Biology subjects

Emonet, T.

Publications and source records attributed to Emonet, T..

At least 19 recordsLinked to original sources

bioRxiv2026

A neural circuit for olfactory motion detection

Movement is a defining feature of dynamic environments and a key variable encoded by sensory systems. In vision, neural mechanisms that extract motion direction have been studied extensively across species, revealing circuits that compare signals across space and time. Odor plumes likewise carry motion information in their spatiotemporal structure, which walking fruit flies detect and exploit to improve navigation (Brudner et al., 2025; Kadakia et al., 2022), independent of wind sensing. However, how olfactory circuits compute odor motion remains unknown. Here we identify circuitry in the Drosophila antennal lobe that transforms bilateral odor inputs into direction-selective signals that are propagated to higher brain regions. These direction-selective signals were widespread across most measured olfactory channels, spanning pheromones, food odors, and aversive cues. Directional responses were elicited by odor traces with naturalistic temporal statistics and tuned to inter-antennal delays of {approx}40 ms. Connectomic, physiological, and behav-ioral analyses identified one GABAergic inhibitory neuron in the antennal lobe as a key mediator of direction selectivity. Measurements of dynamics in direction-selective neurons revealed ipsilateral excitation and delayed contralateral inhibition. In a minimal data-driven model, this mechanism was sufficient to generate the observed direction-selective responses. These results establish motion detection as a circuit-level olfactory computation and reveal how an early sensory circuit transforms spatiotemporal chemical signals into a neural representation of odor motion to guide navigation.

neuroscience↗

bioRxiv2026

Growth-dependent sensory bet-hedging enhances collective navigation

Phenotypic heterogeneity in microbes can be a double-edged sword -- boosting individual survival in uncertain environments, but potentially compromising beneficial population coordination. Dissecting how microbes resolve this tradeoff is challenging because interactions span multiple scales--from molecular interactions to single-cell behavior, population dynamics, and environmental feedback. Here, we address this question for the Escherichia coli chemotaxis system, which implements both individual motile explorations and collective resource exploitations using the same cellular machinery. We quantify the heterogeneity of individual sensory and behavioral phenotypes, as well as the abundance of key signaling proteins during growth in various environments, and test their impact on population-scale collective migration. We identify growth rate as a key environment-dependent physiological variable governing not only the mean but also the variance of sensory phenotypes. Remarkably, rather than hindering population coordination, we find that sensory diversity benefits collective chemotactic navigation in uncertain environments. Strong heterogeneity of expressed phenotypes enhances readiness to multiple sensory cues, and the required population coordination is achieved by phenotypic filtering of that diversity by the collective behavior itself. These results reveal a sensory bet-hedging strategy for collective navigation during population growth: diversity in sensitivity to nutrients currently being consumed is reduced to promote focused exploitation, while it is increased for nutrients not yet encountered to enhance exploration for new growth opportunities.

biophysics↗

bioRxiv2025

Evolutionary consequences of bacterial resistance to a flagellotropic phage

Bacteria can evolve resistance to bacteriophage attack via mutations that alter phage receptors on the cell surface. Flagellotropic phages bind to motility-enabling flagella, creating an evolutionary trade-off, since losing flagellar function reduces fitness in many environments. We experimentally evolved Escherichia coli populations under selection by flagellotropic phage (chi), on soft-agar swim plates which favor motility. Whole genome sequencing revealed early emergence of non-motile mutants with disrupted motility-genes, followed by motile mutants with flagellin gene mutations. Swim-plate assays and single-cell tracking showed variable motility effects among resistant mutants, with some faster and others slower than ancestors. Increased tumble bias suggested altered flagellar rotation. Kinase-response in the upstream chemotaxis pathway was also remodeled in -resistant mutants. Our findings demonstrate that evolved phage-resistance can cause motility to trade-off or trade-up, revealing diverse evolutionary outcomes under combined selection pressures. TeaserEvolution redesigns bacterial swimming and navigation to escape viruses while maintaining motility in complex environments.

evolutionary biology↗

bioRxiv2025

Fly navigational responses to odor motion and gradient cues are tuned to plume statistics

Odor cues guide animals to food and mates. Different environmental conditions can create differently patterned odor plumes, making navigation more challenging. Prior work has shown that animals turn upwind when they detect odor and cast crosswind when they lose it. Animals with bilateral olfactory sensors can also detect directional odor cues, such as odor gradient and odor motion. It remains unknown how animals use these two directional odor cues to guide crosswind navigation in odor plumes with distinct statistics. Here, we investigate this problem theoretically and experimentally. We show that these directional odor cues provide complementary information for navigation in different plume environments. We numerically analyzed real plumes to show that odor gradient cues are more informative about crosswind directions in relatively smooth odor plumes, while odor motion cues are more informative in turbulent or complex plumes. Neural networks trained to optimize crosswind turning converge to distinctive network structures that are tuned to odor gradient cues in smooth plumes and to odor motion cues in complex plumes. These trained networks improve the performance of artificial agents navigating plume environments that match the training environment. By recording Drosophila fruit flies as they navigated different odor plume environments, we verified that flies show the same correspondence between informative cues and plume types. Fly turning in the crosswind direction is correlated with odor gradients in smooth plumes and with odor motion in complex plumes. Overall, these results demonstrate that these directional odor cues are complementary across environments, and that animals exploit this relationship. SignificanceMany animals use smell to find food and mates, often navigating complex odor plumes shaped by environmental conditions. While upwind movement upon odor detection is well established, less is known about how animals steer crosswind to stay in the plume. We show that directional odor cues--gradients and motion--guide crosswind navigation differently depending on plume structure. Gradients carry more information in smooth plumes, while motion dominates in turbulent ones. Neural network trained to optimize crosswind navigation reflect this distinction, developing gradient sensitivity in smooth environments and motion sensitivity in complex ones. Experimentally, fruit flies adjust their turning behavior to prioritize the most informative cue in each context. These findings likely generalize to other animals navigating similarly structured odor plumes.

animal behavior and cognition↗

bioRxiv2024

Microscopic Phage Adsorption Assay: High-throughput quantification of virus particle attachment to host bacterial cells

Phages, viruses of bacteria, play a pivotal role in Earths biosphere and hold great promise as therapeutic and diagnostic tools in combating infectious diseases. Attachment of phages to bacterial cells is a crucial initial step of the interaction. The classic assay to quantify the dynamics of phage attachment involves co-culturing and enumeration of bacteria and phages, which is laborious, lengthy, hence low-throughput, and only provides ensemble estimates of model-based adsorption rate constants. Here, we utilized fluorescence microscopy and particle tracking to obtain trajectories of individual virus particles interacting with cells. The trajectory durations quantified the heterogeneity in dwell time, the time that each phage spends interacting with a bacterium. The average dwell time strongly correlated with the classically-measured adsorption rate constant. We successfully applied this technique to quantify host-attachment dynamics of several phages including those targeting key bacterial pathogens. This approach should benefit the field of phage biology by providing highly quantitative, model-free readouts at single-virus resolution, helping to uncover single-virus phenomena missed by traditional measurements. Owing to significant reduction in manual effort, our method should enable rapid, high-throughput screening of a phage library against a target bacterial strain for applications such as therapy or diagnosis.

microbiology↗

bioRxiv2024

E. coli do not count single molecules

Organisms use specialized sensors to measure their environments, but the fundamental principles that determine their accuracy remain largely unknown. In Escherichia coli chemotaxis, we previously found that gradient-climbing speed is bounded by the amount of information that cells acquire from their environment, and that E. coli operate near this bound. However, it remains unclear what prevents them from acquiring more information. Past work argued that E. colis chemosensing is limited by the physics of molecules stochastically arriving at cells receptors, without direct evidence. Here, we show instead that E. coli are far from this physical limit. To show this, we develop a theoretical approach that uses information rates to quantify how accurately behaviorally-relevant signals can be estimated from available observations: molecule arrivals for the physical limit; chemotaxis signaling activity for E. coli. Measuring these information rates in single-cell experiments across multiple background concentrations, we find that E. coli encode two orders of magnitude less information than the physical limit. Thus, E. coli chemosensing is limited by internal noise in signal processing rather than the physics of molecule diffusion, motivating investigation of what specific physical and biological constraints shaped the evolution of this prototypical sensory system.

biophysics↗

bioRxiv2024

Lattice ultrasensitivity produces large gain in E. coli chemosensing

The E. coli chemosensory lattice, consisting of receptors, kinases, and adaptor proteins, is an important test case for biochemical signal processing. Kinase output is characterized by precise adaptation to a wide range of background ligand levels and large gain in response to small relative changes in concentration. Existing models of this lattice achieve their gain through allosteric interactions between either receptors or core units of receptors and kinases. Here we introduce a model which operates through an entirely different mechanism in which receptors gate inherently far from equilibrium enzymatic reactions between neighboring kinases. Our lattice model achieves gain through a mechanism more closely related to zero-order ultrasensitivity than to allostery. Thus, we call it lattice ultrasensitivity (LU). Unlike other lattice critical models, the LU model can achieve arbitrarily high gain through time-scale separation, rather than through finetuning. The model also captures qualitative experimental results which are difficult to reconcile with existing models. We discuss possible implementations in the lattices baseplate where long flexible linkers could potentially mediate interactions between neighboring core units.

biophysics↗

bioRxiv2024

Bifurcation enhances temporal information encoding in the olfactory periphery

Living systems continually respond to signals from the surrounding environment. Survival requires that their responses adapt quickly and robustly to the changes in the environment. One particularly challenging example is olfactory navigation in turbulent plumes, where animals experience highly intermittent odor signals while odor concentration varies over many length- and timescales. Here, we show theoretically that Drosophila olfactory receptor neurons (ORNs) can exploit proximity to a bifurcation point of their firing dynamics to reliably extract information about the timing and intensity of fluctuations in the odor signal, which have been shown to be critical for odor-guided navigation. Close to the bifurcation, the system is intrinsically invariant to signal variance, and information about the timing, duration, and intensity of odor fluctuations is transferred efficiently. Importantly, we find that proximity to the bifurcation is maintained by mean adaptation alone and therefore does not require any additional feedback mechanism or fine-tuning. Using a biophysical model with calcium-based feedback, we demonstrate that this mechanism can explain the measured adaptation characteristics of Drosophila ORNs.

neuroscience↗

bioRxiv2024

Non-genetic adaptation by collective migration

Cell populations must adjust their phenotypic composition to adapt to changing environments. One adaptation strategy is to maintain distinct phenotypic subsets within the population and to modulate their relative abundances via gene regulation. Another strategy involves genetic mutations, which can be augmented by stress-response pathways. Here, we studied how a migrating bacterial population regulates its phenotypic distribution to traverse diverse environments. We generated isogenic Escherichia coli populations with varying distributions of swimming behaviors and observed their phenotype distributions during migration in liquid and porous environments. We found that the migrating populations became enriched with high-performing swimming phenotypes in each environment, allowing the populations to adapt without requiring mutations or gene regulation. This adaptation is dynamic and rapid, reversing in a few doubling times when migration ceases. By measuring the chemoreceptor abundance distributions during migration towards different attractants, we demonstrated that adaptation acts on multiple chemotaxis-related traits simultaneously. These measurements are consistent with a general mechanism in which adaptation results from a balance between cell growth generating diversity and collective migration eliminating under-performing phenotypes. Thus, collective migration enables cell populations with continuous, multi-dimensional phenotypes to flexibly and rapidly adapt their phenotypic composition to diverse environmental conditions. Significance statementConventional cell adaptation mechanisms, like gene regulation and stochastic phenotypic switching, act swiftly but are limited to a few traits, while mutation-driven adaptations unfold slowly. By quantifying phenotypic diversity during bacterial collective migration, we discovered an adaptation mechanism that rapidly and reversibly adjusts multiple traits simultaneously. By balancing the generation of diversity through growth with the loss of phenotypes unable to keep up, this process tunes the phenotypic composition of migrating populations to the environments they traverse, without gene regulation or mutations. Given the prevalence of collective migration in microbes, cancers, and embryonic development, non-genetic adaptation through collective migration may be a universal mechanism for populations to navigate diverse environments, offering insights into broader applications across various fields.

systems biology↗

bioRxiv2023

Direct measurement of dynamic attractant gradients reveals breakdown of the Patlak-Keller-Segel chemotaxis model

Chemotactic bacteria not only navigate chemical gradients, but also shape their environments by consuming and secreting attractants. Investigating how these processes influence the dynamics of bacterial populations has been challenging because of a lack of experimental methods for measuring spatial profiles of chemoattractants in real time. Here, we use a fluorescent sensor for aspartate to directly measure bacterially generated chemoattractant gradients during collective migration. Our measurements show that the standard Patlak-Keller-Segel model for collective chemotactic bacterial migration breaks down at high cell densities. To address this, we propose modifications to the model that consider the impact of cell density on bacterial chemotaxis and attractant consumption. With these changes, the model explains our experimental data across all cell densities, offering new insight into chemotactic dynamics. Our findings highlight the significance of considering cell density effects on bacterial behavior, and the potential for fluorescent metabolite sensors to shed light on the complex emergent dynamics of bacterial communities. SIGNIFICANCE STATEMENTDuring collective cellular processes, cells often dynamically shape and respond to their chemical environments. Our understanding of these processes is limited by the ability to measure these chemical profiles in real time. For example, the Patlak-Keller-Segel model has widely been used to describe collective chemotaxis towards self-generated gradients in various systems, albeit without direct verification. Here we used a biocompatible fluorescent protein sensor to directly observe attractant gradients created and chased by collectively-migrating bacteria. Doing so uncovered limitations of the standard chemotaxis model at high cell densities and allowed us to establish an improved model. Our work demonstrates the potential for fluorescent protein sensors to measure the spatiotemporal dynamics of chemical environments in cellular communities.

biophysics↗

bioRxiv2023

Sensory diversity and precise adaptation enable independent bet-hedging strategies for multiple signals at the same time

In uncertain environments, phenotypic diversity can be advantageous for survival. However, as the environmental uncertainty decreases, the relative advantage of having diverse phenotypes decreases. Here, we show how populations of E. coli integrate multiple chemical signals to adjust sensory diversity in response to changes in the prevalence of each ligand in the environment. Measuring kinase activity in single cells, we quantified the sensitivity distribution to various chemoattractants in different mixtures of background stimuli. We found that when ligands bind uncompetitively, the population tunes sensory diversity to each signal independently, decreasing diversity when the signal ambient concentration increases. However, amongst competitive ligands the population can only decrease sensory diversity one ligand at a time. Mathematical modeling suggests that sensory diversity tuning benefits E. coli populations by modulating how many cells are committed to tracking each signal proportionally as their prevalence changes.

systems biology↗

bioRxiv2022

Novelty detection and multiple timescale integration drive Drosophila orientation dynamics in temporally diverse olfactory environments

To survive, insects must effectively navigate odors plumes to their source. In natural plumes, turbulent winds break up smooth odor regions into disconnected patches, so navigators encounter brief bursts of odor interrupted by bouts of clean air. The timing of these encounters plays a critical role in navigation, determining the direction, rate, and magnitude of insects orientation and speed dynamics. Still, disambiguating the specific role of odor timing from other cues, such as spatial structure, is challenging due to natural correlations between plumes temporal and spatial features. Here, we use optogenetics to isolate temporal features of odor signals, examining how the frequency and duration of odor encounters shape the navigational decisions of freely-walking Drosophila. We find that fly angular velocity depends on signal frequency and intermittency - fraction of time signal can be detected - but not directly on durations. Rather than switching strategies when signal statistics change, flies smoothly transition between signal regimes, by combining an odor offset response with a frequency-dependent novelty-like response. In the latter, flies are more likely to turn in response to each odor hit only when the hits are sparse. Finally, the upwind bias of individual turns relies on a filtering scheme with two distinct timescales, allowing rapid and sustained responses in a variety of signal statistics. A quantitative model incorporating these ingredients recapitulates fly orientation dynamics across a wide range of environments.

animal behavior and cognition↗

bioRxiv2022

Optimal inference of molecular interactions in live FRET imaging

Intensity-based live-cell fluorescence resonance energy transfer (FRET) imaging converts otherwise unobservable molecular interactions inside cells into fluorescence time-series signals. However, inferring the degree of molecular interactions from these observables is challenging, due to experimental complications such as spectral crosstalk, photobleaching, and measurement noise. Conventional methods solve this inverse problem through algebraic manipulations of the observables, but such manipulations inevitably accumulate measurement noise, limiting the scope of FRET analysis. Here, we introduce a Bayesian inference framework, B-FRET, which estimates molecular interactions from FRET data in a statistically optimal manner. B-FRET requires no additional measurements beyond those routinely conducted in standard 3-cube FRET imaging methods, and yet, by using the information contained in the data more efficiently, dramatically improves the signal-to-noise ratio (SNR). We validate B-FRET using simulated data, and then apply it to FRET data measured from single bacterial cells, a system with notoriously low SNR, to reveal signaling dynamics that are otherwise hidden in noise.

biophysics↗

bioRxiv2021

Odor motion sensing enables complex plume navigation

Studies dating back a century (Flugge, 1934) have stressed the critical role of the wind as the primary directional cue in odor plume navigation. Here, we show that Drosophila shape their navigational decisions using a second directional cue - the direction of motion of odors - which they detect from the temporal correlations of the odor signal between their two antennae. Using a high-resolution virtual reality paradigm to deliver spatiotemporally complex fictive odors to freely-walking flies, we demonstrate that such odor direction sensing is computationally equivalent to motion detection algorithms underlying motion detection in vision. Simulations and theoretical analysis of turbulent plumes reveal that odor motion contains valuable directional information absent from the airflow; indeed, this information is used by both Drosophila and virtual agents to navigate naturalistic odor environments. The generality of our findings suggests that odor direction sensing is likely used throughout the animal kingdom, and could significantly improve olfactory robot navigation in harsh chemical environments.

neuroscience↗

bioRxiv2021

A mechanism for migrating bacterial populations to non-genetically adapt to new environments

Populations of chemotactic bacteria can rapidly expand into new territory by consuming and chasing an attractant cue in the environment, increasing the populations overall growth in nutrient-rich environments. Although the migrating fronts driving this expansion contain cells of multiple swimming phenotypes, the consequences of non-genetic diversity for population expansion are unknown. Here, through theory and simulations, we predict that expanding populations non-genetically adapt their phenotype composition to migrate effectively through multiple physical environments. Swimming phenotypes in the migrating front are spatially sorted by chemotactic performance, but the mapping from phenotype to performance depends on the environment. Therefore, phenotypes that perform poorly localize to the back of the group, causing them to selectively fall behind. Over cell divisions, the group composition dynamically enriches for high-performers, enhancing migration speed and overall growth. Furthermore, non-genetic inheritance controls a trade-off between large composition shifts and slow responsiveness to new environments, enabling a diverse population to out-perform a non-diverse one in varying environments. These results demonstrate that phenotypic diversity and collective behavior can synergize to produce emergent functionalities. Non-genetic inheritance may generically enable bacterial populations to transiently adapt to new situations without mutations, emphasizing that genotype-to-phenotype mappings are dynamic and context-dependent.

cell biology↗

bioRxiv2021

Navigating a diversity of turbulent plumes is enhanced by sensing complementary temporal features of odor signals

We and others have shown that during odor plume navigation, walking Drosophila melanogaster bias their motion upwind in response to both the frequency of their encounters with the odor (Demir et al., 2020), and the intermittency of the odor signal, i.e. the fraction of time the signal is above a detection threshold (Alvarez-Salvado et al., 2018). Here we combine and simplify previous mathematical models that recapitulated these data to investigate the benefits of sensing both of these temporal features, and how these benefits depend on the spatiotemporal statistics of the odor plume. Through agent-based simulations, we find that navigators that only use frequency or intermittency perform well in some environments - achieving maximal performance when gains are near those inferred from experiment - but fail in others. Robust performance across diverse environments requires both temporal modalities. However, we also find a steep tradeoff when using both sensors simultaneously, suggesting a strong benefit to modulating how much each sensor is weighted, rather than using both in a fixed combination across plumes.

neuroscience↗

bioRxiv2021

E. coli chemotaxis is information-limited

Organisms must acquire and use environmental information to guide their behaviors. However, it is unclear whether and how information quantitatively limits behavioral performance. Here, we relate information to behavioral performance in Escherichia coli chemotaxis. First, we derive a theoretical limit for the maximum achievable gradient-climbing speed given a cells information acquisition rate. Next, we measure cells gradient-climbing speeds and the rate of information acquisition by the chemotaxis pathway. We find that E. coli make behavioral decisions with much less than the 1 bit required to determine whether they are swimming up-gradient. However, they use this information efficiently, performing near the theoretical limit. Thus, information can limit organisms performance, and sensory-motor pathways may have evolved to efficiently use information from the environment.

biophysics↗

bioRxiv2020

Walking Drosophila navigate complex plumes using stochastic decisions biased by the timing of odor encounters

Insects find food, mates, and egg-laying sites by tracking odor plumes swept by complex wind patterns. Previous studies have shown that moths and flies localize plumes by surging upwind at odor onset and turning cross- or downwind at odor offset. Less clear is how, once within the expanding cone of the odor plume, insects use their brief encounters with individual odor packets, whose location and timing are random, to progress towards the source. Experiments and theory have suggested that the timing of odor encounters might assist navigation, but connecting behaviors to individual encounters has been challenging. Here, we imaged complex odor plumes simultaneous with freely-walking flies, allowing us to quantify how behavior is shaped by individual odor encounters. Combining measurements, dynamical models, and statistical inference, we found that within the plume cone, individual encounters did not trigger reflexive surging, casting, or counterturning. Instead, flies turned stochastically with stereotyped saccades, whose direction was biased upwind by the timing of prior odor encounters, while the magnitude and rate of saccades remained constant. Odor encounters did not strongly affect walking speed. Instead, flies used encounter timing to modulate the rate of transitions between walks and stops. When stopped, flies initiated walks using information from multiple odor encounters, suggesting that integrating evidence without losing position was part of the strategy. These results indicate that once within the complex odor plume, where odor location and timing are unpredictable, animals navigate with biased random walks shaped by the entire sequence of encounters.

neuroscience↗