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Drought is a major stressor to soil microbial communities, and the intensification of climate change is predicted to increase hydric stress worldwide in the coming decades. As a possible mitigating factor for the consequences of prolonged drought periods, above and belowground biodiversity can increase ecosystem resistance and resilience by improving metabolic redundancy and complementarity as biodiversity increases. Here, we investigated the interaction effect between plant richness and successive, simulated summer drought on soil microbial communities during a period of 9 years.To do that, we made use of a well-established biodiversity experiment (The Jena Experiment) to investigate the response of microbial richness and community composition to successive drought periods alongside a plant richness gradient, which covers 1-, 2-, 4-, 8-, 16-, and 60-species plant communities. Plots were covered from natural precipitation by installing rain shelters 6 weeks every summer. Bulk soil samples were collected 1 year after the last summer drought was simulated. Our data indicate that bacterial richness increased after successive exposure to drought, with the increase being stable along the plant richness gradient. We identified a significant effect of plant species richness on the soil microbial community composition and determined the taxa significantly impacted by drought at each plant richness level. Our data successfully demonstrates that summer drought might have a legacy effect on soil bacterial communities.
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Bactérias , Biodiversidade , Secas , Plantas , Estações do Ano , Microbiologia do Solo , Bactérias/classificação , Bactérias/genética , Bactérias/crescimento & desenvolvimento , Plantas/microbiologia , Microbiota , Mudança Climática , Ecossistema , Solo/químicaRESUMO
Soil organic carbon (SOC) plays an essential role in mediating community structure and metabolic activities of belowground biota. Unraveling the evolution of belowground communities and their feedback mechanisms on SOC dynamics helps embed the ecology of soil microbiome into carbon cycling, which serves to improve biodiversity conservation and carbon management strategy under global change. Here, croplands with a SOC gradient were used to understand how belowground metabolisms and SOC decomposition were linked to the diversity, composition, and co-occurrence networks of belowground communities encompassing archaea, bacteria, fungi, protists, and invertebrates. As SOC decreased, the diversity of prokaryotes and eukaryotes also decreased, but their network complexity showed contrasting patterns: prokaryotes increased due to intensified niche overlap, while that of eukaryotes decreased possibly because of greater dispersal limitation owing to the breakdown of macroaggregates. Despite the decrease in biodiversity and SOC stocks, the belowground metabolic capacity was enhanced as indicated by increased enzyme activity and decreased enzymatic stoichiometric imbalance. This could, in turn, expedite carbon loss through respiration, particularly in the slow-cycling pool. The enhanced belowground metabolic capacity was dominantly driven by greater multitrophic network complexity and particularly negative (competitive and predator-prey) associations, which fostered the stability of the belowground metacommunity. Interestingly, soil abiotic conditions including pH, aeration, and nutrient stocks, exhibited a less significant role. Overall, this study reveals a greater need for soil C resources across multitrophic levels to maintain metabolic functionality as declining SOC results in biodiversity loss. Our researchers highlight the importance of integrating belowground biological processes into models of SOC turnover, to improve agroecosystem functioning and carbon management in face of intensifying anthropogenic land-use and climate change.
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Carbono , Solo , Solo/química , Biodiversidade , Bactérias , ArchaeaRESUMO
Numerous studies have demonstrated that biodiversity drives ecosystem functioning, yet how biodiversity loss alters ecosystems functioning and stability in the long-term lacks experimental evidence. We report temporal effects of species richness on community productivity, stability, species asynchrony, and complementarity, and how the relationships among them change over 17 years in a grassland biodiversity experiment. Productivity declined more rapidly in less diverse communities resulting in temporally strengthening positive effects of richness on productivity, complementarity, and stability. In later years asynchrony played a more important role in increasing community stability as the negative effect of richness on population stability diminished. Only during later years did species complementarity relate to species asynchrony. These results show that species complementarity and asynchrony can take more than a decade to develop strong stabilizing effects on ecosystem functioning in diverse plant communities. Thus, the mechanisms stabilizing ecosystem functioning change with community age.
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Ecossistema , Pradaria , Biodiversidade , Plantas , BiomassaRESUMO
Growing threats from extreme climatic events and biodiversity loss have raised concerns about their interactive consequences for ecosystem functioning. Evidence suggests biodiversity can buffer ecosystem functioning during such climatic events. However, whether exposure to extreme climatic events will strengthen the biodiversity-dependent buffering effects for future generations remains elusive. We assess such transgenerational effects by exposing experimental grassland communities to eight recurrent summer droughts versus ambient conditions in the field. Seed offspring of 12 species are then subjected to a subsequent drought event in the glasshouse, grown individually, in monocultures or in 2-species mixtures. Comparing productivity between mixtures and monocultures, drought-selected plants show greater between-species complementarity than ambient-selected plants when recovering from the subsequent drought, causing stronger biodiversity effects on productivity and better recovery of drought-selected mixtures after the drought. These findings suggest exposure to recurrent climatic events can improve ecosystem responses to future events through transgenerational reinforcement of species complementarity.
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Secas , Ecossistema , Biodiversidade , Pradaria , Plantas , Estações do AnoRESUMO
Soil fungi are fundamental to plant productivity, yet their influence on the temporal stability of global terrestrial ecosystems, and their capacity to buffer plant productivity against extreme drought events, remain uncertain. Here we combined three independent global field surveys of soil fungi with a satellite-derived temporal assessment of plant productivity, and report that phylotype richness within particular fungal functional groups drives the stability of terrestrial ecosystems. The richness of fungal decomposers was consistently and positively associated with ecosystem stability worldwide, while the opposite pattern was found for the richness of fungal plant pathogens, particularly in grasslands. We further demonstrated that the richness of soil decomposers was consistently positively linked with higher resistance of plant productivity in response to extreme drought events, while that of fungal plant pathogens showed a general negative relationship with plant productivity resilience/resistance patterns. Together, our work provides evidence supporting the critical role of soil fungal diversity to secure stable plant production over time in global ecosystems, and to buffer against extreme climate events.
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Ecossistema , Solo , Secas , Plantas , Microbiologia do SoloRESUMO
Experiments showed that biodiversity increases grassland productivity and nutrient exploitation, potentially reducing fertiliser needs. Enhancing biodiversity could improve P-use efficiency of grasslands, which is beneficial given that rock-derived P fertilisers are expected to become scarce in the future. Here, we show in a biodiversity experiment that more diverse plant communities were able to exploit P resources more completely than less diverse ones. In the agricultural grasslands that we studied, management effects either overruled or modified the driving role of plant diversity observed in the biodiversity experiment. Nevertheless, we show that greater above- (plants) and belowground (mycorrhizal fungi) biodiversity contributed to tightening the P cycle in agricultural grasslands, as reduced management intensity and the associated increased biodiversity fostered the exploitation of P resources. Our results demonstrate that promoting a high above- and belowground biodiversity has ecological (biodiversity protection) and economical (fertiliser savings) benefits. Such win-win situations for farmers and biodiversity are crucial to convince farmers of the benefits of biodiversity and thus counteract global biodiversity loss.
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Agricultura/métodos , Biodiversidade , Pradaria , Fósforo/metabolismo , Agricultura/economia , Biomassa , Fertilizantes/economia , Análise de Classes Latentes , Micorrizas/classificação , Micorrizas/metabolismo , Fósforo/análise , Fósforo/economia , Plantas/classificação , Plantas/metabolismo , Plantas/microbiologia , Solo/química , Microbiologia do SoloRESUMO
Theoretical and empirical advances have revealed the importance of biodiversity for stabilizing ecosystem functions through time. Despite the global degradation of soils, whether the loss of soil microbial diversity can destabilize ecosystem functioning is poorly understood. Here, we experimentally quantified the contribution of soil fungal and bacterial communities to the temporal stability of four key ecosystem functions related to biogeochemical cycling. Microbial diversity enhanced the temporal stability of all ecosystem functions and this pattern was particularly strong in plant-soil mesocosms with reduced microbial richness where over 50% of microbial taxa were lost. The stabilizing effect of soil biodiversity was linked to asynchrony among microbial taxa whereby different soil fungi and bacteria promoted different ecosystem functions at different times. Our results emphasize the need to conserve soil biodiversity for the provisioning of multiple ecosystem functions that soils provide to the society.
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Fenômenos Fisiológicos Bacterianos , Ecossistema , Fungos/fisiologia , Microbiota , Microbiologia do Solo , Alemanha , SuíçaRESUMO
In natural ecosystems, positive effects of plant diversity on ecosystem functioning have been widely observed, yet whether this is true in cropping systems remains unclear. Here we assessed the impact of crop diversification on soil microbial diversity, soil multifunctionality (SMF) and crop yields in 155 cereal fields across a 3,000 km north-south European gradient. Overall, crop diversity showed a relatively minor effect on soil microbial diversity, SMF and yields. In contrast, the proportion of time with crop cover (including cash crops, cover crops or forage leys) during the past ten-year crop rotation had a much stronger impact. This suggests that increasing crop cover can enhance both yields and soil functioning, while also providing habitat for soil microorganisms. We found that SMF did not positively contribute to crop yields, highlighting that care must be taken to balance the provision of food with environmentally beneficial functions and services, since they do not always go hand in hand.
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Understanding factors that maintain ecosystem stability is critical in the face of environmental change. Experiments simulating species loss from grassland have shown that losing biodiversity decreases ecosystem stability. However, as the originally sown experimental communities with reduced biodiversity develop, plant evolutionary processes or the assembly of interacting soil organisms may allow ecosystems to increase stability over time. We explored such effects in a long-term grassland biodiversity experiment with plant communities with either a history of co-occurrence (selected communities) or no such history (naïve communities) over a 4-yr period in which a major flood disturbance occurred. Comparing communities of identical species composition, we found that selected communities had temporally more stable biomass than naïve communities, especially at low species richness. Furthermore, selected communities showed greater biomass recovery after flooding, resulting in more stable post-flood productivity. In contrast to a previous study, the positive diversity-stability relationship was maintained after the flooding. Our results were consistent across three soil treatments simulating the presence or absence of co-selected microbial communities. We suggest that prolonged exposure of plant populations to a particular community context and abiotic site conditions can increase ecosystem temporal stability and resilience due to short-term evolution. A history of co-occurrence can in part compensate for species loss, as can high plant diversity in part compensate for the missing opportunity of such adaptive adjustments.
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Ecossistema , Pradaria , Biodiversidade , Biomassa , PlantasRESUMO
A large body of research shows that biodiversity loss can reduce ecosystem functioning. However, much of the evidence for this relationship is drawn from biodiversity-ecosystem functioning experiments in which biodiversity loss is simulated by randomly assembling communities of varying species diversity, and ecosystem functions are measured. This random assembly has led some ecologists to question the relevance of biodiversity experiments to real-world ecosystems, where community assembly or disassembly may be non-random and influenced by external drivers, such as climate, soil conditions or land use. Here, we compare data from real-world grassland plant communities with data from two of the largest and longest-running grassland biodiversity experiments (the Jena Experiment in Germany and BioDIV in the United States) in terms of their taxonomic, functional and phylogenetic diversity and functional-trait composition. We found that plant communities of biodiversity experiments cover almost all of the multivariate variation of the real-world communities, while also containing community types that are not currently observed in the real world. Moreover, they have greater variance in their compositional features than their real-world counterparts. We then re-analysed a subset of experimental data that included only ecologically realistic communities (that is, those comparable to real-world communities). For 10 out of 12 biodiversity-ecosystem functioning relationships, biodiversity effects did not differ significantly between the full dataset of biodiversity experiments and the ecologically realistic subset of experimental communities. Although we do not provide direct evidence for strong or consistent biodiversity-ecosystem functioning relationships in real-world communities, our results demonstrate that the results of biodiversity experiments are largely insensitive to the exclusion of unrealistic communities and that the conclusions drawn from biodiversity experiments are generally robust.
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Biodiversidade , Ecossistema , Alemanha , Filogenia , PlantasRESUMO
Arbuscular mycorrhizal fungi (AMF) play an important role in maintaining plant diversity and productivity in grassland ecosystems. However, very few studies have investigated how AMF and plant communities co-vary between contrasting environments in natural ecosystems. Intensive sampling (50 soil samples) was conducted in natural open grasslands at both 3570 and 4556 m on Mount Segrila on the Southeast Tibetan Plateau. We used 454-pyrosequencing to investigate soil AMF communities and to explore relationships between AMF diversity and plant richness, productivity and community composition. AMF diversity was negatively correlated with plant richness at 3570 m but positively at 4556 m. Differences in AMF community composition between elevations were attributable to plant community composition, soil pH and available phosphorus concentration. The AMF community was more phylogenetically clustered at the higher elevation than the lower elevation. However, greater phylogenetic clustering (under dispersion) of AMF communities at the two elevations was positively correlated with above-ground biomass. Our results indicate that plant community composition and environmental filtering are the primary drivers structuring the AMF community. Phylogenetic relatedness may be important in explaining the function of AMF communities in alpine ecosystems.
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Altitude , Micorrizas , Plantas/microbiologia , Biodiversidade , Biomassa , Ecossistema , Genes Fúngicos , Metagenoma , Metagenômica/métodos , Micobioma , Micorrizas/classificação , Micorrizas/genética , Filogenia , Solo/química , Microbiologia do Solo , TibetRESUMO
The soil microbiome is highly diverse and comprises up to one quarter of Earth's diversity. Yet, how such a diverse and functionally complex microbiome influences ecosystem functioning remains unclear. Here we manipulated the soil microbiome in experimental grassland ecosystems and observed that microbiome diversity and microbial network complexity positively influenced multiple ecosystem functions related to nutrient cycling (e.g. multifunctionality). Grassland microcosms with poorly developed microbial networks and reduced microbial richness had the lowest multifunctionality due to fewer taxa present that support the same function (redundancy) and lower diversity of taxa that support different functions (reduced functional uniqueness). Moreover, different microbial taxa explained different ecosystem functions pointing to the significance of functional diversity in microbial communities. These findings indicate the importance of microbial interactions within and among fungal and bacterial communities for enhancing ecosystem performance and demonstrate that the extinction of complex ecological associations belowground can impair ecosystem functioning.
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Bactérias , Biodiversidade , Ecossistema , Fungos , Pradaria , Microbiota , Microbiologia do Solo , Ecologia , Consórcios MicrobianosRESUMO
Droughts associated with climate change alter ecosystem functions, especially in systems characterized by low biodiversity, such as agricultural fields. Management strategies aimed at buffering climate change effects include the enhancement of intraspecific crop diversity as well as the diversity of beneficial interactions with soil biota, such as arbuscular mycorrhizal fungi (AMF). However, little is known about reciprocal relations of crop and AMF diversity under drought conditions. To explore the interactive effects of plant genotype richness and AMF richness on plant yield under ambient and drought conditions, we established fully crossed diversity gradients in experimental microcosms. We expected highest crop yield and drought tolerance at both high barley and AMF diversity. While barley richness and AMF richness altered the performance of both barley and AMF, they did not mitigate detrimental drought effects on the plant and AMF. Root biomass increased with mycorrhiza colonization rate at high AMF richness and low barley richness. AMF performance increased under higher richness of both barley and AMF. Our findings indicate that antagonistic interactions between barley and AMF may occur under drought conditions, particularly so at higher AMF richness. These results suggest that unexpected alterations of plant-soil biotic interactions could occur under climate change.
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Biodiversidade , Secas , Ecossistema , Hordeum/genética , Micorrizas/classificação , Genótipo , Hordeum/metabolismo , Hordeum/microbiologia , Micorrizas/genética , Micorrizas/isolamento & purificação , Micorrizas/metabolismo , Microbiologia do SoloRESUMO
Soil microbes are known to be key drivers of several essential ecosystem processes such as nutrient cycling, plant productivity and the maintenance of plant species diversity. However, how plant species diversity and identity affect soil microbial diversity and community composition in the rhizosphere is largely unknown. We tested whether, over the course of 11 years, distinct soil bacterial communities developed under plant monocultures and mixtures, and if over this time frame plants with a monoculture or mixture history changed in the bacterial communities they associated with. For eight species, we grew offspring of plants that had been grown for 11 years in the same field monocultures or mixtures (plant history in monoculture vs. mixture) in pots inoculated with microbes extracted from the field monoculture and mixture soils attached to the roots of the host plants (soil legacy). After 5 months of growth in the glasshouse, we collected rhizosphere soil from each plant and used 16S rRNA gene sequencing to determine the community composition and diversity of the bacterial communities. Bacterial community structure in the plant rhizosphere was primarily determined by soil legacy and by plant species identity, but not by plant history. In seven of the eight plant species the number of individual operational taxonomic units with increased abundance was larger when inoculated with microbes from mixture soil. We conclude that plant species richness can affect below-ground community composition and diversity, feeding back to the assemblage of rhizosphere bacterial communities in newly establishing plants via the legacy in soil.
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Biodiversidade , Microbiota/fisiologia , Microbiota/genética , RNA Ribossômico 16S/genética , Rizosfera , Microbiologia do SoloRESUMO
Concern about the functional consequences of unprecedented loss in biodiversity has prompted biodiversity-ecosystem functioning (BEF) research to become one of the most active fields of ecological research in the past 25 years. Hundreds of experiments have manipulated biodiversity as an independent variable and found compelling support that the functioning of ecosystems increases with the diversity of their ecological communities. This research has also identified some of the mechanisms underlying BEF relationships, some context-dependencies of the strength of relationships, as well as implications for various ecosystem services that mankind depends upon. In this paper, we argue that a multitrophic perspective of biotic interactions in random and non-random biodiversity change scenarios is key to advance future BEF research and to address some of its most important remaining challenges. We discuss that the study and the quantification of multitrophic interactions in space and time facilitates scaling up from small-scale biodiversity manipulations and ecosystem function assessments to management-relevant spatial scales across ecosystem boundaries. We specifically consider multitrophic conceptual frameworks to understand and predict the context-dependency of BEF relationships. Moreover, we highlight the importance of the eco-evolutionary underpinnings of multitrophic BEF relationships. We outline that FAIR data (meeting the standards of findability, accessibility, interoperability, and reusability) and reproducible processing will be key to advance this field of research by making it more integrative. Finally, we show how these BEF insights may be implemented for ecosystem management, society, and policy. Given that human well-being critically depends on the multiple services provided by diverse, multitrophic communities, integrating the approaches of evolutionary ecology, community ecology, and ecosystem ecology in future BEF research will be key to refine conservation targets and develop sustainable management strategies.
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High biodiversity aboveground tends to increase the stability of ecosystem functioning when faced with a changing environment. However, whether and how soil biota affect ecosystem stability is less clear. Here, we introduce a framework for understanding the effects of soil biota on variation in ecosystem functioning under environmental changes. We conclude that soil biota may be a neglected factor determining ecosystem stability through their direct and indirect effects on plant diversity, the net productivity of an ecosystem, and compensatory dynamics among plant species, and via altering ecosystem resistance and resilience. Furthermore, future research needs to consider that effects of soil biota on ecosystem stability will vary depending on extrinsic factors, and for a given perturbation and ecosystem function.
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Ecossistema , Microbiologia do Solo , Biodiversidade , Micorrizas/fisiologia , Plantas/microbiologiaRESUMO
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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Research on mycorrhizal interactions has traditionally developed into separate disciplines addressing different organizational levels. This separation has led to an incomplete understanding of mycorrhizal functioning. Integration of mycorrhiza research at different scales is needed to understand the mechanisms underlying the context dependency of mycorrhizal associations, and to use mycorrhizae for solving environmental issues. Here, we provide a road map for the integration of mycorrhiza research into a unique framework that spans genes to ecosystems. Using two key topics, we identify parallels in mycorrhiza research at different organizational levels. Based on two current projects, we show how scientific integration creates synergies, and discuss future directions. Only by overcoming disciplinary boundaries, we will achieve a more comprehensive understanding of the functioning of mycorrhizal associations.
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Micorrizas/fisiologia , Raízes de Plantas/microbiologia , SimbioseRESUMO
Soil microbial communities affect species demographic rates of plants. In turn, plants influence the composition and function of the soil microbiome, potentially resulting in beneficial feedbacks that alter their fitness and establishment. For example, differences in the ability to stimulate soil enzyme activity among plant lineages may affect plant growth and reproduction. We used a common garden study to test differences in plant-stimulated soil enzyme activity between lineages of the same species across developmental stages. Lineages employed different strategies whereby growth, days to flowering and seed size traded-off with plant-stimulated soil enzyme activity. Specifically, the smaller seeded lineage stimulated more enzyme activity at the early stage of development and flowered earlier while the larger seeded lineage sustained lower but consistent enzyme activity through development. We suggest that these lineages, which are both successful invaders, employ distinct strategies (a colonizer and a competitor) and differ in their influence on soil microbial activity. Synthesis. The ability to influence the soil microbial community by plants may be an important trait that trades off with growth, flowering, and seed size for promoting plant establishment, reproduction, and invasion.