Accuracy of direct gradient sensing by single cells

Abstract

Many types of cells are able to accurately sense shallow gradients of chemicals across their diameters, allowing the cells to move towards or away from chemical sources. This chemotactic ability relies on the remarkable capacity of cells to infer gradients from particles randomly arriving at cell-surface receptors by diffusion. Whereas the physical limits of concentration sensing by cells have been explored, there is no theory for the physical limits of gradient sensing. Here, we derive such a theory, using as models a perfectly absorbing sphere and a perfectly monitoring sphere, which, respectively, infer gradients from the absorbed surface particle density or the positions of freely diffusing particles inside a spherical volume. We find that the perfectly absorbing sphere is superior to the perfectly monitoring sphere, both for concentration and gradient sensing, since previously observed particles are never remeasured. The superiority of the absorbing sphere helps explain the presence at the surfaces of cells of signal degrading enzymes, such as PDE for cAMP in Dictyostelium discoideum (Dicty) and BAR1 for mating factor alpha in Saccharomyces cerevisiae (budding yeast). Quantitatively, our theory compares favorably to recent measurements of Dicty moving up a cAMP gradient, suggesting these cells operate near the physical limits of gradient detection.

main text: 2 figures and 1 table; supporting information: 1 figure

References in corpus (2)

• Persistent Cell Motion in the Absence of External Signals: A Search Strategy for Eukaryotic Cells
• Fluctuation Induced Instabilities in Front Propagation up a Co-Moving Reaction Gradient in Two Dimensions

Cited by in corpus (66)

• The Energetic Costs of Cellular Computation
• Cost and Precision of Brownian Clocks
• Cell-cell communication enhances the capacity of cell ensembles to sense shallow gradients during morphogenesis
• Maximum likelihood and the single receptor
• Origins of eukaryotic excitability
• Limits of sensing temporal concentration changes by single cells
• Optimal run-and-tumble based transportation of a Janus particle with active steering
• Limits to the precision of gradient sensing with spatial communication and temporal integration
• Mutual information in time-varying biochemical systems
• Bacteria push the limits of chemotactic precision to navigate dynamic chemical gradients
• Chemotactic predator-prey dynamics
• Physical limit to concentration sensing amid spurious ligands
• Noise and information transmission in promoters with multiple internal states
• Dynamics of a microorganism moving by chemotaxis in its own secretion
• Fundamental limits to collective concentration sensing in cell populations
• Receptor crosstalk improves concentration sensing of multiple ligands
• Optimal decision making for sperm chemotaxis in the presence of noise
• Physical Limits on Bacterial Navigation in Dynamic Environments
• Cell-to-cell variation sets a tissue-rheology-dependent bound on collective gradient sensing
• Know the single-receptor sensing limit? Think again
• Collective chemotaxis through noisy multicellular gradient sensing
• Optimal receptor-cluster size determined by intrinsic and extrinsic noise
• Noise Filtering Strategies of Adaptive Signaling Networks: The Case of E. Coli Chemotaxis
• Immune cells use active tugging forces to distinguish affinity and accelerate evolution
• Fractional Patlak-Keller-Segel equations for chemotactic superdiffusion
• Chemical Cloaking
• A connection between bacterial chemotactic network and optimal filtering
• Sense and sensitivity: physical limits to multicellular sensing, migration and drug response
• Increased accuracy of ligand sensing by receptor internalization
• Mixed analytical-stochastic simulation method for the recovery of a Brownian gradient source from probability fluxes to small windows
• How input fluctuations reshape the dynamics of a biological switching system
• Extending the dynamic range of transcription factor action by translational regulation
• Bayesian gradient sensing in the presence of rotational diffusion
• Dispersion for Two Classes of Random Variables: General Theory and Application to Inference of an External Ligand Concentration by a Cell
• Precision of flow sensing by self-communicating cells
• Active transport improves the precision of linear long distance molecular signalling
• Noise Effects in Nonlinear Biochemical Signaling
• Chemotaxis in uncertain environments: hedging bets with multiple receptor types
• Role of spatial averaging in multicellular gradient sensing
• Persistent pseudopod splitting is an effective chemotaxis strategy in shallow gradients
• Multicellular sensing at a feedback-induced critical point
• Triangulation sensing: how cells recover a source from diffusing particles in three dimensions
• Accuracy of position determination in Ca${}^{2+}$ signaling
• Positional information readout in $C{a}^{2+}$ signaling
• Learning optimal integration of spatial and temporal information in noisy chemotaxis
• Gradient sensing limit of a cell when controlling the elongating direction
• Signal reconstruction in diffusion-based molecular communication
• Autologous chemotaxis at high cell density
• Extrinsic and intrinsic correlations in molecular information transmission
• Unified Linear Fluctuation-Response Theory Arbitrarily Far from Equilibrium
• Precision of protein thermometry
• Dispersion of the time spent in a state: General expression for unicyclic model and dissipation-less precision
• Increased accuracy of ligand sensing by receptor diffusion on cell surface
• Local Clustering and Global Spreading of Receptors for Optimal Spatial Gradient Sensing
• Nonequilibrium fluctuation-response relations for state observables
• Limitations on concentration measurements and gradient discerning times in cellular systems
• Physical limits to sensing material properties
• Accuracy in readout of glutamate concentrations by neuronal cells
• Nonlinear Response Relations and Fluctuation-Response Inequalities for Nonequilibrium Stochastic Systems
• Biological efficiency in processing information
• Accuracy of direct gradient sensing by cell-surface receptors
• Physical limits on chemical sensing in bounded domains
• Average search time bound in cue based search strategy
• Distinct cell shapes determine accurate chemotaxis
• Computational methods and fast hybrid stochastic simulations for triangulation sensing and identifying principles of cell navigation in the brain
• Hunchback promoters can readout morphogenetic positional information in less than a minute