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Gore, J.

Publications and source records attributed to Gore, J..

At least 37 records · Page 2Linked to original sources

Warmer temperatures favor slower-growing bacteria in natural marine communities

Earths life-sustaining oceans harbor diverse bacterial communities that display varying composition across time and space. While particular patterns of variation have been linked to a range of factors, unifying rules are lacking, preventing the prediction of future changes. Here, analyzing the distribution of fast- and slow-growing bacteria in ocean datasets spanning seasons, latitude, and depth, we show that higher seawater temperatures universally favor slower-growing taxa, in agreement with theoretical predictions. Our results explain why slow growers dominate at the ocean surface, during summer, and near the tropics, and provide a framework to understand how bacterial communities will change in a warmer world.

ecology↗

A taste for numbers: Caenorhabditis elegans foraging follows a low-dimensional rule of thumb

Rules of thumb are behavioral algorithms that approximate optimal behavior while lowering cognitive and sensory costs. One way to reduce these costs is by reducing dimensionality: While the theoretically optimal behavior may depend on many environmental variables, a rule of thumb may use a low-dimensional combination of variables that performs reasonably well. Experimental proof of a dimensionality reduction requires an exhaustive mapping of all relevant combinations of several environmental parameters, which we performed for Caenorhabditis elegans foraging by covering all combinations of food density (across 4 orders of magnitude) and food type (across 12 bacterial strains). We found a one-dimensional rule: Worms respond to food density measured as number of bacteria per unit surface, disregarding other factors such as biomass content or bacterial strain. We also measured fitness experimentally, determining that the rule is near-optimal and therefore constitutes a rule of thumb that leverages the most informative environmental variable.

animal behavior and cognition↗

Community interactions drive the evolution of antibiotic tolerance in bacteria

The emergence of antibiotic tolerance (prolonged survival against exposure) in natural bacterial populations is a major concern. Since it has been studied primarily in isogenic populations, we do not yet understand how ecological interactions in a diverse community impact the evolution of tolerance. To address this, we studied the evolutionary dynamics of a synthetic bacterial community composed of two interacting strains. In this community, an antibiotic-resistant strain protected the other, susceptible strain by degrading the antibiotic ampicillin in the medium. Surprisingly, we found that in the presence of antibiotics, the susceptible strain evolved tolerance. Tolerance was typified by an increase in survival as well as an accompanying decrease in growth rate, highlighting a trade-off between the two. A simple mathematical model explained that the observed decrease in death rate, even when coupled with a decreased growth rate, is beneficial in a community with weak protective interactions. In the presence of strong interactions, the model predicted that the trade-off would instead be detrimental and tolerance would not emerge, which we experimentally verified. By whole genome sequencing the evolved tolerant isolates, we identified three genetic hotspots which accumulated mutations in parallel lines, suggesting their association with tolerance. Our work highlights that ecological interactions can promote antibiotic tolerance in bacterial communities, which has remained understudied. SignificanceBacteria evolve to evade antibiotic pressure, leading to adverse infection outcomes. Understanding the evolutionary dynamics which lead to different antibiotic responses has thus far focused on single-strain bacterial populations, with limited attention to multi-strain communities which are more common in nature. Here, we experimentally evolved a simple two-strain community, comprising an antibiotic-resistant strain protecting a susceptible one, and found that susceptible populations evolve tolerance, helping them better survive long antibiotic exposure. Using the interplay between community interactions, antibiotic dynamics, and resource availability, we explain this finding with a simple mathematical model, and predict and experimentally verify that an increased resistant strain carrying capacity would render tolerance detrimental. Our results highlight that community interactions can alter bacterial evolutionary responses to antibiotics.

evolutionary biology↗

Detection of functional activity in brain white matter using fiber architecture informed synchrony mapping

A general linear model is widely used for analyzing fMRI data, in which the blood oxygenation-level dependent (BOLD) signals in gray matter (GM) evoked in response to neural stimulation are modeled by convolving the time course of the expected neural activity with a canonical hemodynamic response function (HRF) obtained a priori. The maps of brain activity produced reflect the magnitude of local BOLD responses. However, detecting BOLD signals in white matter (WM) is more challenging as the BOLD signals are weaker and the HRF is different, and may vary more across the brain. Here we propose a model-free approach to detect changes in BOLD signals in WM by measuring task-evoked increases of BOLD signal synchrony in WM fibers. The proposed approach relies on a simple assumption that, in response to a functional task, BOLD signals in relevant fibers are modulated by stimulus-evoked neural activity and thereby show greater synchrony than when measured in a resting state, even if their magnitudes do not change significantly. This approach is implemented in two technical stages. First, for each voxel a fiber-architecture-informed spatial window is created with orientation distribution functions constructed from diffusion imaging data. This provides the basis for defining neighborhoods in WM that share similar local fiber architectures. Second, a modified principal component analysis (PCA) is used to estimate the synchrony of BOLD signals in each spatial window. The proposed approach is validated using a 3T fMRI dataset from the Human Connectome Project (HCP) at a group level. The results demonstrate that neural activity can be reliably detected as increases in fMRI signal synchrony within WM fibers that are engaged in a task with high sensitivities and reproducibility.

neuroscience↗

Emergent phases of ecological diversity and dynamics mapped in microcosms

Natural ecological communities display striking features, such as high biodiversity and a wide range of dynamics, that have been difficult to explain in a unified framework. Using experimental bacterial microcosms, we perform the first direct test of recent complex systems theory predicting that simple aggregate parameters dictate emergent behaviors of the community. As either the number of species or the strength of species interactions is increased, we show that microbial ecosystems transition between distinct qualitative dynamical phases in the predicted order, from a stable equilibrium where all species coexist, to partial coexistence, to emergence of persistent fluctuations in species abundance. Under the same conditions, high biodiversity and fluctuations allow and require each other. Our results demonstrate predictable emergent diversity and dynamics in ecological communities. One-Sentence SummaryA phase diagram of ecological dynamics and diversity as a function of coarse-grained features of species interaction network.

biophysics↗

Slow expanders invade by forming dented fronts in microbial colonies

Most organisms grow in space, whether they are viruses spreading within a host tissue or invasive species colonizing a new continent. Evolution typically selects for higher expansion rates during spatial growth, but it has been suggested that slower expanders can take over under certain conditions. Here, we report an experimental observation of such population dynamics. We demonstrate that the slower mutants win not only when the two types are intermixed at the front but also when they are spatially segregated into sectors. The latter was thought to be impossible because previous studies focused exclusively on the global competitions mediated by expansion velocities but overlooked the local competitions at sector boundaries. We developed a theory of sector geometry that accounts for both local and global competitions and describes all possible sector shapes. In particular, the theory predicted that a slower, but more competitive, mutant forms a dented V-shaped sector as it takes over the expansion front. Such sectors were indeed observed experimentally and their shapes matched up quantitatively with the theory. In simulations, we further explored several mechanism that could provide slow expanders with a local competitive advantage and showed that they are all well-described by our theory. Taken together, our results shed light on previously unexplored outcomes of spatial competition and establish a universal framework to understand evolutionary and ecological dynamics in expanding populations. SignificanceLiving organisms never cease to evolve, so there is a significant interest in predicting and controlling evolution in all branches of life sciences from medicine to agriculture. The most basic question is whether a trait should increase or decrease in a given environment. The answer seems to be trivial for traits such as the growth rate in a bioreactor or the expansion rate of a tumor. Yet, it has been suggested that such traits can decrease rather than increase during evolution. Here, we report a mutant that outcompeted the ancestor despite having a slower expansion velocity. To explain this observation, we developed and validated a theory that describes spatial competition between organisms with different expansion rates and arbitrary competitive interactions.

evolutionary biology↗

Diauxic lags explain unexpected coexistence in multi-resource environments

How the coexistence of species is affected by the presence of multiple resources is a major question in microbial ecology. We experimentally demonstrate that differences in diauxic lags, which occur as species deplete their own environments and adapt their metabolisms, allow slow-growing microbes to stably coexist with faster-growing species in multi-resource environments despite being excluded in single-resource environments. In our focal example, an Acinetobacter species (Aci2) competitively excludes Pseudomonas aurantiaca (Pa) on alanine and on glutamate. However, they coexist on the combination of both resources. Experiments reveal that Aci2 grows faster but Pa has shorter diauxic lags. We establish a tradeoff between Aci2s fast growth and Pas short lags as their mechanism for coexistence. We model this tradeoff to accurately predict how environmental changes affect community composition. We extend our work by surveying a large set of competitions and observe coexistence nearly three times as frequently when the slow-grower is the fast-switcher. Our work illustrates a potentially common mechanism for the emergence of multi-resource coexistence despite single-resource competitive exclusions.

ecology↗

A simple linear relationship between resource availability and microbial community diversity

The relationship between the number of available nutrients and community diversity is a central question for ecological research that remains unanswered. Here, we studied the assembly of hundreds of soil-derived microbial communities on a wide range of well-defined resource environments, from single carbon sources to combinations of up to 16. We found that, while single resources supported multispecies communities varying from 8 to 40 taxa, mean community richness increased only one-by-one with additional resources. Cross-feeding could reconcile these seemingly contrasting observations, with the metabolic network seeded by the supplied resources explaining the changes in richness due to both the identity and the number of resources, as well as the distribution of taxa across different communities. By using a consumer-resource model incorporating the inferred cross-feeding network, we provide further theoretical support to our observations and a framework to link the type and number of environmental resources to microbial community diversity.

ecology↗

Horizontal gene transfer becomes disadvantageous in rapidly fluctuating environments

Horizontal gene transfer (HGT) allows organisms to share genetic material with non-offspring, and is typically considered beneficial for evolving populations. Recent unexplained observations suggest that HGT rates in nature are linked with environmental dynamics, being high in static environments but surprisingly low in fluctuating environments. Here, using a geometric model of adaptation, we show that this trend might arise from evolutionary constraints. During adaptation in our model, a population of phenotype vectors aligns with a potentially fluctuating environmental vector while experiencing mutation, selection, drift and HGT. Simulations and theory reveal that HGT shapes a trade-off between the adaptation speed of populations and their fitness. This trade-off gives rise to an optimal HGT rate which decreases sharply with the rate of environmental fluctuations. Our results are consistent with data from natural populations, and strikingly suggest that HGT may sometimes carry a significant disadvantage for populations.

evolutionary biology↗

Environmental fluctuations reshape an unexpected diversity-disturbance relationship in a microbial community

Environmental disturbances have long been theorized to play a significant role in shaping the diversity and composition of ecosystems1,2. However, fundamental limitations in our ability to specify the characteristics of a disturbance in the field and laboratory have produced an inconsistent picture of diversity-disturbance relationships (DDRs) that shape the structure of ecosystems3. Here, using a recently developed continuous culture system with tunable environmental control4, we decomposed a dilution disturbance into intensity and fluctuation components5,6, and tested their effects on the diversity of a soil-derived bacterial community across hundreds of replicate cultures. We observed an unexpected U-shaped relationship between community diversity and disturbance intensity in the absence of fluctuations, an observation counter to classical intuition. Adding fluctuations erased the U-shape and increased community diversity across all disturbance intensities. All of these results are well-captured by a Monod consumer resource model, which further reveals how U-shaped DDRs emerge based on a novel "niche flip" mechanism in which competitive outcomes flip and coexistence regimes subsequently collapse at intermediate disturbance levels. Broadly, our results demonstrate how distinct features of an environmental disturbance can interact in complex ways to govern ecosystem assembly and produce all the major classes of DDRs, without invoking other organizational principles. With these findings, we construct a unifying framework that reconciles the disparate DDRs observed in nature, and propose strategies for predictively reshaping the compositional complexity of microbiomes and other ecosystems.

bioengineering↗

Positive interactions are common among culturable bacteria

Interspecies interactions shape the structure and function of microbial communities. In particular, positive, growth-promoting interactions can significantly affect the diversity and productivity of natural and engineered communities. However, the prevalence of positive interactions and the conditions in which they occur are not well understood. To address this knowledge gap, we used kChip, an ultra-high throughput coculture platform, to measure 180,408 interactions among 20 soil bacteria across 40 carbon environments. We find that positive interactions, often described to be rare, occur commonly, primarily as parasitisms between strains that differ in their carbon consumption profiles. Notably, non-growing strains are almost always promoted by strongly growing strains (85%), suggesting a simple positive interaction-mediated approach for cultivation, microbiome engineering, and microbial consortium design. One Sentence SummaryExperimental measurement of >150,000 bacterial cocultures reveals that growth-promoting interactions occur commonly and depend on differences in nutrient consumption preferences.

ecology↗

Inversion of pheromone preference optimizes foraging in C. elegans

Foraging animals have to locate food sources that are usually patchily distributed and subject to competition. Deciding when to leave a food patch is challenging and requires the animal to integrate information about food availability with cues signaling the presence of other individuals (e.g. pheromones). To study how social information transmitted via pheromones can aid foraging decisions, we investigated the behavioral responses of the model nematode Caenorhabditis elegans to food depletion and pheromone accumulation in food patches. We experimentally show that animals consuming a food patch leave it at different times and that the leaving time affects the animal preference for its pheromones. In particular, worms leaving early are attracted to their pheromones, while worms leaving later are repelled by them. We further demonstrate that the inversion from attraction to repulsion depends on associative learning and, by implementing a simple model, we highlight that it is an adaptive solution to optimize food intake during foraging.

ecology↗

Colonization with heterologous bacteria reprograms a Caenorhabditis elegans nutritional phenotype

Animals rely on the gut microbiome to process complex food compounds that the host cannot digest and to synthesize nutrients that the host cannot produce. New systems are needed to study how the expanded metabolic capacity provided by the gut microbiome impacts the nutritional status and health of the host. Here we colonized the nematode Caenorhabditis elegans gut with cellulolytic bacteria that enabled C. elegans to utilize cellulose, an otherwise indigestible substrate, as a carbon source. The nutritional benefits of colonization with cellulolytic bacteria were assayed directly, by incorporation of isotopic biomass, and indirectly, as host larval yield resulting from glucose release in the gut. As a community component in the worm gut, cellulolytic bacteria can also support additional bacterial species with specialized roles, which we demonstrate by using Lactobacillus to protect against Salmonella infection. As a model system, C. elegans colonized with cellulolytic bacteria can be used to study microbiome-host interactions. Engineered microbiome communities may provide host organisms with novel functions, such as the ability to use more complex nutrient sources and to fight against pathogen infections. One Sentence SummaryHeterologous bacteria colonizing an animal gut help digest complex sugars to provide nutrition for the host in a model system.

microbiology↗

Higher Temperatures Generically Favor Slower-Growing Bacterial Species in Multispecies Communities

Temperature is among the cardinal environmental variables which determine the composition and function of microbial communities. Many culture-independent studies have characterized communities that are affected by changing temperatures, either due to seasonal cycles1-3, long-term warming4-6, or latitudinal/elevational gradients7-8. However, a predictive understanding of how microbial communities respond to such changes in temperature is still lacking, partly because it is not obvious which aspects of microbial physiology determine whether a species should benefit from temperature alteration. Here, we incorporate how microbial growth rates change with temperature to a modified Lotka-Volterra competition model9, and predict that higher temperatures should generically favor slower-growing species in a bacterial community. We experimentally confirm this prediction in pairwise cocultures assembled from a diverse set of species, and we show that these changes to pairwise outcomes with temperature are also predictive of changing outcomes in three-species communities, suggesting our theory may propagate to more complex assemblages. Our results demonstrate that it is possible to predict how bacterial communities will shift with temperature knowing only the growth rates of the community members. These results provide a testable hypothesis for future studies of more complex, natural communities, and we hope that this work will help bridge the gap between ecological theory and the complex dynamics observed in metagenomic surveys.

ecology↗

Emergence of alternative stable states in microbial communities in a fluctuating environment

The effect of environmental fluctuations is a major question in ecology. While it is widely accepted that fluctuations and other types of disturbances can increase biodiversity, we have only a limited understanding of the circumstances in which other types of outcomes can occur in a fluctuating environment. Here we explore this question with laboratory microcosms, using cocultures of two bacterial species, P. putida and P. veronii. At low dilution rates we observe competitive exclusion of P. veronii, whereas at high dilution rates we observe competitive exclusion of P. putida. When the dilution rate alternates between high and low, we do not observe coexistence between the species, but rather alternative stable states, in which only one species survives and initial species fractions determine the identity of the surviving species. The Lotka-Volterra model with a fluctuating mortality rate predicts that this outcome is independent of the timing of the fluctuations, and that the time-averaged mortality would also lead to alternative stable states, a prediction that we confirm experimentally. Other pairs of species can coexist in a fluctuating environment, and again consistent with the model we observe coexistence in the time-averaged dilution rate. We find a similar time-averaging result holds in a three-species community, highlighting that simple linear models can in some cases provide powerful insight into how communities will respond to environmental fluctuations.

ecology↗

Strength of species interactions determines biodiversity and stability in microbial communities

Organisms - especially microbes - tend to live in complex communities. While some of these ecosystems are very bio-diverse, others arent1-3, and while some are very stable over time others undergo strong temporal fluctuations4,5. Despite a long history of research and a plethora of data it is not fully understood what sets biodiversity and stability of ecosystems6,7. Theory as well as experiments suggest a connection between species interaction, biodiversity, and stability of ecosystems8-13, where an increase of ecosystem stability with biodiversity could be observed in several cases7,9,14. However, what causes these connections remains unclear. Here we show in microbial ecosystems in the lab that the concentrations of available nutrients can set the strength of interactions between bacteria. At high nutrient concentrations, extensive microbial growth leads to strong chemical modifications of the environment, causing more negative interactions between species. These stronger interactions exclude more species from the community - resulting in a loss of biodiversity. At the same time, these stronger interactions also decrease the stability of the microbial communities, providing a mechanistic link between species interaction, biodiversity and stability.

ecology↗

Cooperation mitigates diversity loss in a spatially expanding microbial population

The evolution and potentially even the survival of a spatially expanding population depends on its genetic diversity, which can decrease rapidly due to a serial founder effect. The strength of the founder effect is predicted to depend strongly on the details of the growth dynamics. Here, we probe this dependence experimentally using a single microbial species, Saccharomyces cerevisiae, expanding in multiple environments that induce varying levels of cooperativity during growth. We observe a drastic reduction in diversity during expansions when yeast grows non-cooperatively on simple sugars, but almost no loss of diversity when cooperation is required to digest complex metabolites. These results are consistent with theoretical expectations. When cells grow independently from each other, the expansion proceeds as a pulled wave driven by the growth at the low-density tip of the expansion front. Such populations lose diversity rapidly because of the strong genetic drift at the expansion edge. In contrast, diversity loss is substantially reduced in pushed waves that arise due to cooperative growth. In such expansions, the low-density tip of the front grows much more slowly and is often reseeded from the genetically diverse population core. Additionally, in both pulled and pushed expansions, we observe a few instances of abrupt changes in allele fractions due to rare fluctuations of the expansion front and show how to distinguish such rapid genetic drift from selective sweeps.\n\nSignificance statementSpatially expanding populations lose genetic diversity rapidly because of the repeated bottlenecks formed at the front as a result of the serial founder effect. However, the rate of diversity loss depends on the specifics of the expanding population, such as its growth and dispersal dynamics. We have previously demonstrated that changing the amount of within-species cooperation leads to a qualitative transition in the nature of expansion from pulled (driven by migration at the low density tip) to pushed (driven by migration from the high density region at the front, but behind the tip). Here we demonstrate experimentally that pushed waves, which emerge in the presence of sufficiently strong cooperation, result in strongly reduced genetic drift during range expansions, thus preserving genetic diversity in the newly colonized region.

ecology↗

Transient invaders can induce shifts between alternative stable states of microbial communities

Microbial dispersal often leads to the arrival of outsider organisms into ecosystems. When their arrival give rise to successful invasions, outsider species establish within the resident community, which can dramatically alter the ecosystem. Seemingly less influential, the potential impact of unsuccessful invaders that interact only transiently with the community has remained largely ignored. Here, we experimentally demonstrate that such transient invasions can perturb the stability of microbial ecosystems and induce a lasting transition to an alternative stable state, even when the invader species itself does not survive the transition. First, we develop a mechanistic understanding of how environmental changes caused by such transient invaders can drive a community shift in a simple, bistable model system. Beyond this, we show that transient invaders can also induce switches between stable states in more complex communities isolated from natural soil samples. Our results demonstrate that short-term interactions with an invader species can induce lasting shifts in community composition and function.\n\nOne Sentence SummaryTransient invaders can cause lasting shifts in community composition and function.

ecology↗