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Periodical cicadas exhibit life cycles with durations of 13 or 17 years, and it is now accepted that large prime cycles arose to avoid synchrony with predators. Less well explored is how, in the face of intrinsic biological and environmental noise, insects within a brood emerge together in large successive swarms from underground during springtime warming. Here, we consider the decision-making process of underground cicadas experiencing random, spatially correlated thermal microclimates such as those in nature. Introducing short-range communication between insects leads to an Ising model of consensus building with a quenched, spatially correlated random magnetic field and annealed site dilution, which displays the kinds of collective swarms seen in nature. These results highlight the need for fieldwork to quantify the spatial fluctuations in thermal microclimates and their relationship to the spatiotemporal dynamics of swarm emergence.
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Hemípteros , Animais , ConsensoRESUMO
The recent discovery of the striking sheetlike multicellular choanoflagellate species Choanoeca flexa that dynamically interconverts between two hemispherical forms of opposite orientation raises fundamental questions in cell and evolutionary biology, as choanoflagellates are the closest living relatives of animals. It similarly motivates questions in fluid and solid mechanics concerning the differential swimming speeds in the two states and the mechanism of curvature inversion triggered by changes in the geometry of microvilli emanating from each cell. Here we develop fluid dynamical and mechanical models to address these observations and show that they capture the main features of the swimming, feeding, and inversion of C. flexa colonies, which can be viewed as active, shape-shifting polymerized membranes.
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Coanoflagelados , Animais , Coanoflagelados/metabolismo , Natação , Evolução BiológicaRESUMO
A fundamental issue in biology is the nature of evolutionary transitions from unicellular to multicellular organisms. Volvocine algae are models for this transition, as they span from the unicellular biflagellate Chlamydomonas to multicellular species of Volvox with up to 50,000 Chlamydomonas-like cells on the surface of a spherical extracellular matrix. The mechanism of phototaxis in these species is of particular interest since they lack a nervous system and intercellular connections; steering is a consequence of the response of individual cells to light. Studies of Volvox and Gonium, a 16-cell organism with a plate-like structure, have shown that the flagellar response to changing illumination of the cellular photosensor is adaptive, with a recovery time tuned to the rotation period of the colony around its primary axis. Here, combining high-resolution studies of the flagellar photoresponse of micropipette-held Chlamydomonas with 3D tracking of freely swimming cells, we show that such tuning also underlies its phototaxis. A mathematical model is developed based on the rotations around an axis perpendicular to the flagellar beat plane that occur through the adaptive response to oscillating light levels as the organism spins. Exploiting a separation of timescales between the flagellar photoresponse and phototurning, we develop an equation of motion that accurately describes the observed photoalignment. In showing that the adaptive timescales in Volvocine algae are tuned to the organisms' rotational periods across three orders of magnitude in cell number, our results suggest a unified picture of phototaxis in green algae in which the asymmetry in torques that produce phototurns arise from the individual flagella of Chlamydomonas, the flagellated edges of Gonium, and the flagellated hemispheres of Volvox.
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Chlamydomonas , Clorófitas , Volvox , Filogenia , Fototaxia , Evolução BiológicaRESUMO
The collapse of a catenoidal soap film when the rings supporting it are moved beyond a critical separation is a classic problem in interface motion in which there is a balance between surface tension and the inertia of the surrounding air, with film viscosity playing only a minor role. Recently [Goldstein et al., Phys. Rev. E, 2021, 104, 035105], we introduced a variant of this problem in which the catenoid is bisected by a glass plate located in a plane of symmetry perpendicular to the rings, producing two identical hemicatenoids, each with a surface Plateau border (SPB) on the glass plate. Beyond the critical ring separation, the hemicatenoids collapse in a manner qualitatively similar to the bulk problem, but their motion is governed by the frictional forces arising from viscous dissipation in the SPBs. We present numerical studies of a model that includes classical laws in which the frictional force fv for SPB motion on wet surfaces is of the form fv â¼ Can, where Ca is the capillary number. Our experimental data on the temporal evolution of this process confirms the expected value n = 2/3 for mobile surfactants and stress-free interfaces. This study can help explain the fragmentation of bubbles inside very confined geometries such as porous materials or microfluidic devices.
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Bacteria often form surface-bound communities, embedded in a self-produced extracellular matrix, called biofilms. Quantitative studies of bioflim growth have typically focused on unconfined expansion above solid or semisolid surfaces, leading to exponential radial growth. This geometry does not accurately reflect the natural or biomedical contexts in which biofilms grow in confined spaces. Here, we consider one of the simplest confined geometries: a biofilm growing laterally in the space between a solid surface and an overlying elastic sheet. A poroelastic framework is utilized to derive the radial growth rate of the biofilm; it reveals an additional self-similar expansion regime, governed by the Poisson's ratio of the matrix, leading to a finite maximum radius, consistent with our experimental observations of growing Bacillus subtilis biofilms confined by polydimethylsiloxane.
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Bacillus subtilis , Biofilmes , Matriz ExtracelularRESUMO
The prevalence of multicellular organisms is due in part to their ability to form complex structures. How cells pack in these structures is a fundamental biophysical issue, underlying their functional properties. However, much remains unknown about how cell packing geometries arise, and how they are affected by random noise during growth - especially absent developmental programs. Here, we quantify the statistics of cellular neighborhoods of two different multicellular eukaryotes: lab-evolved 'snowflake' yeast and the green alga Volvox carteri. We find that despite large differences in cellular organization, the free space associated with individual cells in both organisms closely fits a modified gamma distribution, consistent with maximum entropy predictions originally developed for granular materials. This 'entropic' cellular packing ensures a degree of predictability despite noise, facilitating parent-offspring fidelity even in the absence of developmental regulation. Together with simulations of diverse growth morphologies, these results suggest that gamma-distributed cell neighborhood sizes are a general feature of multicellularity, arising from conserved statistics of cellular packing.
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Evolução Molecular Direcionada , Volvox/genética , Leveduras/genética , Tamanho Celular , Filogenia , Volvox/citologia , Volvox/fisiologia , Leveduras/citologia , Leveduras/fisiologiaRESUMO
In tissues as diverse as amphibian skin and the human airway, the cilia that propel fluid are grouped in sparsely distributed multiciliated cells (MCCs). We investigate fluid transport in this "mosaic" architecture, with emphasis on the trade-offs that may have been responsible for its evolutionary selection. Live imaging of MCCs in embryos of the frog Xenopus laevis shows that cilia bundles behave as active vortices that produce a flow field accurately represented by a local force applied to the fluid. A coarse-grained model that self-consistently couples bundles to the ambient flow reveals that hydrodynamic interactions between MCCs limit their rate of work so that they best shear the tissue at a finite but low area coverage, a result that mirrors findings for other sparse distributions such as cell receptors and leaf stomata.
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Cílios/fisiologia , Hidrodinâmica , Animais , Humanos , Xenopus laevisRESUMO
Experimental and theoretical work reported here on the collapse of catenoidal soap films of various viscosities reveal the existence of a robust geometric feature that appears not to have been analyzed previously; prior to the ultimate pinchoff event on the central axis, which is associated with the formation of a well-studied local double-cone structure folded back on itself, the film transiently consists of two acute-angle cones connected to the supporting rings, joined by a central quasicylindrical region. As the cylindrical region becomes unstable and pinches, the opening angle of those cones is found to be universal, independent of film viscosity. Moreover, that same opening angle at pinching is found when the transition occurs in a hemicatenoid bounded by a surface. The approach to the conical structure is found to obey classical Keller-Miksis scaling of the minimum radius as a function of time, down to very small but finite radii. While there is a large body of work on the detailed structure of the singularities associated with ultimate pinchoff events, these large-scale features have not been addressed. Here we study these geometrical aspects of film collapse by several distinct approaches, including a systematic analysis of the linear and weakly nonlinear dynamics in the neighborhood of the saddle node bifurcation leading to collapse, both within mean curvature flow and the physically realistic Euler flow associated with the incompressible dynamics of the surrounding air. These analyses are used to show how much of the geometry of collapsing catenoids is accurately captured by a few active modes triggered by boundary deformation. A separate analysis based on a mathematical sequence of shapes progressing from the critical catenoid towards the Goldschmidt solution is shown to predict accurately the cone angle at pinching. We suggest that the approach to the conical structures can be viewed as passage close to an unstable fixed point of conical similarity solutions. The overall analysis provides the basis for the systematic study of more complex problems of surface instabilities triggered by deformations of the supporting boundaries.
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Cardiovascular disease remains one of the world's leading causes of death. Myocardial infarction (heart attack) is triggered by occlusion of coronary arteries by platelet-rich thrombi (clots). The development of new anti-platelet drugs to prevent myocardial infarction continues to be an active area of research and is dependent on accurately modelling the process of clot formation. Occlusive thrombi can be generated in vivo in a range of species, but these models are limited by variability and lack of relevance to human disease. Although in vitro models using human blood can overcome species-specific differences and improve translatability, many models do not generate occlusive thrombi. In those models that do achieve occlusion, time to occlusion is difficult to measure in an unbiased and objective manner. In this study we developed a simple and robust approach to determine occlusion time of a novel in vitro microfluidic assay. This highlighted the potential for occlusion to occur in thrombosis microfluidic devices through off-site coagulation, obscuring the effect of anti-platelet drugs. We therefore designed a novel occlusive thrombosis-on-a-chip microfluidic device that reliably generates occlusive thrombi at arterial shear rates by quenching downstream coagulation. We further validated our device and methods by using the approved anti-platelet drug, eptifibatide, recording a significant difference in the "time to occlude" in treated devices compared to control conditions. These results demonstrate that this device can be used to monitor the effect of antithrombotic drugs on time to occlude, and, for the first time, delivers this essential data in an unbiased and objective manner.
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Preparações Farmacêuticas , Trombose , Coagulação Sanguínea , Plaquetas , Humanos , Dispositivos Lab-On-A-Chip , Trombose/tratamento farmacológicoRESUMO
Turing instabilities of reaction-diffusion systems can only arise if the diffusivities of the chemical species are sufficiently different. This threshold is unphysical in most systems with N=2 diffusing species, forcing experimental realizations of the instability to rely on fluctuations or additional nondiffusing species. Here, we ask whether this diffusive threshold lowers for N>2 to allow "true" Turing instabilities. Inspired by May's analysis of the stability of random ecological communities, we analyze the probability distribution of the diffusive threshold in reaction-diffusion systems defined by random matrices describing linearized dynamics near a homogeneous fixed point. In the numerically tractable cases N⩽6, we find that the diffusive threshold becomes more likely to be smaller and physical as N increases, and that most of these many-species instabilities cannot be described by reduced models with fewer diffusing species.
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Deformations of cell sheets during morphogenesis are driven by developmental processes such as cell division and cell shape changes. In morphoelastic shell theories of development, these processes appear as variations of the intrinsic geometry of a thin elastic shell. However, morphogenesis often involves large bending deformations that are outside the formal range of validity of these shell theories. Here, by asymptotic expansion of three-dimensional incompressible morphoelasticity in the limit of a thin shell, we derive a shell theory for large intrinsic bending deformations and emphasize the resulting geometric material anisotropy and the elastic role of cell constriction. Taking the invagination of the green alga Volvox as a model developmental event, we show how results for this theory differ from those for a classical shell theory that is not formally valid for these large bending deformations and reveal how these geometric effects stabilize invagination.
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In the cellular phenomena of cytoplasmic streaming, molecular motors carrying cargo along a network of microtubules entrain the surrounding fluid. The piconewton forces produced by individual motors are sufficient to deform long microtubules, as are the collective fluid flows generated by many moving motors. Studies of streaming during oocyte development in the fruit fly Drosophila melanogaster have shown a transition from a spatially disordered cytoskeleton, supporting flows with only short-ranged correlations, to an ordered state with a cell-spanning vortical flow. To test the hypothesis that this transition is driven by fluid-structure interactions, we study a discrete-filament model and a coarse-grained continuum theory for motors moving on a deformable cytoskeleton, both of which are shown to exhibit a swirling instability to spontaneous large-scale rotational motion, as observed.
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Citoesqueleto/química , Citoesqueleto/metabolismo , Microtúbulos/química , Microtúbulos/metabolismo , Modelos Biológicos , Animais , Fenômenos Biomecânicos , Citoplasma/química , Citoplasma/metabolismo , Corrente Citoplasmática , Drosophila melanogasterRESUMO
An important question in early neural development is the origin of stochastic nuclear movement between apical and basal surfaces of neuroepithelia during interkinetic nuclear migration. Tracking of nuclear subpopulations has shown evidence of diffusion - mean squared displacements growing linearly in time - and suggested crowding from cell division at the apical surface drives basalward motion. Yet, this hypothesis has not yet been tested, and the forces involved not quantified. We employ long-term, rapid light-sheet and two-photon imaging of early zebrafish retinogenesis to track entire populations of nuclei within the tissue. The time-varying concentration profiles show clear evidence of crowding as nuclei reach close-packing and are quantitatively described by a nonlinear diffusion model. Considerations of nuclear motion constrained inside the enveloping cell membrane show that concentration-dependent stochastic forces inside cells, compatible in magnitude to those found in cytoskeletal transport, can explain the observed magnitude of the diffusion constant.
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Movimento Celular , Núcleo Celular/metabolismo , Retina/embriologia , Peixe-Zebra/embriologia , Animais , Difusão , Embrião não Mamífero/embriologiaRESUMO
One of the characteristic features of many marine dinoflagellates is their bioluminescence, which lights up nighttime breaking waves or seawater sliced by a ship's prow. While the internal biochemistry of light production by these microorganisms is well established, the manner by which fluid shear or mechanical forces trigger bioluminescence is still poorly understood. We report controlled measurements of the relation between mechanical stress and light production at the single cell level, using high-speed imaging of micropipette-held cells of the marine dinoflagellate Pyrocystis lunula subjected to localized fluid flows or direct indentation. We find a viscoelastic response in which light intensity depends on both the amplitude and rate of deformation, consistent with the action of stretch-activated ion channels. A phenomenological model captures the experimental observations.
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Dinoflagellida/fisiologia , Modelos Biológicos , Dinoflagellida/química , Dinoflagellida/ultraestrutura , Canais Iônicos/química , Canais Iônicos/fisiologia , Luminescência , Análise de Célula Única , Estresse Mecânico , Substâncias Viscoelásticas/químicaRESUMO
Centrioles are cylindrical assemblies whose peripheral microtubule array displays a 9-fold rotational symmetry that is established by the scaffolding protein SAS6. Centriole symmetry can be broken by centriole-associated structures, such as the striated fibers in Chlamydomonas that are important for ciliary function. The conserved protein CCDC61/VFL3 is involved in this process, but its exact role is unclear. Here, we show that CCDC61 is a paralog of SAS6. Crystal structures of CCDC61 demonstrate that it contains two homodimerization interfaces that are similar to those found in SAS6, but result in the formation of linear filaments rather than rings. Furthermore, we show that CCDC61 binds microtubules and that residues involved in CCDC61 microtubule binding are important for ciliary function in Chlamydomonas. Together, our findings suggest that CCDC61 and SAS6 functionally diverged from a common ancestor while retaining the ability to scaffold the assembly of basal body-associated structures or centrioles, respectively.
Assuntos
Proteínas de Ciclo Celular/química , Proteínas de Ciclo Celular/metabolismo , Chlamydomonas/fisiologia , Cílios/metabolismo , Proteínas Associadas aos Microtúbulos/química , Proteínas Associadas aos Microtúbulos/metabolismo , Proteínas de Algas/química , Proteínas de Algas/metabolismo , Linhagem Celular , Chlamydomonas/classificação , Cristalografia por Raios X , Células HEK293 , Humanos , Microtúbulos/metabolismo , Modelos Moleculares , Filogenia , Conformação Proteica , Domínios Proteicos , Multimerização ProteicaRESUMO
Green algae of the Volvocine lineage, spanning from unicellular Chlamydomonas to vastly larger Volvox, are models for the study of the evolution of multicellularity, flagellar dynamics, and developmental processes. Phototactic steering in these organisms occurs without a central nervous system, driven solely by the response of individual cells. All such algae spin about a body-fixed axis as they swim; directional photosensors on each cell thus receive periodic signals when that axis is not aligned with the light. The flagella of Chlamydomonas and Volvox both exhibit an adaptive response to such signals in a manner that allows for accurate phototaxis, but in the former the two flagella have distinct responses, while the thousands of flagella on the surface of spherical Volvox colonies have essentially identical behavior. The planar 16-cell species Gonium pectorale thus presents a conundrum, for its central 4 cells have a Chlamydomonas-like beat that provide propulsion normal to the plane, while its 12 peripheral cells generate rotation around the normal through a Volvox-like beat. Here we combine experiment, theory, and computations to reveal how Gonium, perhaps the simplest differentiated colonial organism, achieves phototaxis. High-resolution cell tracking, particle image velocimetry of flagellar driven flows, and high-speed imaging of flagella on micropipette-held colonies show how, in the context of a recently introduced model for Chlamydomonas phototaxis, an adaptive response of the peripheral cells alone leads to photoreorientation of the entire colony. The analysis also highlights the importance of local variations in flagellar beat dynamics within a given colony, which can lead to enhanced reorientation dynamics.
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Comamonadaceae/fisiologia , Comamonadaceae/efeitos da radiação , Fototaxia , Hidrodinâmica , Modelos Biológicos , RotaçãoRESUMO
The growing concerns over desertification have spurred research into technologies aimed at acquiring water from nontraditional sources such as dew, fog, and water vapor. Some of the most promising developments have focused on improving designs to collect water from fog. However, the absence of a shared framework to predict, measure, and compare the water collection efficiencies of new prototypes is becoming a major obstacle to progress in the field. We address this problem by providing a general theory to design efficient fog collectors as well as a concrete experimental protocol to furnish our theory with all the necessary parameters to quantify the effective water collection efficiency. We show in particular that multilayer collectors are required for high fog collection efficiency and that all efficient designs are found within a narrow range of mesh porosity. We support our conclusions with measurements on simple multilayer harp collectors.
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Superhydrophobic surfaces (SHSs) have the potential to reduce drag at solid boundaries. However, multiple independent studies have recently shown that small amounts of surfactant, naturally present in the environment, can induce Marangoni forces that increase drag, at least in the laminar regime. To obtain accurate drag predictions, one must solve the mass, momentum, bulk surfactant and interfacial surfactant conservation equations. This requires expensive simulations, thus preventing surfactant from being widely considered in SHS studies. To address this issue, we propose a theory for steady, pressure-driven, laminar, two-dimensional flow in a periodic SHS channel with soluble surfactant. We linearise the coupling between flow and surfactant, under the assumption of small concentration, finding a scaling prediction for the local slip length. To obtain the drag reduction and interfacial shear, we find a series solution for the velocity field by assuming Stokes flow in the bulk and uniform interfacial shear. We find how the slip and drag depend on the nine dimensionless groups that together characterize the surfactant transport near SHSs, the gas fraction and the normalized interface length. Our model agrees with numerical simulations spanning orders of magnitude in each dimensionless group. The simulations also provide the constants in the scaling theory. Our model significantly improves predictions relative to a surfactant-free one, which can otherwise overestimate slip and underestimate drag by several orders of magnitude. Our slip length model can provide the boundary condition in other simulations, thereby accounting for surfactant effects without having to solve the full problem.
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One approach to quantifying biological diversity consists of characterizing the statistical distribution of specific properties of a taxonomic group or habitat. Microorganisms living in fluid environments, and for whom motility is key, exploit propulsion resulting from a rich variety of shapes, forms, and swimming strategies. Here, we explore the variability of swimming speed for unicellular eukaryotes based on published data. The data naturally partitions into that from flagellates (with a small number of flagella) and from ciliates (with tens or more). Despite the morphological and size differences between these groups, each of the two probability distributions of swimming speed are accurately represented by log-normal distributions, with good agreement holding even to fourth moments. Scaling of the distributions by a characteristic speed for each data set leads to a collapse onto an apparently universal distribution. These results suggest a universal way for ecological niches to be populated by abundant microorganisms.