Multitrophic interactions in the rhizosphere of a temperate forest tree affect plant carbon flow into the belowground food web

Maboreke, Hazel; Graf, Marcel; Grams, Thorsten E. E.; Herrmann, Sylvie; Scheu, Stefan; Rueß, Liliane

doi:10.1016/j.soilbio.2017.09.002

Cited by 30 publications

(19 citation statements)

References 69 publications

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“…Moreover, a negative effect of fungal grazers, as detected in the singular treatments, likely was balanced by better resource availability via plant feeder induced "leakage" into the rhizosphere environment. This is consistent with findings by Maboreke et al [26], who reported comparable synergistic interactions between fungal-feeding Collembola and plant-feeding nematodes.…”

Section: Multitrophic Interactionssupporting

confidence: 93%

“…Compared to the sole functional group treatments and the control, the biomass of bacteria and fungi increased. Fungal grazing by nematodes likely has released nutrients immobilized in fungal biomass as resources for bacteria, which corresponds to findings of Maboreke et al [26], who reported that grazing by Collembola promoted bacterial growth. Additionally, the presence of bacterial feeders likely regulated the bacterial biomass [67], thereby reducing competition for root carbon, and in turn indirectly facilitating fungal growth.…”

Section: Multitrophic Interactionssupporting

confidence: 86%

“…Such nematode induced "leakage" in the rhizosphere is well known for annual and crop plants, e.g., clover, barley or maize [16,17,53]. For perennial woody plants, P. penetrans was reported to stimulate microbial growth in the rhizosphere of oak [25], predominantly due to a promotion of plant carbon flow belowground [26]. On the other hand, transcriptome analyses revealed P. penetrans to act as a strong root carbon sink leading to resource competition with the oak's ectomycorrhizal symbiont P. croceum [54].…”

Section: Plant Feedersmentioning

confidence: 98%

“…On the other side, feeding activity of fungal grazers and plant feeders can negatively affect mycorrhiza fungi, and hence hamper nutrient acquisition by trees [20,21].Insight into these relationships of trees and rhizosphere organisms is necessary for sustainable forest management [22,23]. In temperate forests, Pedunculate Oak (Quercus robur L.) is an economically important species [24], which was recently used as model to investigate rhizosphere interactions by employing nematodes as plant feeders and Collembola as fungal grazers [25,26]. However, due to the complexness of rhizosphere processes, and the technical challenges to manipulate this habitat, existing knowledge is still largely fragmentary.…”

mentioning

confidence: 99%

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Micro-Food Web Structure Shapes Rhizosphere Microbial Communities and Growth in Oak

et al. 2018

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The multitrophic interactions in the rhizosphere impose significant impacts on microbial community structure and function, affecting nutrient mineralisation and consequently plant performance. However, particularly for long-lived plants such as forest trees, the mechanisms by which trophic structure of the micro-food web governs rhizosphere microorganisms are still poorly understood. This study addresses the role of nematodes, as a major component of the soil micro-food web, in influencing the microbial abundance and community structure as well as tree growth. In a greenhouse experiment with Pedunculate Oak seedlings were grown in soil, where the nematode trophic structure was manipulated by altering the proportion of functional groups (i.e., bacterial, fungal, and plant feeders) in a full factorial design. The influence on the rhizosphere microbial community, the ectomycorrhizal symbiont Piloderma croceum, and oak growth, was assessed. Soil phospholipid fatty acids were employed to determine changes in the microbial communities. Increased density of singular nematode functional groups showed minor impact by increasing the biomass of single microbial groups (e.g., plant feeders that of Gram-negative bacteria), except fungal feeders, which resulted in a decline of all microorganisms in the soil. In contrast, inoculation of two or three nematode groups promoted microbial biomass and altered the community structure in favour of bacteria, thereby counteracting negative impact of single groups. These findings highlight that the collective action of trophic groups in the soil micro-food web can result in microbial community changes promoting the fitness of the tree, thereby alleviating the negative effects of individual functional groups.Diversity 2018, 10, 15 2 of 16 diversity nematodes hold a central position in the micro-food web [10,11] and participate in both bottom-up and top-down controlled webs [12]. Their multitrophic interactions in the soil micro-food web can impose various impacts on plant fitness. In resource regulated food webs nematode grazing maintains bacterial and fungal populations in a youthful state, regulates microbial composition, and enhances decomposition activity [13,14]. Moreover, the "leakage" of root cell content induced by plant feeders can increase carbon translocation into the rhizosphere, thereby indirectly stimulating microbial biomass [15][16][17]. Furthermore, nematodes recycle nutrients by excretion (e.g., ammonium) otherwise locked up in microbial biomass, making them accessible for plant up-take [18,19]. On the other side, feeding activity of fungal grazers and plant feeders can negatively affect mycorrhiza fungi, and hence hamper nutrient acquisition by trees [20,21].Insight into these relationships of trees and rhizosphere organisms is necessary for sustainable forest management [22,23]. In temperate forests, Pedunculate Oak (Quercus robur L.) is an economically important species [24], which was recently used as model to investigate rhizosphere interactions by employing nematode...

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Section: Multitrophic Interactionssupporting

confidence: 93%

Section: Multitrophic Interactionssupporting

confidence: 86%

Section: Plant Feedersmentioning

confidence: 98%

mentioning

confidence: 99%

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Micro-Food Web Structure Shapes Rhizosphere Microbial Communities and Growth in Oak

et al. 2018

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“…, , Maboreke et al. ). Such phytometers (called PhytOakmeter) can help to deepen our understanding of mechanisms up to molecular level contributing to patterns on ecosystem level we find.…”

Section: Investigating Links Between Biodiversity and Ecosystem Functmentioning

confidence: 99%

Mycorrhiza in tree diversity–ecosystem function relationships: conceptual framework and experimental implementation

et al. 2018

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The widely observed positive relationship between plant diversity and ecosystem functioning is thought to be substantially driven by complementary resource use of plant species. Recent work suggests that biotic interactions among plants and between plants and soil organisms drive key aspects of resource use complementarity. Here, we provide a conceptual framework for integrating positive biotic interactions across guilds of organisms, more specifically between plants and mycorrhizal types, to explain resource use complementarity in plants and its consequences for plant competition. Our overarching hypothesis is that ecosystem functioning increases when more plant species associate with functionally dissimilar mycorrhizal fungi because differing mycorrhizal types will increase coverage of habitat space for and reduce competition among plants. We introduce a recently established field experiment (MyDiv) that uses different pools of tree species that associate with either arbuscular or ectomycorrhizal fungi to create orthogonal experimental gradients in tree species richness and mycorrhizal associations and present initial results. Finally, we discuss options for future mechanistic studies on resource use complementarity within MyDiv. We show how mycorrhizal types and biotic interactions in MyDiv can be used in the future to test novel questions regarding the mechanisms underlying biodiversity–ecosystem function relationships.

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Direct and indirect trophic interactions of soil nematodes impact chickpea and oat nutrition

et al. 2020

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Aims Root lesion nematodes (RLN) have negative impacts on legume-grass systems. These impacts might be moderated by bacterial feeding nematodes (BFN) presence. It remains unknown how these trophic groups of nematodes interactively impact plant productivity and dynamics of carbon (C) and nitrogen (N) in grasslegume mixtures. We addressed this research gap using inter-kingdom interactions in a model system. Methods Chickpea and oat were grown in mono-and mixed cultures, and RLN and BFN were applied alone and in combination. Plant biomass, shoot C and N content and isotopic composition, and mineral N in soil were measured. Results RLN presence reduced root biomass across treatments. This reduction was stronger in the grass than the legume and was not modified by BFN. Nematodes increased plant shoot N concentrations. RLN and BFN had interactive effects on shoot nutrient concentration resulting in reduced shoot C concentration when both trophic groups were combined. Shoot δ 15 N data revealed transfer of symbiotically fixed N from chickpea to oat in the presence of RLN. However, this N transfer did not result in improved oat growth. Conclusions Interactive effects of soil organisms can cascade aboveground, influencing C and N dynamics and ecosystem productivity.

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Multitrophic interactions in the rhizosphere of a temperate forest tree affect plant carbon flow into the belowground food web

Cited by 30 publications

References 69 publications

Micro-Food Web Structure Shapes Rhizosphere Microbial Communities and Growth in Oak

Micro-Food Web Structure Shapes Rhizosphere Microbial Communities and Growth in Oak

Mycorrhiza in tree diversity–ecosystem function relationships: conceptual framework and experimental implementation

Direct and indirect trophic interactions of soil nematodes impact chickpea and oat nutrition

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