Feedbacks of plant identity and diversity on the diversity and community composition of rhizosphere microbiomes from a long-term biodiversity experiment

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.</p

Plant responses to diversity‐driven selection and associated rhizosphere microbial communities

Plant diversity loss can alter plant–plant and plant–rhizosphere microbiome interactions. These altered interactions, in turn, may exert diversity‐driven selection pressure to which plants respond with phenotypic changes. Diverse plant communities may favour the survival and fitness of individuals with traits that avoid competition. Conversely, monocultures may accumulate species‐specific pests favouring greater investment in defence traits. Yet, it is unknown how altered plant rhizosphere interactions influence the plant diversity‐driven selection for altered plant phenotypes. We tested for plant diversity‐driven selection on plant above‐ground traits and how these traits are modified by their rhizosphere microbial communities after 11 years in experimental plant monocultures and mixtures. Plants propagated from monocultures or mixtures were grown in combination with their ‘home’ versus ‘away’ arbuscular mycorrhizal fungi (AMF) or non‐AMF microbes in two separate experiments using five and eight plant species, respectively. We hypothesized that plants in monocultures may be selected for better defence and better performance in association with rhizosphere microbial communities compared with plants in mixtures. Monoculture and mixture plants significantly differed in their above‐ground phenotypes. As predicted, plant traits related to defence (greater leaf mass per area and leaf dry matter content, reduced leaf damage) were more pronounced in monoculture plants in both experiments. Effects of the rhizosphere microbial communities, which generally enhanced plant growth, tended to be species‐specific. Significant three‐way interactions between diversity‐driven selection, AMF treatment and plant species showed that home versus away effects could be positive or negative, depending on plant species. We conclude that long‐term differences in plant diversity lead to selection for altered plant phenotypes. Such differences may be further modified in association with the AMF microbial communities derived from the different plant diversity treatments, but often outcomes are species‐specific. This suggests that plant species differ in their capacity to respond to diversity loss and associated changes in rhizosphere microbial communities, making it complicated to predict community‐level responses to such loss

Co‐occurrence history increases ecosystem stability and resilience in experimental plant communities

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

Evolution increases ecosystem temporal stability and recovery from a flood in grassland communities

Understanding factors that increase ecosystem stability is critical in the face of environmental change. Biodiversity plays a key role in buffering ecosystems against disturbances such as extreme climatic events. The evolution of biological communities within their local environment may also increase ecosystem stability and resilience, but this has yet to be tested. Here, we provide evidence for such evolutionary effects using a long-term grassland biodiversity experiment. Communities of plants with a history of co-occurrence (co-selected communities) were temporally more stable at low diversity than the same communities of plants with no such history (naïve communities). Furthermore, co-selected communities exhibited greater recovery following a major flood, resulting in more stable post-flood productivity. These results demonstrate that community evolution can increase ecosystem stability under normal circumstances and in response to extreme disturbance, but also suggest that high diversity can in part compensate for evolutionary naïvety