The study of bacterial ion channels has provided fundamental insights into the structural basis of neuronal signaling. However, the native role of ion channels in bacteria has remained elusive. Here we show that ion channels conduct long-range electrical signals within bacterial biofilm communities through spatially propagating waves of potassium. These waves result from a positive feedback loop, in which a metabolic trigger induces release of intracellular potassium, which in turn depolarizes neighboring cells. Propagating through the biofilm, this wave of depolarization coordinates metabolic states among cells in the interior and periphery of the biofilm. Deletion of the potassium channel abolishes this response. As predicted by a mathematical model, we further show that spatial propagation can be hindered by specific genetic perturbations to potassium channel gating. Together, these results demonstrate a function for ion channels in bacterial biofilms, and provide a prokaryotic paradigm for active, long-range electrical signaling in cellular communities.
Cells that reside within a community can cooperate and also compete with each other for resources. It remains unclear how these opposing interactions are resolved at the population level. Here we investigated such an internal conflict within a microbial biofilm community: Cells in the biofilm periphery not only protect interior cells from external attack, but also starve them through nutrient consumption. We discovered that this conflict between protection and starvation is resolved through emergence of long-range metabolic codependence between peripheral and interior cells. As a result, biofilm growth halts periodically, increasing nutrient availability for the sheltered interior cells. We show that this collective oscillation in biofilm growth benefits the community in the event of a chemical attack. These findings indicate that oscillations support population-level conflict resolution by coordinating competing metabolic demands in space and time, suggesting new strategies to control biofilm growth.
Summary Bacteria residing within biofilm communities can coordinate their behavior through cell-to-cell signaling. However, it remains unclear if these signals can also influence the behavior of distant cells that are not part of the community. Using a microfluidic approach, we find that potassium ion channel-mediated electrical signaling generated by a Bacillus subtilis biofilm can attract distant cells. Integration of experiments and mathematical modeling indicates that extracellular potassium emitted from the biofilm alters the membrane potential of distant cells, thereby directing their motility. This electrically-mediated attraction appears to be a generic mechanism that enables cross-species interactions, as Pseudomonas aeruginosa cells also become attracted to the electrical signal released by the B. subtilis biofilm. Cells within a biofilm community can thus not only coordinate their own behavior, but also influence the behavior of diverse bacteria at a distance through long-range electrical signaling.
Bacteria within communities can interact to organize their behavior. It has been unclear whether such interactions can extend beyond a single community to coordinate the behavior of distant populations. We discovered that two Bacillus subtilis biofilm communities undergoing metabolic oscillations can become coupled through electrical signaling and synchronize their growth dynamics. Coupling increases competition by also synchronizing demand for limited nutrients. As predicted by mathematical modeling, we confirm that biofilms resolve this conflict by switching from in-phase to antiphase oscillations. This results in time-sharing behavior, where each community takes turns consuming nutrients. Time-sharing enables biofilms to counterintuitively increase growth under reduced nutrient supply. Distant biofilms can thus coordinate their behavior to resolve nutrient competition through time-sharing, a strategy used in engineered systems to allocate limited resources.
A large number of proteins are sufficiently unstable that their full 3D structure cannot be resolved. The origins of this intrinsic disorder are not well understood, but its ubiquitous presence undercuts the principle that a protein's structure determines its function. Here we present a quantitative theory that makes predictions regarding the role of intrinsic disorder in protein structure and function. In particular, we discuss the implications of analytical solutions of a series of fundamental thermodynamic models of protein interactions in which disordered proteins are characterized by positive folding free energies. We validate our predictions by assigning protein function by using the gene ontology classification-in which ''protein binding'', ''catalytic activity'', and ''transcription regulator activity'' are the three largest functional categories-and by performing genome-wide surveys of both the amount of disorder in these functional classes and binding affinities for both prokaryotic and eukaryotic genomes. Specifically, without assuming any a priori structure-function relationship, the theory predicts that both catalytic and low-affinity binding (Kd տ10 ؊7 M) proteins prefer ordered structures, whereas only high-affinity binding proteins (found mostly in eukaryotes) can tolerate disorder. Relevant to both transcription and signal transduction, the theory also explains how increasing disorder can tune the binding affinity to maximize the specificity of promiscuous interactions. Collectively, these studies provide insight into how natural selection acts on folding stability to optimize protein function.binding ͉ catalysis ͉ intrinsic disorder ͉ specificity ͉ transcription M ost proteins are not stable enough for current technologies to resolve their full 3D structure (1). In fact, estimates suggest that anywhere between 25% and 41% of the proteins in eukaryotic genomes contain long-disordered regions (2). It has been suggested that disorder itself plays a functional role by, e.g., allowing for multiple interaction partners (3) and functional diversity (4-6), which are particularly important in cell signaling and cancer (7). The correlation between intrinsic disorder and protein function, however, is still nebulous and led us to look for more general principles that might relate protein function and disorder. Unlike the aforementioned bioinformatics approaches and other heuristic models (8), here we examine the linkage between disorder and protein function from a thermodynamic point of view.Without assuming any structure-function relationship, we look for experimentally derived parameters that might relate protein function and disorder. As described by Dyson and Wright (9), proteins in the cellular environment may have disorder in long loops, end terminals, hinge regions, domains, and even covering their full sequences. However, in a complex, these motifs acquire well-defined 3D structures. Common descriptors to all these forms of disorder are the folding free energy (⌬G f ) of the motifs participating in...
Signal transmission among cells enables long-range coordination in biological systems. However, the scarcity of quantitative measurements hinders the development of theories that relate signal propagation to cellular heterogeneity and spatial organization. We address this problem in a bacterial community that employs electrochemical cell-to-cell communication. We developed a model based on percolation theory, which describes how signals propagate through a heterogeneous medium. Our model predicts that signal transmission becomes possible when the community is organized near a critical phase transition between a disconnected and a fully connected conduit of signaling cells. By measuring population-level signal transmission with single-cell resolution in wild-type and genetically modified communities, we confirm that the spatial distribution of signaling cells is organized at the predicted phase transition. Our findings suggest that at this critical point, the population-level benefit of signal transmission outweighs the single-cell level cost. The bacterial community thus appears to be organized according to a theoretically predicted spatial heterogeneity that promotes efficient signal transmission.
Highlights d Bacteria form membrane-potential-based memory, reminiscent of neurons d Bacterial memory is formed through a light-induced change to potassium channels d As predicted by a Hodgkin-Huxley model, memory is robust to ionic perturbations d Complex memory patterns can be encoded in a biofilm at the single-cell level
Straw returning is an effective way to improve soil quality. Whether the bacterial community development has been changed by long-term straw returning in non-calcareous fluroacquic soil is not clear. In this study, the following five treatments were administered: soil without fertilizer (CK); wheat and corn straw returning (WC); wheat straw returning with 276 kg N ha −1 yr −1 (WN); manure, 60,000 kg ha −1 pig manure compost (M) and wheat and corn straw returning with 276 kg N ha −1 yr −1 (WCN). The high-throughput 16S rRNA sequencing technology was used to evaluate the bacterial communities. The results showed that the community was composed mostly of two dominant groups (Proteobacteria and Acidobacteria). Bacterial diversity increased after the application of straw and manure. Principal component analyses revealed that the soil bacterial community differed significantly between treatments. The WCN treatment showed relatively higher total soil N, available P, available K, and organic carbon and invertase, urease, cellulase activities and yield than the WC treatment. Our results suggested that application of N fertilizer to straw returning soil had significantly higher soil fertility and enzyme activity than straw returning alone, which resulted in a different bacterial community composition, Stenotrophomonas, Pseudoxanthomonas, and Acinetobacter which were the dominant genera in the WC treatment while Candidatus, Koribacter and Granulicella were the dominant genera in the WCN treatment. To summarize, wheat and maize straw returning with N fertilizer would be the optimum proposal for improving soil quality and yield in the future in non-calcareous fluro-acquicwheat and maize cultivated soils in the North China Plain in China.
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