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.
From microbial biofilm communities to multicellular organisms, 3D macroscopic structures develop through poorly understood interplay between cellular processes and mechanical forces. Investigating wrinkled biofilms of Bacillus subtilis, we discovered a pattern of localized cell death that spatially focuses mechanical forces, and thereby initiates wrinkle formation. Deletion of genes implicated in biofilm development, together with mathematical modeling, revealed that ECM production underlies the localization of cell death. Simultaneously with cell death, we quantitatively measured mechanical stiffness and movement in WT and mutant biofilms. Results suggest that localized cell death provides an outlet for lateral compressive forces, thereby promoting vertical mechanical buckling, which subsequently leads to wrinkle formation. Guided by these findings, we were able to generate artificial wrinkle patterns within biofilms. Formation of 3D structures facilitated by cell death may underlie self-organization in other developmental systems, and could enable engineering of macroscopic structures from cell populations.pattern formation | self-assembly | systems dynamics S elf-organization in space and time is a fundamental developmental process, defined by the autonomous formation of 3D macroscopic structures by replicating cell populations (1-3). Such 3D pattern formation underlies the development of all multicellular organisms and cellular communities, and appears to be governed by two principal processes. First, genetic programs control cellular processes, such as growth, death, and differentiation. Second, 3D structure formation involves macroscopic movement of cell populations that are determined by mechanical properties and physical forces (4). Recent studies have investigated each of these processes separately in different biological systems (5-8). However, insight into the direct interplay between cellular and mechanical processes that drives development requires simultaneous measurement of both processes, and thus constitutes a major challenge.Compared with multicellular organisms, microbial biofilms are simpler systems for investigating the interaction between cellular and mechanical aspects of 3D self-organization during development. Interestingly, these microbial communities still exhibit diverse cellular behaviors and complex spatial organization (9-14). For example, biofilms can develop from a single cell and give rise to complex 3D wrinkle structures that are visible to the naked eye, comprising billions of cells (9, 10, 15) (Fig. 1A). Aside from replication, bacterial cells can also exhibit other behaviors, such as genetically controlled cell death (9,16,17) and excretion of ECM components (9,13,(18)(19)(20)(21). In fact, one of the defining features of any biofilm is that cells are embedded within an ECM composed of diverse molecules, such as polysaccharides and amyloid fibers (19-21). The ECM is required for wrinkle formation and appears to provide the biofilm with resilience against environmental extrem...
Nuclear proteins are selectively imported into the nucleus by transport factors such as importin-alpha and importin-beta. Here, we show that the expression of importin-alpha subtypes is strictly regulated during neural differentiation of mouse embryonic stem (ES) cells, and that the switching of importin-alpha subtype expression is critical for neural differentiation. Moreover, reproducing the switching of importin-alpha subtype expression in undifferentiated ES cells induced neural differentiation in the presence of leukaemia inhibitory factor (LIF) and serum, coordinated with the regulated expression of Oct3/4, Brn2 and SOX2, which are involved in ES-neural identity determination. These transcription factors were selectively imported into the nucleus by specific subtypes of importin-alpha. Thus, importin-alpha subtype switching has a major impact on cell differentiation through the regulated nuclear import of a specific set of transcription factors. This is the first study to propose that transport factors should be considered as major players in cell-fate determination.
All cellular membranes have the functionality of generating and maintaining the gradients of electrical and electrochemical potentials. Such potentials were generally thought to be an essential but homeostatic contributor to complex bacterial behaviors. Recent studies have revised this view, and we now know that bacterial membrane potential is dynamic and plays signaling roles in cellcell interaction, adaptation to antibiotics, and sensation of cellular conditions and environments. These discoveries argue that bacterial membrane potential dynamics deserve more attention. Here, we review the recent studies revealing the signaling roles of bacterial membrane potential dynamics. We also introduce basic biophysical theories of the membrane potential to the microbiology community and discuss the needs to revise these theories for applications in bacterial electrophysiology. Membrane Potential Is Important for Bacterial FunctionsAcross the cellular membrane there is an electrical potential (see Glossary) difference, akin to a conventional battery. This electrical potential across the membrane, membrane potential (a.k.a. transmembrane voltage), is a source of free energy which enables cells to do chemical and mechanical work. Due to its well-known importance in fundamental cellular functions such as ATP synthesis [1,2], this potential was generally assumed to be homeostatic. However, recent studies revealed that the bacterial membrane potential is dynamicit can act as a tool for information signaling and processing. It is now evident that membrane potential regulates a wide range of bacterial physiology and behaviors, for example, pH homeostasis [3,4], membrane transport [5], motility [6,7], antibiotic resistance [8], cell division [9], electrical communication [10,11], and environmental sensing [12][13][14]. Here, we review the physiological roles of bacterial membrane potential as a source of free energy and as a means of information signaling and processing (Figure 1). The roles of membrane potential in bioenergetics are well documented in textbooks (e.g., [15]). Thus, our main focus is on recent studies reporting the dynamic signaling.While we introduce the basic biophysical theories of membrane potential that are critical for microbiological investigations, in-depth biophysical analyses and concepts of membrane potential, including dipolar potential and electrodiffusion, are beyond the scope of this article. This is due to our focus here on microbiological context. For these topics, we recommend the reviews [16][17][18][19]. This review focuses on studies at the cellular level. Readers interested in studies on the molecular dynamics of prokaryotic ion channels are directed to the reviews [20][21][22]. They are only superficially mentioned because of our focus on the cell-level phenomena. Membrane potential dynamics is not the only electrical process in cells. The other important electrical and electrochemical cellular processes, such as redox metabolism, external electron transfer (EET), and direct interspecies ele...
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