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ABSTRACT As environments worldwide change at unprecedented rates during the Anthropocene, understanding context dependency—how species interactions vary depending on environmental context—is crucial. Combining comparative genomics across 42 angiosperms with transcriptomics, genome‐wide association mapping and gene duplication origin analyses, we show for the first time that gene family expansions are important to context‐dependent regulation of species interactions. Gene families expanded in mycorrhizal fungi‐associating plants display up to 200% more context‐dependent gene expression and double the genetic variation associated with mycorrhizal benefits to plant fitness. Moreover, we discover these gene family expansions arise primarily from tandem duplications with > 2‐times more tandem duplications genome‐wide, indicating gene family expansions continuously supply genetic variation, allowing fine‐tuning of context dependency in species interactions throughout plant evolution. Taken together, our results spotlight how widespread gene duplications can provide molecular flexibility required for plant–microbial interactions to match changing environmental conditions. 

Summary Plant microbiomes have the potential to mitigate the impacts of climate change, yet both the complexity of climate change and the complexity of plant–microbe interactions make applications and future predictions challenging. Here, we embrace this complexity, reviewing how different aspects of climate change influence beneficial plant–microbe interactions and how advances in theory, tools, and applications may improve understanding and predictability of climate change effects on plants, microbiomes, and their roles within ecosystems. New advances include consideration of (1) interactions among climate stressors, such as more variable precipitation regimes combined with warmer mean temperature; (2) mechanisms that promote the stability of microbiome functions; (3) legacies of stress affecting the functionality of microbial communities under future stress; and (4) temporally repeated plant–microbe interactions or feedbacks. We also identify key gaps in each of these areas and spotlight the need for more research bridging molecular biology and ecology to develop a more mechanistic understanding of how climate change shapes beneficial microbe–plant interactions. 

ABSTRACT Understanding the impact of microbial interactions on plants is critical for maintaining healthy native ecosystems and sustainable agricultural practices. Despite the reality that genetically distinct plants host multiple microbes of large effect in the field, it remains unclear the extent to which host genotypes modulate non‐additive microbial interactions and how these interactions differ between benign/pathogenic environments. Our study fills this gap by performing a large‐scale manipulative microbiome experiment across seven genotypes of the model legumeMedicago truncatula. We combine plant performance metrics, survival analyses, predictive modelling, RNA extractions and targeted gene expression to assess how host genotype and microbes non‐additively interact to shape plant growth and disease ecology. Our results reveal three important findings: (1) host genotypes with high tolerance to pathogens benefit more from multiple mutualist interactions than susceptible genotypes, (2) only high‐tolerance genotypes retain the same beneficial host performance outcomes from the benign environment within the pathogenic environment and (3) the quality of the symbiotic relationship with mutualists is a strong predictor of host survival against pathogenic disease. By applying these findings towards developing crops that promote synergistic microbial interactions, yields and pathogen defence could be simultaneously increased while reducing the need for toxic fertilisers and pesticides. 

ABSTRACT Microorganisms underpin numerous ecosystem processes and support biodiversity globally. Yet, we understand surprisingly little about what structures environmental microbiomes, including how to efficiently identify key players. Microbiome network theory predicts that highly connected hubs act as keystones, but this has never been empirically tested in nature. Combining culturing, sequencing, networks and field experiments, we isolated ‘central’ (highly connected, hub taxa), ‘intermediate’ (moderately connected), and ‘peripheral’ (weakly/unconnected) microbes and experimentally evaluated their effects on soil microbiome assembly during early succession in nature. Central early colonisers significantly (1) enhanced biodiversity (35%–40% richer communities), (2) reshaped trajectories of microbiome assembly and (3) increased recruitment of additional influential microbes by > 60%. In contrast, peripheral microbes did not increase diversity and were transient taxa, minimally affected by the presence of other microbes. This work elucidates fundamental principles of network theory in microbial ecology and demonstrates for the first time in nature that central microbes act as keystone taxa. 

Abstract As ecosystems face unprecedented change and habitat loss, pursuing comprehensive and resilient habitat restoration will be integral to protecting and maintaining natural areas and the services they provide. Microbiomes offer an important avenue for improving restoration efforts as they are integral to ecosystem health and functioning. Despite microbiomes' importance, unresolved knowledge gaps hinder their inclusion in restoration efforts. Here, we address two critical gaps in understanding microbial roles in restoration—fungal microbiomes' importance in “reconstructive” restoration efforts and how management and restoration decisions interactively impact fungal communities and their cascading effects on trees. We combined field surveys, microbiome sequencing, and greenhouse experiments to determine how reconstructing an iconic landscape feature—tree islands—in the highly imperiled Everglades impacts fungal microbiomes and fungal effects on native tree species compared with their natural counterparts under different proposed hydrological management regimes. Constructed islands used in this research were built from peat soil and limestone collected from deep sloughs and levees nearby the restoration sites in 2003, providing 18 years for microbiome assembly on constructed islands. We found that while fungal microbiomes from natural and constructed tree islands exhibited similar diversity and richness, they differed significantly in community composition. These compositional differences arose mainly from changes to which fungal taxa were present on the islands rather than changes in relative abundances. Surprisingly, ~50% of fungal hub taxa (putative keystone fungi) from natural islands were missing on constructed islands, suggesting that differences in community composition of constructed island could be important for microbiome stability and function. The differences in fungal composition between natural and constructed islands had important consequences for tree growth. Specifically, these compositional differences interacted with hydrological regime (treatments simulating management strategies) to affect woody growth across the four tree species in our experiment. Taken together, our results demonstrate that reconstructing a landscape feature without consideration of microbiomes can result in diverging fungal communities that are likely to interact with management decisions leading to meaningful consequences for foundational primary producers. Our results recommend cooperation between restoration practitioners and ecologists to evaluate opportunities for active management and restoration of microbiomes during future reconstructive restoration. 

Summary Plants naturally harbor diverse microbiomes that can dramatically impact their health and productivity. However, it remains unclear how fungal microbiome diversity, especially in the phyllosphere, impacts intermicrobial interactions and consequent nonadditive effects on plant productivity.Combining manipulative experiments, field collections, culturing, microbiome sequencing, and synthetic consortia, we experimentally tested for the first time how foliar fungal community diversity impacts plant productivity. We inoculated morning glories (Ipomoea hederifoliaL.) with 32 phyllosphere consortia of either low or high diversity or with single fungal taxa, and measured effects on plant productivity and allocation.We found the following: (1) nonadditive effects were pervasive with 56% of fungal consortia interacting synergistically or antagonistically to impact plant productivity, including some consortia capable of generating acute synergism (e.g. > 1000% increase in productivity above the additive expectation), (2) interactions among ‘commensal’ fungi were responsible for this nonadditivity in diverse consortia, (3) synergistic interactions were approximately four times stronger than antagonistic effects, (4) fungal diversity affected the magnitude but not frequency or direction of nonadditivity, and (5) diversity affected plant performance nonlinearly with the highest performance in low‐diversity treatments.These findings highlight the importance of interpreting plant–microbiome interactions under a framework that incorporates intermicrobial interactions and nonadditive outcomes to understand natural complexity. 

Abstract Anthropogenic habitat fragmentation—the breaking up of natural landscapes—is a pervasive threat to biodiversity and ecosystem function world‐wide. Fragmentation results in a mosaic of remnant native habitat patches embedded in human‐modified habitat known as the ‘matrix’. By introducing novel environmental conditions in matrix habitats and reducing connectivity of native habitats, fragmentation can dramatically change how organisms experience their environment. The effects of fragmentation can be especially important in urban landscapes, which are expanding across the globe. Despite this surging threat and the importance of microbiomes for ecosystem services, we know very little about how fragmentation affects microbiomes and even less about their consequences for plant–microbe interactions in urban landscapes.By combining field surveys, microbiome sequencing and experimental mesocosms, we (1) investigated how microbial community diversity, composition and functional profiles differed between 15 native pine rockland fragments and the adjacent urban matrix habitat, (2) identified habitat attributes that explained significant variation in microbial diversity of native core habitat compared to urban matrix and (3) tested how changes in urbanized and low connectivity microbiomes affected plant community productivity.We found urban and native microbiomes differed substantively in diversity, composition and functional profiles, including symbiotic fungi decreasing 81% and pathogens increasing 327% in the urban matrix compared to native habitat. Furthermore, fungal diversity rapidly declined as native habitats became increasingly isolated, with ~50% of variation across the landscape explained by habitat connectivity alone. Interestingly, microbiomes from native habitats increased plant productivity by ~300% while urban matrix microbiomes had no effect, suggesting that urbanization may decouple beneficial plant–microbe interactions. In addition, microbial diversity within native habitats explained significant variation in plant community productivity, with higher productivity linked to more diverse microbiomes from more connected, larger fragments.Synthesis. Taken together, our study not only documents significant changes in microbial diversity, composition and functions in the urban matrix, but also supports that two aspects of habitat fragmentation—the introduction of a novel urban matrix and reduced habitat connectivity—disrupt microbial effects on plant community productivity, highlighting preservation of native microbiomes as critical for productivity in remnant fragments. 

Summary 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. 

Abstract 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. 

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.