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Bergelson, J.

Publications and source records attributed to Bergelson, J..

At least 19 recordsLinked to original sources

Multiple host species maintain genetic diversity in herbivore populations

How natural populations maintain genetic variation for fitness remains a central problem in evolutionary biology. Theory predicts that opposing selective pressures across environments can preserve fitness-associated polymorphism, but how interactions among species contribute to this process remains poorly understood. Here we show that host diversity preserves standing genetic variation within sexual populations of the leafmining fly Scaptomyza flava. We evolved twelve populations for ten generations on either of two naturally co-occurring host plants or on both, pooling survivors from the two hosts before mating. Single-host populations evolved reciprocal fitness trade-offs, whereas two-host populations maintained relatively even performance across hosts. Whole-genome time series dynamics identified a linked region in which alleles increased on one host and decreased on the other, while showing little net change under two-host conditions. Wild flies reared from the two hosts showed corresponding allele-frequency differences within this region. Across the genome, two-host populations retained more rare variants than populations evolving on either host alone. These findings show that selection imposed by different host species in sympatry can maintain standing genetic diversity within an herbivore population.

evolutionary biology↗

Deep sequencing artificially inflates estimates of microbial diversity

Sequencing artifacts challenge accuracy and reproducibility when quantifying microbial diversity. To track error propagation in microbiome analyses, we analyze no-diversity amplicons, which are amplified from host genes with limited genetic diversity or from synthetic spike-ins. We find that sequencing at greater than 104 reads exponentially increased no-diversity amplicon sequence variant (ASV) richness, with hundreds of ASVs observed per sample. This striking pattern was shared with microbial amplicons (16S rRNA, ITS, gyrB, rpoB), which revealed inflated Shannon diversity with an increase in read counts for both the community and within taxa. Comparing sequencing error profiles between no-diversity and microbial amplicons showed that truncating reads to shorter lengths and use of the AVITI Element platform can mitigate, but not abolish, the impacts of artificial inflation; we recommend caution when read depths vary orders of magnitude between samples. Overall, utilizing no-diversity amplicons can help optimize parameters to improve estimates of microbial diversity.

ecology↗

Biotic-response networks are an important organizer of the transcriptome in wild Arabidopsis thaliana populations

Extensive laboratory experimentation has revealed conserved molecular pathways controlling growth and stress responses in plants, yet how these programs operate in natural settings remains poorly understood. We investigated transcriptome organization in wild populations of Arabidopsis thaliana by sampling plants from 60 natural sites in Europe and North America across two seasons. Transcriptomes varied extensively among individuals and showed largely continuous rather than discrete structure across geography and season. Although disease and microbial colonization were common in the wild, wild transcriptomes did not simply recapitulate canonical laboratory stress signatures. Measured microbial infection, environmental, and phenotypic variables explained only a modest fraction of total expression variation, but infection-associated signals accounted for the largest share of the explainable component. Consistent with this, biotic-response networks defined in controlled laboratory experiments were well conserved in wild transcriptomes, whereas control and abiotic-response networks were substantially reorganized. Together, these results suggest that while core transcriptional modules remain recognizable across environments, regulatory relationships among modules differ markedly between laboratory and natural contexts. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=129 SRC="FIGDIR/small/711176v1_ufig1.gif" ALT="Figure 1"> View larger version (28K): org.highwire.dtl.DTLVardef@1c89152org.highwire.dtl.DTLVardef@bcd1acorg.highwire.dtl.DTLVardef@6975a2org.highwire.dtl.DTLVardef@1a9e2fe_HPS_FORMAT_FIGEXP M_FIG C_FIG

genomics↗

Natural selection acting on the genetics of host response to commensal bacteria

BackgroundMicrobiota members collectively contribute to individual performance in humans, animals, and plants. This led to the quest for probiotics to improve host health and reproductive performance. Although the efficacy of probiotics is known to be strongly affected by environmental factors, microbe-microbe interactions, and microbial strain identity, the effects of host genotype and the underlying genetic architecture have been overlooked. In addition, the evolutionary causes of such genetic variation are typically not addressed. In this study, we aimed to describe the genetic architecture of the adaptation of the host plant Arabidopsis thaliana to commensal bacterial members of its native microbiota by identifying candidate genes associated with fitness proxies and presenting signatures of natural selection. ResultsA Genome-Wide Association study conducted under field conditions revealed extensive variation within a new mapping population of 162 genotypes of A. thaliana scored for total seed production and its two underlying components, namely fruit number and mean seed number per fruit, in response to 13 commensal strains. In agreement with the strong host genotype x commensal strain identity interactions observed for each reproductive trait, the polygenic genetic architecture was highly flexible among the 13 commensal strains. Candidate genes exhibited a significant enrichment in signatures of both local adaptation and balancing selection. In line with the phenotyped reproductive traits, we identified seven candidate genes with functions specifically and strongly linked to seed germination and fertility. ConclusionsOur findings reveal the importance of genotype-by-genotype interactions when measuring fitness proxies on a wild plant species inoculated with key members of its native microbiota. In addition, this study improves our understanding of the genetic signatures of natural selection acting on native host-microbiota adaptive interactions.

evolutionary biology↗

Seasonality, land use, and diversity shape microbiome-pathogen interactions in wild populations of Arabidopsis thaliana

The microbiome often protects plants against pathogens, but most findings are limited to controlled experiments in the lab. In the context of wild populations, one key challenge is to understand sources of variation that impact the commensal microbiome, which in turn shapes the degree of protection. Here, we surveyed both disease symptoms and microbiomes from wild populations of Arabidopsis thaliana over four consecutive seasons (fall/spring) across three different land use types. Land use types varied in the extent of anthropogenic influences and included forest meadows, human-impacted fields adjacent to agriculture or municipal parks, and highly disturbed habitats near railroad tracks. By building an integrative map of abiotic and biotic variables, we find that a key predictor of disease was biodiversity across ecological scales. Plant communities with higher diversity were associated with reduced disease burden in A. thaliana populations but also increased diversity within the microbiome of A. thaliana. This increased microbial diversity was additionally associated with less disease in A. thaliana. However, the diversity-microbiome-disease relationships were all sensitive to season and further modulated by land use. Taken together, our work highlights the importance of anthropogenic change reshaping species interactions across ecological scales to impact disease risk in wild plant populations.

ecology↗

Rapid adaptation and extinction across climates in synchronized outdoor evolution experiments of Arabidopsis thaliana

Climate change is threatening species with extinction, and rapid evolutionary adaptation may be their only option for population rescue over short ecological timescales. However, direct observations of rapid genetic adaptation and population dynamics across climates are rare across species. To fill this gap, we conducted a replicated, globally synchronized evolution experiment with the plant Arabidopsis thaliana for 5 years in over 30 outdoor experimental gardens with distinct climates across Europe, the Levant, and North America. We performed whole-genome sequencing on [~]70,000 surviving reproductive individuals and directly observed rapid and repeatable adaptation across climates. Allele frequency changes over time were parallel in experimental evolution replicates within the same climates, while they diverged across contrasting climates--with some allele frequency shifts best explained by strong selection between -46% to +60%. Screening the genome for signals of rapid climate adaptation identified a polygenic architecture with both known and novel adaptive genetic variants connected to important ecological phenotypes including environmental stress responses, CAM5 and HEAT SHOCK FACTORs, and germination and spring flowering timing, CYTOCHROME P450s and TSF. We found evolutionary adaptation trends were often predictable, but variable across environments. In warm climates, high evolutionary predictability was associated with population survival up to 5 years, while erratic trends were an early warning for population extinction. Together, these results show rapid climate adaptation may be possible, but understanding its limits across species will be key for biodiversity forecasting.

evolutionary biology↗

Life-history trade-offs explain local adaptation in Arabidopsis thaliana

Local adaptation has been demonstrated in many organisms, but the traits involved, and the temporal and spatial scales at which selection acts are generally unknown. We carried out a multi-year study of 200 accessions (natural inbred lines) of Swedish Arabidopsis thaliana using local field sites and a combination of common-garden experiments that measured adult survival and fecundity, and selection experiments that measured fitness over the full life cycle. We found evidence of strong and variable selection, with particular genotypes favored more than five-fold in certain years and locations. Fecundity showed evidence of classical local adaptation, with accessions generally performing better closer to their home. However, relative to other accessions, southern ones usually had the highest fecundity---but were far more sensitive to harsh winters and slug herbivory, which strongly decreased both survival and fecundity. Furthermore, accessions originally sampled on beaches had low fecundity in all common-garden experiments, but massively outperformed all other accessions in the selection experiments, presumably due to an advantage during seedling establishment associated with their very large seeds. We conclude that local adaptation in A. thaliana reflects strong temporally and spatially varying selection on multiple traits, generally involving trade-offs and different life-history strategies, making fitness difficult to predict and measure.

genetics↗

Evolutionary implications of plant host interactions with a generalist pathogen

It is widely believed that eco-evolutionary feedbacks arising from host-pathogen interactions shape the number and frequency of resistance (R) genotypes and their allelic polymorphism. A subset of R genes exhibit unusually strong signatures of balancing selection, sometimes even existing as a trans-specific polymorphism. Here, we explore the role of alternative hosts on R gene evolution through a simple model of two closely related host species that share a single generalist pathogen. We ask (i) how shared interactions determine the R gene repertoires and polymorphism in each host and (ii) under which circumstances (trans-specific) polymorphism is maintained. Our results indicate that interactions with a generalist pathogen are more likely to sustain polymorphism at a shared R gene compared to the maintenance of polymorphism at R genes private to each host. The former can translate into trans-specific resistance gene polymorphism. Further, we observe that increasing the relative proportion of a single host species favors fixation of private resistance in the less common host, which stays effective because the pathogen tracks the more common host. Our model thus sheds light on how R gene dynamics are shaped by interactions with a shared generalist pathogen and the pathogens response to alternative hosts.

evolutionary biology↗

Negative frequency-dependent selection contributes to modular structure of effector repertoires in Pseudomonas syringae

The evolutionary fate of multi-strain pathogens is shaped by host-pathogen ecological interactions. In bacterial pathogens of plants, enhanced strain characterization and advances in our understanding of molecular mechanisms underlying defense pathways open the door for revisiting the role of negative frequency-dependent selection (NFDS) in strain structure, including its interplay with genetic exchange. NFDS arising from specific defense is one potential mechanism for generating, maintaining, and structuring pathogen diversity. In plants, specific protection against microbial pathogens involves Resistance proteins (R-proteins) that recognize virulence factors (effectors) secreted by pathogens, typically to subvert the initial line of host defense. Here we formulate a stochastic computational co-evolution model that explicitly incorporates variable length R-gene and effector repertoires, and migration from their regional pools. We use this model to understand potential mechanisms shaping effector repertoire structure and associated strain coexistence in the generalist plant pathogen P. syringae. The demonstration of a modular structure in our numerical simulations motivates the analysis of genome sequences from 76 strains collected in the Midwestern US and 1104 strains from global sources. We find that effector repertories both locally and globally exhibit a modular structure, with higher similarity within than between clusters. The observed modules are consistent with the core genome phylogeny and are unexplained by plant host species, location of isolation, and genetic linkage between effectors. An extension of the model is needed to take into account the evidence for genetic exchange and the phylogenetic congruence of effector modules. We initialize the system with a phylogenetically congruent modular structure and include recombination rates decreasing as a function of phylogenetic distance. We show that NFDS can counter-balance the effects of mixing due to recombination and in so doing, contributes to the maintenance of strain structure. These findings indicate that the observed similarity clusters may constitute, in part, emergent niches arising from eco-evolutionary dynamics that contribute to strain coexistence.

ecology↗

Diet outperforms microbial transplant to drive microbiome recovery post-antibiotics

High-fat, low-fiber Western-style diets (WD) induce microbiome dysbiosis characterized by reduced taxonomic diversity and metabolic breadth1,2, which in turn increases risk for a wide array of metabolic3-5, immune6 and systemic pathologies. Recent work has established that WD can impair microbiome resilience to acute perturbations like antibiotic treatment7,8, although we know little about the mechanism of impairment and the specific host consequences of prolonged post-antibiotic dysbiosis. Here, we characterize the trajectory by which the gut microbiome recovers its taxonomic and functional profile after antibiotic treatment in mice on regular chow (RC) and WD, and find that only mice on RC undergo a rapid successional process of recovery. Metabolic modeling indicates that RC diet promotes the development of syntrophic cross- feeding interactions, while on WD, a dominant taxon monopolizes readily available resources without releasing syntrophic byproducts. Intervention experiments reveal that an appropriate dietary resource environment is both necessary and sufficient for rapid and robust microbiome recovery, whereas microbial transplant is neither. Furthermore, prolonged post-antibiotic dysbiosis in mice on WD renders them susceptible to infection by the intestinal pathogen Salmonella enterica serovar Typhimurium. Our data challenge widespread enthusiasm for fecal microbiota transplant (FMT) as a strategy to address dysbiosis and demonstrate that specific dietary interventions are, at minimum, an essential prerequisite for effective FMT, and may afford a safer, more natural, and less invasive alternative to FMT.

microbiology↗

The repercussions of timing in the invasion of synthetic bacterial communities

Microbial communities regularly experience ecological invasions that can lead to changes in composition and function. Factors thought to affect the outcome of invasions, like diversity and resource use, vary over the course of community assembly, potentially altering susceptibility to arriving invaders. We used synthetic bacterial communities to evaluate the success and impact of invasions occurring at different times during the community assembly process. Fifteen distinct communities were subjected to each of three bacterial invaders at the initial assembly of the community ("initial"), 24 hours into community assembly ("early"), when the community was still undergoing transient dynamics, and 7 days into community assembly ("late"), once the community had settled into its final composition. Communities were passaged daily and characterized through sequencing after reaching a stable composition. Invasions were most successful and had their largest effect on composition when they occurred before a community had settled into a stable composition. Surprisingly, we found instances where an invader was ultimately excluded yet had profound and long-lasting effects on invaded communities. We also found that common community members were more greatly impacted by invaders than rare community members. Higher invasion success and impact were associated with lower community resource use efficiency, which varied throughout assembly. Our results demonstrate that microbial communities experiencing transient community dynamics are more prone to invasion, a finding relevant to efforts to modify the composition of microbial communities.

ecology↗

Richness and density jointly determine context dependence in bacterial interactions

Pairwise interactions are often used to predict features of complex microbial communities due to the challenge of measuring multi-species interactions in high dimensional contexts. This assumes that interactions are unaffected by community context. Here, we used synthetic bacterial communities to investigate that assumption by observing how interactions varied across contexts. Interactions were most often weakly negative and showed clear phylogenetic signal. Community richness and total density emerged as strong predictors of interaction strength and contributed to an attenuation of interactions as richness increased. Population level and per-capita measures of interactions both displayed such attenuation, suggesting factors beyond systematic changes in population size were involved; namely, changes to the interactions themselves. Nevertheless, pairwise interactions retained some predictive value across contexts, provided those contexts were not substantially diverged in richness. These results suggest that understanding the emergent properties of microbial interactions can improve our ability to predict features of microbial communities.

microbiology↗

Dynamic genetic adaptation of Bacteroides thetaiotaomicron murine gut colonization

To understand how a bacterium ultimately succeeds or fails in adapting to a new environment, it is essential to assess the temporal dynamics of its fitness over the course of colonization. The mammalian gut, into which exogenous microorganisms are regularly introduced, represents a biologically and clinically relevant system to explore microbial adaptational processes. In this study, we introduce a human-derived commensal organism, Bacteroides thetaiotaomicron, into the guts of germ-free mice to 1) determine whether the genetic requirements for colonization shift over time and, if so, 2) characterize the biological functions required for microbial survival at different points of colonization. The results of a high-throughput functional genetics assay (BarSeq), transcriptomics, and metabolomics converge on several conclusions. First, adaptation to the host gut occurs in distinct stages. We observed drastic changes in gene usage during the first week, shifting from high expression of amino acid biosynthesis to polysaccharide utilization genes. These changes were sustained thereafter, except for the continued upregulation of a single polysaccharide utilization locus responsible for the degradation of raffinose-family oligosaccharides rich in the standard chow diet fed to our mice. Spontaneous mutations in wildtype Bt also evolve around this locus, highlighting the importance of efficient carbohydrate metabolism in long-term persistence within a monoassociated gut. To improve microbiome-based therapies, it will be important to appreciate and meet the distinct needs of the organism during each stage of colonization. ImportanceMicrobes regularly disperse across and adapt to new environments and ecological niches. A clinically significant microbial niche home to trillions of microbes is the mammalian gut. Temporal processes of microbial adaptation over the course of gut colonization are poorly understood on a genetic, transcriptional, and metabolite level. In this study, we leverage a three-pronged approach to characterize gut colonization as a dynamic process with shifting genetic determinants of microbial fitness. This study sheds light on host colonization by Bacteroides thetaiotaomicron, an organism that is prevalent and dominant across healthy human microbiomes, and not only identifies key pathways involved in colonization, but determines the timing of when these pathways are most vital to colonization success. By demonstrating that the key determinants of colonization success in the gut change over time, the results of this study highlight the importance of considering ecological dynamics in developing more effective microbiome-based therapies.

microbiology↗

Genome-wide association mapping within a single Arabidopsis thaliana population reveals a richer genetic architecture for defensive metabolite diversity

A paradoxical finding from genome-wide association studies (GWAS) in plants is that variation in metabolite profiles typically maps to a small number of loci, despite the complexity of underlying biosynthetic pathways. This discrepancy may partially arise from limitations presented by geographically diverse mapping panels. Properties of metabolic pathways that impede GWAS by diluting the additive effect of a causal variant, such as allelic and genic heterogeneity and epistasis, would be expected to increase in severity with the geographic range of the mapping panel. We hypothesized that a population from a single locality would reveal an expanded set of associated loci. We tested this in a French Arabidopsis thaliana population (< 1 km transect) by profiling and conducting GWAS for glucosinolates, a suite of defensive metabolites that have been studied in depth through functional and genetic mapping approaches. For two distinct classes of glucosinolates, we discovered more associations at biosynthetic loci than previous GWAS with continental-scale mapping panels. Candidate genes underlying novel associations were supported by concordance between their observed effects in the TOU-A population and previous functional genetic and biochemical characterization. Local populations complement geographically diverse mapping panels to reveal a more complete genetic architecture for metabolic traits.

evolutionary biology↗

Species-specific gene duplication in Arabidopsis thaliana evolved novel phenotypic effects on morphological traits under strong positive selection

Gene duplication is increasingly recognized as an important mechanism for the origination of new genes, as revealed by comparative genomic analysis. However, the ways in which new duplicate genes contribute to phenotypic evolution remain largely unknown, especially in plants, owing to a lack of experimental and phenotypic data. In this study, we identified the new gene Exov, derived from a partial gene region duplication of its parental gene Exov-L, which is a member of an exonuclease family, into a different chromosome in Arabidopsis thaliana. We experimentally investigated the phenotypic effects of Exov and Exov-L in an attempt to understand how the new gene diverged from the parental copy and contributes to phenotypic evolution. Evolutionary analysis demonstrated that Exov is a species-specific gene that originated within the last 3.5 million years and shows strong signals of positive selection. Unexpectedly, RNAseq analyses reveal that the new gene, despite its young age, has acquired a large number of novel direct and indirect interactions in which the parental gene does not engage. This is consistent with a high, selection-driven substitution rate in the protein sequence encoded by Exov in contrast to the slowly evolving Exov-L, suggesting an important role for Exov in phenotypic evolution. We analyzed phenotypic effects of exov and exov-l single T-DNA-insertion mutants;double exov, exov-l T-DNA insertion mutants; and CRISPR/Cas9-mediated exovcrp and exov-lcrp knockouts on seven morphological traits in both the new and parental genes. We detected significant segregation of morphological changes for all seven traits when assessed in terms of single mutants, as well as morphological changes for seven traits associated with segregation of double exov, exov-l mutants. Substantial divergence of phenotypic effects between new and parental genes was revealed by principal component analyses, suggesting neofunctionalization in the new gene. These results reveal a young gene that plays critical roles in biological processes that underlie morphological and developmental evolution in Arabidopsis thaliana.

evolutionary biology↗

Metabolic profile discriminates and predicts Arabidopsis susceptibility to virus under field conditions

As obligatory parasites, plant viruses alter host cellular metabolism. There is a lack of information on the variability of virus-induced metabolic responses among genetically diverse plants in a natural context with daily changing conditions. To decipher the metabolic landscape of plant-virus interactions in a natural setting, one hundred and thirty-two and twenty-six accessions of Arabidopsis thaliana were inoculated with Turnip mosaic virus (TuMV), in two field experiments over 2 years. The accessions were phenotyped for viral accumulation, above-ground biomass, targeted and untargeted metabolic profiles. The accessions revealed quantitative response to the virus, from susceptibility to resistance. Susceptible accessions accumulate primary and secondary metabolites upon infection, at the cost of hindered growth. Orthogonal Partial Least Squares-Discriminant Analysis (OPLS-DA) revealed that the primary metabolites sucrose, glucose and glutamate discriminate susceptible and resistant accessions. Twenty-one metabolic signatures were found to significantly accumulate in resistant accessions whereas they maintained their growth at the same level as mock-inoculated plants without biomass penalty. Metabolic content was demonstrated to discriminate and to be highly predictive of the susceptibility of inoculated Arabidopsis. The PLS coefficient estimated in the training data set reveals, after cross-validation, a correlation of 0.61 between predicted and true viral accumulation. This study is the first to describe the metabolic landscape of plant-virus interactions in a natural setting and its predictive link to susceptibility. It reveals that, in this undomesticated species and in ecologically realistic conditions, growth and resistance are in a permanent conversation and provides new insights on plant-virus interactions.

plant biology↗

Transient interactions and influence among bacteria in field-grown Arabidopsis thaliana tissues

Interactions between bacteria are thought to play an important role in the assembly of plant microbial communities (1), yet the extent of temporal variation in these interactions is unclear. We inferred interactions from sequence-based counts of bacteria in a series of Arabidopsis thaliana tissue samples spanning major developmental transitions in the plant life cycle (2). Bacterial interactions were transient, even among variants found together at consecutive developmental stages. The overwhelming majority of these interactions were positive, indicating that competition for the plant niche might be a less important driver of bacterial abundances than cooperation or common responses to host and environmental factors. Over time, interaction networks diverged from an initial scale-free structure and became increasingly modular. In all networks, we found evidence of a hierarchical structure in which hub bacteria bridged network modules. However, the identities of bacteria in these influential roles also varied during plant growth.

ecology↗

Natural bacterial assemblages in Arabidopsis thaliana tissues become more distinguishable and diverse during host development

To study the spatial and temporal dynamics of bacterial colonization under field conditions, we planted and sampled Arabidopsis thaliana during two years at two Michigan sites and surveyed colonists by sequencing 16S rRNA gene amplicons. Mosaic and dynamic assemblages revealed the plant as a patchwork of tissue habitats that differentiated with age. Although assemblages primarily varied between roots and shoots, amplicon sequence variants (ASVs) also differentiated phyllosphere tissues. Increasing assemblage diversity indicated that variants dispersed more widely over time, decreasing the importance of stochastic variation in early colonization relative to tissue differences. As tissues underwent developmental transitions, the root and phyllosphere assemblages became more distinct. This pattern was driven by common variants rather than those restricted to a particular tissue or transiently present at one developmental stage. Patterns also depended critically on fine phylogenetic resolution: when ASVs were grouped at coarse taxonomic levels, their associations with host tissue and age weakened. Thus, the observed spatial and temporal variation in colonization depended upon bacterial traits that were not broadly shared at the family level. Some colonists were consistently more successful at entering specific tissues, as evidenced by their repeatable spatial prevalence distributions across sites and years. However, these variants did not overtake plant assemblages, which instead became more even over time. Together, these results suggested that the increasing effect of tissue type was related to colonization bottlenecks for specific ASVs rather than to their ability to dominate other colonists once established. ImportanceDeveloping synthetic microbial communities that can increase plant yield or deter pathogens requires basic research on several fronts, including the efficiency with which microbes colonize plant tissues, how plant genes shape the microbiome, and the microbe-microbe interactions involved in community assembly. Findings on each of these fronts depend upon the spatial and temporal scales at which plant microbiomes are surveyed. In our study, phyllosphere tissues housed increasingly distinct microbial assemblages as plants aged, indicating that plants can be considered as collections of tissue habitats in which microbial colonists-- natural or synthetic-- establish with differing success. Relationships between host genes and community diversity might vary depending on when samples are collected, given that assemblages grew more diverse as plants aged. Both spatial and temporal trends weakened when colonists were grouped by family, suggesting that functional rather than taxonomic profiling will be necessary to understand the basis for differences in colonization success.

ecology↗