Cascading effects from plants to soil microorganisms explain how plant species richness and simulated climate change affect soil multifunctionality

Valencia, Enrique; Gross, Nicolas; Quero, José L.; Carmona, Carlos P.; Ochoa, Victoria; Gozalo, Beatriz; Delgado‐Baquerizo, Manuel; Dumack, Kenneth; Hamonts, Kelly; Singh, Brajesh K.; Bonkowski, Michael; Maestre, Fernando T.

doi:10.1111/gcb.14440

Cited by 125 publications

(90 citation statements)

References 64 publications

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“…In turn, climatic variables and ecosystem functions are not linked by a single indirect pathway but by multiple indirect pathways with saprophytic fungi as a corner stone. This result is in line with several other studies(Mori et al, 2016;Setälä et al, 2005;Valencia et al, 2018).…”

supporting

confidence: 94%

“…The resulting simpler compounds, scarce in alpine environments, become available for plant and microbial absorption (Moore et al, ; Wall et al, ). Changes in saprophytic fungi communities should thus alter nutrient availability, which impacts productivity, N‐cycling and multifunctionality (Mori et al, ; Valencia et al, ). Nevertheless, also the other trophic groups β‐diversities indirectly drove ecosystem functions turnover through their strong links to the saprophytic fungi β‐diversity.…”

Section: Discussionmentioning

confidence: 99%

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Multi‐trophic β‐diversity mediates the effect of environmental gradients on the turnover of multiple ecosystem functions

et al. 2019

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Much effort has been devoted to better understanding the effects of environment and biodiversity on ecosystem functioning. However, few studies have moved beyond measuring biodiversity as species richness of a single group and/or focusing on a single ecosystem function. While there is a growing recognition that along environmental gradients, the compositional turnover of multiple trophic groups influences not only productivity but multiple ecosystem functions, we do not know yet which components of multi‐trophic β‐diversity influence which ecosystem functions. Here, we captured the biodiversity found in soils using environmental DNA to study total soil multi‐trophic β‐diversity (between all taxa regardless of their trophic group association), horizontal β‐diversities (β‐diversities within trophic groups) and vertical β‐diversity (β‐diversity across trophic groups) along a 1,000 m elevational gradient in the French Alps. Using path analyses, we quantified how these β‐diversity components mediate the effects of environmental turnover on the turnover of multiple ecosystem functions (i.e. productivity, N‐cycling, N‐leaching) and overall multifunctionality. While we found a strong direct effect of soil properties on the turnover of multiple ecosystem functions, we also found an indirect effect of climate and soil properties through multi‐trophic β‐diversity. More specifically, only total multi‐trophic β‐diversity and the horizontal β‐diversity of saprophytic fungi were strongly related to the turnover of multifunctionality and, to a lower extent, the turnover of productivity and N‐cycling. Our results suggest that decomposition processes and resulting nutrient availability are key to understand how ecosystem functions change along soil properties and climatic gradients in alpine ecosystems. By demonstrating how saprophytic fungi and their associated trophic groups can offset the direct responses of multiple ecosystem functions to environmental change, our study highlights the paramount importance of multi‐trophic diversity for better understanding ecosystem multifunctionality in a changing world. A free Plain Language Summary can be found within the Supporting Information of this article.

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confidence: 94%

Section: Discussionmentioning

confidence: 99%

Multi‐trophic β‐diversity mediates the effect of environmental gradients on the turnover of multiple ecosystem functions

et al. 2019

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“…Gradients in moisture availability occur in both wet and dry climates, raising the possibility of interactions. A legacy of studies finding that foliar nitrogen (N) and phosphorus (P) can be correlated with soils (Chadwick et al, 1999; Hedin et al, 2003; Moreno‐Martínez et al, 2018; Valencia et al, 2018; Vitousek et al, 1999; Walker & Syers, 1976) and climate (Bjorkman et al, 2018; Bruelheide et al, 2018; Chen et al, 2013; McGroddy et al, 2004; Reich & Oleksyn, 2004; Tjoelker et al, 1999; Wieczynski et al, 2019) suggests an important role for drought‐habitat interactions. In dry climates, heterogeneity of soil moisture could provide refuge for drought‐intolerant species.…”

Section: Introductionmentioning

confidence: 99%

Where Resource‐Acquisitive Species Are Located: The Role of Habitat Heterogeneity

Seyednasrollah

Clark

2020

Geophysical Research Letters

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Rising temperatures with increased drought pose two challenges for management of future biodiversity. First, are the most vulnerable species concentrated in specific regions and habitats? Second, where can landscape heterogeneity potentially mitigate impacts? We conducted a comprehensive trait analysis of forest plots spanning the eastern United States to quantify how resource-acquisitive species respond to moisture-soil-climate interactions. We found that resource-acquisitive species, including nutrient-acquisitive and moisture-acquisitive species, respond disproportionately to environmental gradients, and their response is largely explained by soil variation. We showed that the strong boundary of resource-acquisitive species occurs near the last glacial limit, highlighting one of the clearest indicators of soil controls. Although local soil moisture may reduce drought-induced stress for moisture-acquisitive species, nutrient-acquisitive species remain vulnerable on wet soils in dry climates. The results suggest that theories explaining species distributions should devote close attention to the combination of local drainage and soil type.Plain Summary language Global warming and drought may cause harm to the biodiversity on the planet. But we may be able to protect species if we can identify vulnerable habitats and regions. To address this challenge, we analyzed a large data set of forest plots across the eastern United States. Our study showed that soil type and local soil moisture play important roles in species response to dry and warm conditions. Our results revealed a sharp change in the population of resource-acquisitive species near the boundary of the last glaciation, indicating a strong soil control. While nutrient-acquisitive species did not benefit from local moisture availability, moisture-acquisitive species favored these conditions.

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“…Beyond medicine, context-dependent, directed microbiome interventions could be applied to agriculture and the environment. External perturbations could modulate the soil microbiome to allow plants to grow in new conditions, such as those provoked by biotic or abiotic stresses such as climate change [6], salt-stress [7], fungal infection [8], and soil over-exploitation [9]. Industrial applications of microbiome engineering will increase the performance of addedvalue chemicals production, such as food (yogurt, beverages), probiotics, enzymes or biofuels [10,11], by modulation of the strain ratio (community enrichment or reduction) or identification of the optimal medium composition [12].…”

Section: Introductionmentioning

confidence: 99%

Dynamic simulations of microbial communities under perturbations: opportunities for microbiome engineering

García-Jiménez

Carrasco

Medina

et al. 2020

Preprint

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Background : There are few large longitudinal microbiome studies, and fewer that include controlled, well-annotated perturbations between sampling-points. Thus, there are few opportunities to employ data-driven computational analyses of perturbed microbial communities over time. Results : Our novel computational system simulates the dynamics of microbial communities under perturbations using genome-scale metabolic models (GEMs). Perturbations include modifications to a) the nutrients available in the medium, allowing modelling of prebiotics; and/or b) the microorganisms present in the community to model, for example, probiotics or pathogen infection. These simulations generate the quantity and types of information required by MDPbiome, an AI system which builds predictive models suggesting the perturbation(s) required to engineer microbial communities to a desired state. We call this novel combination of technologies "MDPbiomeGEM"'. We demonstrate, in a Crohn’s disease microbiome, that MDPbiomeGEM correctly models the influence of both prebiotic fiber and a probiotic, resulting in a recommendation to consume inulin to recover from dysbiosis, consistent with prior biomedical knowledge. When used to model the soil microbiome's ability to degrade the herbicide Atrazine, differing recommendations arise depending on the highly variable state of the initial soil microbial composition, highlighting the relevance of both phosphate and microbes (i.e. Halobacillus sp. and H.stevensii ) in a directed microbiome engineering strategy, consistent with previously published observations. Conclusions : MDPbiomeGEM generates large volumes of longitudinal data of complex microbial communities experiencing perturbations. Machine learning on these data reveal patterns consistent with existing biological knowledge, supporting the validity of the approach. MDPbiomeGEM could save research resources by optimizing sample collection in metagenomics studies through identification of "informative" scenarios/time-points, or by predicting optimal in-vitro culture formulations for generating performant synthetic microbial communities. Finally, MDPbiomeGEM outputs include detailed information about the metabolic state of the community, which can be used to further interpret the impact of perturbations, and potentially could be used to predict novel metabolic biomarkers of a microbiome's state.

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Cascading effects from plants to soil microorganisms explain how plant species richness and simulated climate change affect soil multifunctionality

Cited by 125 publications

References 64 publications

Multi‐trophic β‐diversity mediates the effect of environmental gradients on the turnover of multiple ecosystem functions

Multi‐trophic β‐diversity mediates the effect of environmental gradients on the turnover of multiple ecosystem functions

Where Resource‐Acquisitive Species Are Located: The Role of Habitat Heterogeneity

Dynamic simulations of microbial communities under perturbations: opportunities for microbiome engineering

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