nitrogen Source for Nutrient Uptake by Fagus sylvatica and Populus x canescens Roots

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