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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., (© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.)

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.

Habitat specialization underpins biological processes from species distributions to speciation. However, organisms are often described as specialists or generalists based on a single niche axis, despite facing complex, multidimensional environments. Here, we analysed 236 environmental soil microbiomes across the United States and demonstrate that 90% of >1,200 prokaryotes followed one of two trajectories: specialization on all niche axes (multidimensional specialization) or generalization on all axes (multidimensional generalization). We then documented that this pervasive multidimensional specialization/generalization had many ecological and evolutionary consequences. First, multidimensional specialization and generalization are highly conserved with very few transitions between these two trajectories. Second, multidimensional generalists dominated communities because they were 73 times more abundant than specialists. Lastly, multidimensional specialists played important roles in community structure with ~220% more connections in microbiome networks. These results indicate that multidimensional generalization and specialization are evolutionarily stable with multidimensional generalists supporting larger populations and multidimensional specialists playing important roles within communities, probably stemming from their overrepresentation among pollutant detoxifiers and nutrient cyclers. Taken together, we demonstrate that the vast majority of soil prokaryotes are restricted to one of two multidimensional niche trajectories, multidimensional specialization or multidimensional generalization, which then has far-reaching consequences for evolutionary transitions, microbial dominance and community roles., (© 2023. The Author(s), under exclusive licence to Springer Nature Limited.)

Soil microbiota from stressful environments provide an avenue for climate resilience.

The rapid human-driven changes in the environment during the Anthropocene have placed extreme stress on many plants and animals. Beneficial interactions with microorganisms may be crucial for ameliorating these stressors and facilitating the ecosystem services host organisms provide. Foliar endophytes, microorganisms that reside within leaves, are found in essentially all plants and can provide important benefits (e.g., enhanced drought tolerance or resistance to herbivory). However, it remains unclear how important the legacy effects of the abiotic stressors that select on these microbiomes are for affecting the degree of stress amelioration provided to their hosts. To elucidate foliar endophytes' role in host-plant salt tolerance, especially if salinity experienced in the field selects for endophytes that are better suited to improve the salt tolerance of their hosts, we combined field collections of 90 endophyte communities from 30 sites across the coastal Everglades with a manipulative growth experiment assessing endophyte inoculation effects on host-plant performance. Specifically, we grew >350 red mangrove (Rhizophora mangle) seedlings in a factorial design that manipulated the salinity environment the seedlings experienced (freshwater vs. saltwater), the introduction of field-collected endophytes (live vs. sterilized inoculum), and the legacy of salinity stress experienced by these introduced endophytes, ranging from no salt stress (0 parts per thousand [ppt] salinity) to high salt stress (40 ppt) environments. We found that inoculation with field-collected endophytes significantly increased mangrove performance across almost all metrics examined (15%-20% increase on average), and these beneficial effects typically occurred when the endophytes were grown in saltwater. Importantly, our study revealed the novel result that endophyte-conferred salinity tolerance depended on microbiome salinity legacy in a key coastal foundation species. Salt-stressed mangroves inoculated with endophyte microbiomes from high-salinity environments performed, on average, as well as plants grown in low-stress freshwater, while endophytes from freshwater environments did not relieve host salinity stress. Given the increasing salinity stress imposed by sea level rise and the importance of foundation species like mangroves for ecosystem services, our results indicate that consideration of endophytic associations and their salinity legacy may be critical for the successful restoration and management of coastal habitats., (© 2022 The Ecological Society of America.)

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., (© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.)

Habitat fragmentation is a leading cause of biodiversity and ecosystem function loss in the Anthropocene. Despite the importance of plant-microbiome interactions to ecosystem productivity, we have limited knowledge of how fragmentation affects microbiomes and even less knowledge of its consequences for microbial interactions with plants. Combining field surveys, microbiome sequencing, manipulative experiments, and random forest models, we investigated fragmentation legacy effects on soil microbiomes in imperiled pine rocklands, tested how compositional shifts across 14 fragmentation-altered soil microbiomes affected performance and resource allocation of three native plant species, and identified fragmentation-responding microbial families underpinning plant performance. Legacies of habitat fragmentation were associated with significant changes in microbial diversity and composition (across three of four community axes). Experiments showed plants often strongly benefited from the microbiome's presence, but fragmentation-associated changes in microbiome composition also significantly affected plant performance and resource allocation across all seven metrics examined. Finally, random forest models identified ten fungal and six bacterial families important for plant performance that changed significantly with fragmentation. Our findings not only support the existence of significant fragmentation effects on natural microbiomes, but also demonstrate for the first time that fragmentation-associated changes in microbiomes can have meaningful consequences for native plant performance and investment., (© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.)

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.

Microbiomes can dramatically alter individual plant performance, yet how these effects influence higher-order processes is not well resolved. In particular, little is known about how microbiome effects on individual plants alter plant population dynamics, a question critical to imperiled species conservation. Here we integrate bioassays, multidecadal demographic data, and integral projection modeling to determine how the presence of the natural soil microbiome underlies plant population dynamics. Simulations indicated that the presence of soil microbiomes boosted population growth rates (λ) of the endangered Hypericum cumulicola by 13% on average, the difference between population growth versus decline in 76% of patches. The greatest benefit (47% increase in λ) occurred in low-nutrient, high-elevation habitats, suggesting that the soil microbiome may help expand H. cumulicola 's distribution to include these stressful habitats. Our results demonstrate that soil microbiomes can significantly affect plant population growth and persistence and support the incorporation of soil microbiomes into conservation planning.

A key challenge to understanding microbiomes and their role in ecological processes is contextualizing their effects on host organisms, particularly when faced with environmental stress. One influential theory, the Stress Gradient Hypothesis, might predict that the frequency of positive interactions increases with stressful conditions such that microbial taxa would mitigate harmful effects on host performance. Yet, equally plausible is that microbial taxa could exacerbate these effects. Here, we introduce the Mitigation-Exacerbation Continuum as a novel framework to conceptualize microbial mediation of stress. We (1) use this continuum to quantify microbial mediation of stress for six plant species and (2) test the association between these continuum values and natural species' abundance. We factorially manipulated a common stress (allelopathy) and the presence of soil microbes to quantify microbial effects in benign and stressed environments for two critical early life-history metrics, seed germination and seedling biomass. Although we found evidence of both mitigation and exacerbation among the six species, exacerbation was more common. Across species, the degree of microbial-mediated effects on germination explained >80% of the variation of natural field abundances. Our results suggest a critical role of soil microbes in mediating plant stress responses, and a potential microbial mechanism underlying species abundance., (© 2018 by the Ecological Society of America.)