Search for: All records

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. 

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. 

Summary 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. 

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 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. 

Summary 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.