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Habitat heterogeneity is a key driver of biodiversity of macroorganisms, yet how heterogeneity structures belowground microbial communities is not well understood. Importantly, belowground microbial communities may respond to any number of abiotic, biotic, and spatial drivers found in heterogeneous environments. Here, we examine potential drivers of prokaryotic and fungal communities in soils across the heterogenous landscape of the imperiled Florida scrub, a pyrogenic ecosystem where slight differences in elevation lead to large changes in water and nutrient availability and vegetation composition. We employ a comprehensive, large-scale sampling design to characterize the communities of prokaryotes and fungi associated with three habitat types and two soil depths (crust and subterranean) to evaluate (i) differences in microbial communities across these heterogeneous habitats, (ii) the relative roles of abiotic, biotic, and spatial drivers in shaping community structure, and (iii) the distribution of fungal guilds across these habitats. We sequenced soils from 40 complete replicates of habitat × soil depth combinations and sequenced the prokaryotic 16S and fungal internal transcribed spacer (ITS) regions using Illumina MiSeq. Habitat heterogeneity generated distinct communities of soil prokaryotes and fungi. Spatial distance played a role in structuring crust communities, whereas subterranean microbial communities were primarily structured by the shrub community, whose roots they presumably interacted with. This result helps to explain the unexpected transition we observed between arbuscular mycorrhiza–dominated soils at low-elevation habitats to ectomycorrhiza-dominated soils at high-elevation habitats. Our results challenge previous notions of environmental determinism of microbial communities and generate new hypotheses regarding symbiotic relationships across heterogeneous environments. 

Introductions are a critical tool in the recovery of many imperiled species, yet adequate evaluation and development of best practices has lagged. Importantly, long‐term post‐introduction data are typically lacking, as well as suitable comparisons to wild populations to provide a baseline against which to assess performance. Here, we report on three experimental introductions ofCrotalaria avonensis(Fabaceae), a federally endangered perennial herb that is narrowly endemic to scrub of the Lake Wales Ridge in peninsular Florida, U.S.A. We synthesize 10 years of post‐introduction monitoring at both the introduced and a nearby, protected wild population to (1) develop best practices for conservation, and (2) evaluate the success of the introduction. First, our study identified best practices that included using transplants propagated from stem cuttings, as well as several factors that may increase seed germination such as habitat choice, seed burial, and litter addition. Second, during the 10 years following the introduction, population density in the introduced population was higher than in a nearby protected, wild population, and a comparison of vital rates revealed that this result was due to relatively high clonal and seedling recruitment rates in the introduced population. Furthermore, the source population, which occurred on unprotected lands, precipitously declined during this time period, further highlighting the importance of safeguarding plants from that population. We report that a new, growing population ofC. avonensishas been established to date, with important implications for the species' conservation as well as how introductions are evaluated.

 

Allelopathy is a common and important stressor that shapes plant communities and can alter soil microbiomes, yet little is known about the direct effects of allelochemical addition on bacterial and fungal communities or the potential for allelochemical‐selected microbiomes to mediate plant performance responses, especially in habitats naturally structured by allelopathy.

Here, we present the first community‐wide investigation of microbial mediation of allelochemical effects on plant performance by testing how allelopathy affects soil microbiome structure and how these microbial changes impact germination and productivity across 13 plant species.

The soil microbiome exhibited significant changes to ‘core’ bacterial and fungal taxa, bacterial composition, abundance of functionally important bacterial and fungal taxa, and predicted bacterial functional genes after the addition of the dominant allelochemical native to this habitat. Furthermore, plant performance was mediated by the allelochemical‐selected microbiome, with allelopathic inhibition of plant productivity moderately mitigated by the microbiome.

Through our findings, we present a potential framework to understand the strength of plant–microbial interactions in the presence of environmental stressors, in which frequency of the ecological stress may be a key predictor of microbiome‐mediation strength.

 

Environmental stress is increasing worldwide, yet we lack a clear picture of how stress disrupts the stability of microbial communities and the ecosystem services they provide. Here, we present the first evidence that naturally-occurring microbiomes display network properties characteristic of unstable communities when under persistent stress. By assessing changes in diversity and structure of soil microbiomes along 40 replicate stress gradients (elevation/water availability gradients) in the Florida scrub ecosystem, we show that: (1) prokaryotic and fungal diversity decline in high stress, and (2) two network properties of stable microbial communities—modularity and negative:positive cohesion—have a clear negative relationship with environmental stress, explaining 51–78% of their variation. Interestingly, pathogenic taxa/functional guilds decreased in relative abundance along the stress gradient, while oligotrophs and mutualists increased, suggesting that the shift in negative:positive cohesion could result from decreasing negative:positive biotic interactions consistent with the predictions of the Stress Gradient Hypothesis. Given the crucial role microbiomes play in ecosystem functions, our results suggest that, by limiting the compartmentalization of microbial associations and creating communities dominated by positive associations, increasing stress in the Anthropocene could destabilize microbiomes and undermine their ecosystem services.

 

Fire plays a major role in structuring plant communities across the globe. Interactions with soil microbes impact plant fitness, scaling up to influence plant populations and distributions. Here we present the first factorial manipulation of both fire and soil microbiome presence to investigate their interactive effects on plant performance across a suite of plant species with varying life history traits.

We conducted fully factorial experiments on 11 species from the Florida scrub ecosystem to test plant performance responses to soils with varying fire histories (36 soil sources), the presence/absence of a microbiome, and exposure to an experimental burn.

Results revealed interactive ‘pulse’ effects between fire and the soil microbiome on plant performance. On average, post‐fire soil microbiomes strongly reduced plant productivity compared to unburned or sterilized soils. Interestingly, longer‐term fire ‘legacy’ effects had minor impacts on plant performance and were unrelated to soil microbiomes.

While pulse fire effects on plant–microbiome interactions are short‐term, they could have long‐term consequences for plant communities by establishing differential microbiome‐mediated priority effects during post‐disturbance succession. The prominence of pulse fire effects on plant–microbe interactions has even greater import due to expected increases in fire disturbances resulting from anthropogenic climate change.

 

Microbial symbionts can buffer plant hosts from environmental change. Therefore, understanding how global change factors alter the associations between hosts and their microbial symbionts may improve predictions of future changes in host population dynamics and microbial diversity. Here, we investigated how one global change factor, precipitation, affected the maintenance or loss of symbiotic fungal endophytes in a C₃grass host. Specifically, we examined the distinct responses ofEpichloë(vertically transmitted and systemic) and non‐epichloid endophytes (typically horizontally transmitted and localized) by considering (1) how precipitation altered associations withEpichloëand non‐epichloid endophytic taxa across host ontogeny, and (2) interactive effects of water availability andEpichloëon early seedling life history stages.

We manipulated the presence ofEpichloë amarillansin American beachgrass (Ammophila breviligulata) in a multiyear field experiment that imposed three precipitation regimes (ambient or ±30% rainfall). In laboratory assays, we investigated the interactive effects of water availability andEpichloëon seed viability and germination.

Reduced precipitation decreased the incidence ofEpichloëin leaves in the final sampling period, but had no effect on associations with non‐epichloid taxa.Epichloëreduced the incidence of non‐epichloid endophytes, including systemic p‐endophytes, in seeds. Laboratory assays suggested that association withEpichloëis likely maintained, in part, due to increased seed viability and germination regardless of water availability.

Our study empirically demonstrates several pathways for plant symbionts to be lost or maintained across host ontogeny and suggests that reductions in precipitation can drive the loss of a plant's microbial symbionts.

 

Disentangling the ecological factors that contribute to the assembly of the microbial symbiont communities within eukaryotic hosts is an ongoing challenge. Broadly speaking, symbiont propagules arrive either from external sources in the environment or from internal sources within the same host individual. To understand the relative importance of these propagule sources to symbiont community assembly, we characterized symbiotic fungal endophyte communities within the roots of three species of beachgrass in a field experiment. We manipulated two aspects of the external environment, successional habitat and physical disturbance. To determine the role of internal sources of propagules for endophyte community assembly, we used beachgrass individuals with different pre‐existing endophyte communities. Endophyte species richness and community composition were characterized using culture‐based and next‐generation sequencing approaches. Our results showed that external propagule sources associated with successional habitat, but not disturbance, were particularly important for colonization of most endophytic taxa. In contrast, internal propagule sources played a minor role for most endophytic taxa but were important for colonization by the dominant taxonMicrodochium bolleyi. Our findings highlight the power of manipulative field experiments to link symbiont community assembly to its underlying ecological processes, and to ultimately improve predictions of symbiont community assembly across environments.

 

Diversity and nitrogen addition have positive relationships with plant productivity, yet climate‐induced changes in water availability threaten to upend these established relationships. Using long‐term data from three experiments in a mesic grassland (ranging from 17 to 34 yr of data), we tested how the effects of species richness and nitrogen addition on community‐level plant productivity changed as a function of annual fluctuations in water availability using growing season precipitation and the Standardized Precipitation‐Evapotranspiration Index (SPEI). While results varied across experiments, our findings demonstrate that water availability can magnify the positive effects of both biodiversity and nitrogen addition on productivity. These results suggest that productivity responses to anthropogenic species diversity loss and increasing nitrogen deposition could depend on precipitation regimes, highlighting the importance of testing interactions between multiple global change drivers.