Search bioRxiv⌕ Search

Biology subjects

Afkhami, M. E.

Publications and source records attributed to Afkhami, M. E..

14 recordsLinked to original sources

Hidden drivers of restoration: Persistent divergence in soil microbiome functional capacity post-habitat reconstruction

Ecosystems today are facing unprecedented environmental stress, leading to large-scale losses of habitat and ecosystem services. To address this, reconstructive efforts aim to restore habitat features and their natural complexity, biodiversity, and function. However, many reconstructive efforts fail to consider microbial communities, even though they play key roles in decomposition, nutrient cycling, and plant and animal health. Here, we use shotgun metagenomic sequencing to compare the structure and functional capacity of soil microbial communities from natural Everglades tree islands and islands constructed within a landscape-scale experimental Everglades restoration effort, followed by a manipulative greenhouse experiment to link tree sapling traits with microbiome functional genetic divergence. We found that constructed and natural island microbiomes exhibited strong, robust, and persistent divergence in both taxonomic and functional composition, with natural island microbial communities having greater functional genetic diversity and redundancy. Furthermore, we identified enrichment in functional pathways in constructed island microbiomes such as those involved in pollutant degradation that may reflect continued disturbance leading to shifts in microbiome functional profiles. Despite their capacity for functions such as nitrogen cycling we found to be important for supporting sapling growth, constructed island microbiomes displayed reduced functional genetic diversity and redundancy and were enriched in pathways associated with environmental disturbance, suggesting a potentially diminished capacity for long-term resilience. Overall, our assessment of soil microbial communities in reconstructed and natural habitats emphasizes how reconstructive restoration can impact microbial functional repertoires and highlights the importance of these hidden players in management and restoration of ecosystem health.

ecology↗

Do microbial effects on hosts vary across life stage and vitalrate?

Interactions with microbial symbionts are widespread and can influence host fitness through effects on survival, growth, and reproduction. Demographic and evolutionary theory suggests that symbiont effects on components of host fitness should often vary in strength and even in direction as host and symbiont allocate limited resources. Through a meta-analysis of 1,736 host-symbiont effect size measurements, we evaluated how commonly the direction of symbiont effects varies across host life history stages and vital rates, and whether these effects across stages and vital rates differ across taxa. Contrary to our prediction, we found that, compared to a null expectation, published effects on host vital rates more often occurred consistently in the same direction, rather than in opposition. This finding suggests that symbiosis often provides benefits to host performance that manifest across vital rates. While the direction of symbiotic effect was often consistent, the magnitude of effects differed across fitness components and across host taxonomic groups, highlighting diverse demographic mechanisms by which symbiosis can influence host fitness. For hosts in the Poaceae family, we also found that effects of symbiosis varied across symbiont type: vertically-transmitted Epichloe fungi most strongly benefited seed germination, while the benefits of mycorrhizal fungi and bacterial endophytes were stronger for adult growth and reproduction. Importantly, this literature survey also highlights gaps in the current literature on host-microbe symbiosis. Most studies measure growth during juvenile stages for taxa from iconic, well-studied symbioses. Meta-analytic estimates of symbiotic effects on host life history provide a path towards quantitatively modeling host-symbiont demography across the tree of life.

ecology↗

Land-use intensity overrides grazing and precipitation effects on soil microbial communities in a subtropical agroecosystem

Global change drivers are reshaping agroecosystems and their sustained functions worldwide. While soil microorganisms underpin the resilience of these systems, the individual and interactive effects of multiple anthropogenic stressors on microbial community structure and function using large-scale field experiments remain poorly understood. Here, we utilize a full-factorial field experiment in a subtropical agroecosystem to investigate how land-use intensity, cattle grazing intensity, and altered precipitation regimes interact to shape soil microbiomes. Combining microbiome sequencing with network analyses and functional bioinformatics, we evaluated effects of these drivers on prokaryotic and fungal diversity, composition, predicted functional profiles, and community structure. Land-use intensity emerged as the primary driver of microbial responses, explaining 25% and 13% of the total variation in community composition for prokaryotes and fungi, respectively. Compared to intensively managed pastures, semi-natural pastures had significantly different community composition for prokaryotes and fungi and exhibited 22% higher fungal diversity. Semi-natural pastures were enriched with decomposer-associated taxa and metabolic pathways related to energy and lipid metabolism indicating enhanced microbial activity. Surprisingly, intensively managed pastures showed higher network modularity but lower network richness, suggesting a trade-off between community compartmentalization and complexity under intensive land management. Grazing and precipitation manipulations induced core microbiome changes within land-use intensities but had no impact on overall community structure and no significant interactions with land-use. Together, these findings suggest that long-term land-use legacies exert a persistent influence on soil microbial community structure, function, and organization, shaping the context within which other global change drivers operate in subtropical agroecosystems.

ecology↗

A novel pipeline for the rapid expansion of ecological trait databases using LLMs

This paper presents a novel workflow leveraging Large Language Models (LLMs) to rapidly extract trait data from fungal species descriptions, addressing a significant bottleneck in ecological research. We developed and evaluated an LLM pipeline to extract morphological trait data from arbuscular mycorrhizal fungi, comparing performance against a manually curated dataset (TraitAM). Results demonstrate the potential of LLMs for automated trait data acquisition, though accuracy varies by trait and model, with systematic biases observed. This framework offers a blueprint for building trait databases across diverse taxa and domains, significantly accelerating ecological research and conservation efforts.

ecology↗

Mutualistic microbes drive niche expansion yet constrain diversification

Mutualistic interactions are widely hypothesized to expand ecological niches and promote diversification, yet evidence for this relationship at macroevolutionary scales remains limited. Here, we investigate how fungal seed endophytes (Epichloe) influence niche breadth and diversification across over 100 species of the globally-distributed grass genus Poa. Combining global-scale climate, environmental, phylogenetic, and symbiosis data, we constructed species distribution models for suites of symbiotic and non-symbiotic plant species, then used a range of phylogenetic comparative methods to assess the influence of these symbionts on niche breadth, niche breadth evolution, and diversification. Endophyte-positive species had [~]1.4 times broader primary niche axes (most often associated with temperature tolerances), [~]2.5 times larger geographic ranges, and >30 times faster rates of niche breadth evolution than non-symbiotic species. Endophytic plants also had significantly drier climate centroids, consistent with endophyte-mediated drought tolerance, while simultaneously showing constraints along specific niche dimensions. Despite pronounced niche expansion, hidden state speciation and extinction models revealed two modes of diversification: endophytes decrease diversification rates in young lineages, and have a neutral effect in older lineages. Together, our results demonstrate that mutualists can enhance ecological flexibility while simultaneously constraining macroevolutionary outcomes, revealing a decoupling of niche expansion and diversification, and highlighting the complex role of symbiosis in shaping host evolutionary trajectories.

evolutionary biology↗

The microbial landscape: soil microbiome properties predict plant species distributions

Plant species distributions are shaped by interactions with the abiotic and biotic environment. Despite the known importance of soil microbiomes in shaping plant diversity and function, no study has explicitly determined the ability of the soil microbiome to predict plant species distributions at large scales. We employed paired above- and belowground surveys of plant occurrence and soil microbial taxa and functions across habitat patches (n = 676), applying machine-learning-based distribution modeling to identify the relative influence of the soil microbiome and environmental attributes in predicting plant species (n = 50) distributions across the landscape. We discovered that while abiotic gradients of known importance in this ecosystem were the strongest predictors of many plant species distributions, microbial predictors could have similar or greater influence. Microbiome predictors were collectively more important than abiotic environmental variables for 38% of plant species in this study and explained >70% of the predicted distribution for one species. We identified four microbiome attributes of landscape-scale importance for predicting plant species distributions including prokaryotic richness, fungal richness, the abundance of fungal pathogens, and the abundance of prokaryotic phosphate transport genes in soil. Our findings reveal a previously underappreciated role of the soil microbiome in shaping plant species distributions at a landscape scale, with implications for plant community structure in the context of both ecosystem restoration and future global change.

ecology↗

Climate variability disrupts mutualism-driven increases in population persistence

Understanding how species interactions impact population dynamics and long-term persistence over broad temporal and spatial scales is crucial for predicting species distributions and responses to global change. Here, we integrate range-wide field surveys of [~]90 grass host populations spanning 13 years with demographic modeling based on six-year common garden experiments conducted across the host range to demonstrate that mutualistic fungal endophytes promote population-level persistence and growth of their native host grass across its distribution, with non-mutualistic populations four times more likely to go locally extinct. Despite providing population-level benefits, endophyte prevalence declined eight-fold more in historically mutualistic populations that experienced high climate variability. Thus, mutualisms can underpin population persistence and buffer hosts against environmental stress, but may themselves be vulnerable to global change, with concerning implications for long-term population viability and, ultimately, species distributions under an increasingly uncertain climate.

ecology↗

Non-additive interactions between multiple mutualists and host plant genotype simultaneously promote increased plant growth and pathogen defense

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 7 genotypes of the model legume Medicago truncatula. We combine plant performance metrics, survival analyses, predictive modeling, 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) mutualists confer the same non-additive plant performance benefits in both benign and pathogenic environments, 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 defense could be simultaneously increased while reducing the need for toxic fertilizers and pesticides.

plant biology↗

50-year fire legacy regulates soil microbial carbon and nutrient cycling responses to new fire

Fire disturbances are becoming more common, more intense, and further-reaching across the globe, with consequences for ecosystem functioning. Importantly, fire can have strong effects on the soil microbiome, including community and functional changes after fire, but surprisingly little is known regarding the role of soil fire legacy in shaping responses to recent fire. To address this gap, we conducted a manipulative field experiment administering fire across 32 soils with varying fire legacies, including combinations of 1-7 historic fires and 1-33 years since most recent fire. We analyzed soil metatranscriptomes, determining for the first time how fire and fire legacy interactively affect metabolically-active soil taxa, the microbial regulation of important carbon (C), nitrogen (N) and phosphorus (P) cycling, expression of carbohydrate-cycling enzyme pathways, and functional gene co-expression networks. Experimental fire strongly downregulated fungal activity while upregulating many bacterial and archaeal phyla. Further, fire decreased soil capacity for microbial C and N cycling and P transport, and drastically rewired functional gene co-expression. Perhaps most importantly, we highlight a novel role of soil fire legacy in regulation of microbial C, N, and P responses to recent fire. We observed a greater number of functional genes responsive to the interactive effects of fire and fire legacy than those affected solely by recent fire, indicating that many functional genes respond to fire only under certain fire legacy contexts. Therefore, without incorporating fire legacy of soils, studies will miss important ways that fire shapes microbial roles in ecosystem functioning. Finally, we showed that fire caused significant downregulation of carbon metabolism and nutrient cycling genes in microbiomes under abnormal soil fire histories, producing a novel warning for the future: human manipulation of fire legacies, either indirectly through global change-induced fire intensification or directly through fire suppression, can negatively impact soil microbiome functional responses to new fires.

ecology↗

Gene family expansions underpin context-dependency of the oldest mycorrhizal symbiosis.

As environments worldwide change at unprecedented rates during the Anthropocene, understanding context-dependency - how species regulate interactions to match changing environments - is crucial. However, generalizable molecular mechanisms underpinning context-dependency remain elusive. 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 undergird 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. One-Sentence SummaryGene family expansions arising from tandem duplications underpin genetic regulation and fitness effects of context-dependency

evolutionary biology↗

Phyllosphere fungal diversity generates pervasive non-additive effects on plant performance

O_LIAll plants naturally harbor diverse microbiomes that can dramatically impact their health and productivity. However, it remains unclear how microbiome diversity, especially in the phyllosphere, impacts intermicrobial interactions and consequent non-additive effects on plant productivity. C_LIO_LICombining 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 with 32 synthetic phyllosphere communities of either low or high diversity or with single fungal taxa, and measured effects on plant productivity and allocation. C_LIO_LIWe found 1) non-additive effects were pervasive with 56% of microbial communities 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 non-additivity in diverse communities, 3) synergistic interactions were ~4 times stronger than antagonistic effects, 4) fungal diversity affected the magnitude but not frequency or direction of non-additivity, and 5) diversity affected plant performance nonlinearly with highest performance in low microbial diversity treatments. C_LIO_LIThese findings highlight the importance of interpreting plant-microbial interactions under a framework that incorporates intermicrobial interactions and non-additive outcomes to understand natural complexity. C_LI

ecology↗

Multidimensional specialization and generalization are pervasive in soil prokaryotes with generalists dominating communities and specialists more central in networks

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 analyzed 236 prokaryotic communities across the United States demonstrating for the first time 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 a wide range of 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 likely 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. One-Sentence SummaryPervasive multidimensional specialization and generalization impacts evolutionary trajectories, microbial dominance, and community roles.

microbiology↗

Hub taxa are keystone microbes during early succession

Microorganisms underpin numerous ecosystem processes and support biodiversity globally, yet we understand surprisingly little about what structures environmental microbiomes themselves. Combining culturing, sequencing, and microbial networks, we identified central (highly-connected, hub taxa), intermediate (moderately-connected), and peripheral (weakly/un-connected) microbes and experimentally evaluated their effects on soil microbiome assembly during early succession. Our results demonstrate central early colonizers significantly (1) enhanced biodiversity, (2) increased recruitment of additional influential, hub taxa, and (3) shaped microbiome assembly trajectories. This work elucidates fundamental principles of network theory in microbial ecology and demonstrates for the first time in nature that central, hub microbes are keystones.

microbiology↗

Multiple Mutualist Effects generate synergistic selection and strengthen fitness alignment in a tripartite interaction between legumes, rhizobia, and mycorrhizal fungi

Nearly all organisms interact with multiple mutualists, and complementarity within these complex interactions can result in synergistic fitness effects. However, it remains largely untested how multiple mutualists impact eco-evolutionary dynamics. We tested how multiple microbial mutualists-- N-fixing bacteria and mycorrrhizal fungi-- affected selection and heritability in their shared host plant (Medicago truncatula), as well as fitness alignment between partners. Our results demonstrate for the first time that multispecies mutualisms synergistically affect selection and heritability of host traits and enhance fitness alignment between mutualists. Specifically, we found that multiple mutualists doubled the strength of selection on a plant architectural trait, resulted in 2-3-fold higher heritability of reproductive success, and more than doubled the strength of fitness alignment between N-fixing bacteria and plants. Taken together, these findings show that synergism generated by multiple mutualisms extends to key components of microevolutionary change, and emphasizes the importance of multiple mutualist effects in understanding evolutionary trajectories.

ecology↗