Journal articles: 'Run-and-tumble chemotaxis'

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Bearon, R. "Modelling Run-and-Tumble Chemotaxis in a Shear Flow." Bulletin of Mathematical Biology 62, no. 4 (July 2000): 775–91. http://dx.doi.org/10.1006/bulm.2000.0178.

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Nicolau, Dan V., Judith P. Armitage, and Philip K. Maini. "Directional persistence and the optimality of run-and-tumble chemotaxis." Computational Biology and Chemistry 33, no. 4 (August 2009): 269–74. http://dx.doi.org/10.1016/j.compbiolchem.2009.06.003.

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Locsei, J. T. "Persistence of direction increases the drift velocity of run and tumble chemotaxis." Journal of Mathematical Biology 55, no. 1 (March 13, 2007): 41–60. http://dx.doi.org/10.1007/s00285-007-0080-z.

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Kirkegaard, Julius B., and Raymond E. Goldstein. "The role of tumbling frequency and persistence in optimal run-and-tumble chemotaxis." IMA Journal of Applied Mathematics 83, no. 4 (July 25, 2018): 700–719. http://dx.doi.org/10.1093/imamat/hxy013.

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Renadheer, C. S., Ushasi Roy, and Manoj Gopalakrishnan. "A path-integral characterization of run and tumble motion and chemotaxis of bacteria." Journal of Physics A: Mathematical and Theoretical 52, no. 50 (November 15, 2019): 505601. http://dx.doi.org/10.1088/1751-8121/ab5425.

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Maki, Nazli, Jason E. Gestwicki, Ellen M. Lake, Laura L. Kiessling, and Julius Adler. "Motility and Chemotaxis of Filamentous Cells ofEscherichia coli." Journal of Bacteriology 182, no. 15 (August 1, 2000): 4337–42. http://dx.doi.org/10.1128/jb.182.15.4337-4342.2000.

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ABSTRACT Filamentous cells of Escherichia coli can be produced by treatment with the antibiotic cephalexin, which blocks cell division but allows cell growth. To explore the effect of cell size on chemotactic activity, we studied the motility and chemotaxis of filamentous cells. The filaments, up to 50 times the length of normalE. coli organisms, were motile and had flagella along their entire lengths. Despite their increased size, the motility and chemotaxis of filaments were very similar to those properties of normal-sized cells. Unstimulated filaments of chemotactically normal bacteria ran and stopped repeatedly (while normal-sized bacteria run and tumble repeatedly). Filaments responded to attractants by prolonged running (like normal-sized bacteria) and to repellents by prolonged stopping (unlike normal-sized bacteria, which tumble), until adaptation restored unstimulated behavior (as occurs with normal-sized cells). Chemotaxis mutants that always ran when they were normal sized always ran when they were filament sized, and those mutants that always tumbled when they were normal sized always stopped when they were filament sized. Chemoreceptors in filaments were localized to regions both at the poles and at intervals along the filament. We suggest that the location of the chemoreceptors enables the chemotactic responses observed in filaments. The implications of this work with regard to the cytoplasmic diffusion of chemotaxis components in normal-sized and filamentous E. coli are discussed.

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Son, Kwangmin, Filippo Menolascina, and Roman Stocker. "Speed-dependent chemotactic precision in marine bacteria." Proceedings of the National Academy of Sciences 113, no. 31 (July 20, 2016): 8624–29. http://dx.doi.org/10.1073/pnas.1602307113.

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Chemotaxis underpins important ecological processes in marine bacteria, from the association with primary producers to the colonization of particles and hosts. Marine bacteria often swim with a single flagellum at high speeds, alternating “runs” with either 180° reversals or ∼90° “flicks,” the latter resulting from a buckling instability of the flagellum. These adaptations diverge from Escherichia coli’s classic run-and-tumble motility, yet how they relate to the strong and rapid chemotaxis characteristic of marine bacteria has remained unknown. We investigated the relationship between swimming speed, run–reverse–flick motility, and high-performance chemotaxis by tracking thousands of Vibrio alginolyticus cells in microfluidic gradients. At odds with current chemotaxis models, we found that chemotactic precision—the strength of accumulation of cells at the peak of a gradient—is swimming-speed dependent in V. alginolyticus. Faster cells accumulate twofold more tightly by chemotaxis compared with slower cells, attaining an advantage in the exploitation of a resource additional to that of faster gradient climbing. Trajectory analysis and an agent-based mathematical model revealed that this unexpected advantage originates from a speed dependence of reorientation frequency and flicking, which were higher for faster cells, and was compounded by chemokinesis, an increase in speed with resource concentration. The absence of any one of these adaptations led to a 65–70% reduction in the population-level resource exposure. These findings indicate that, contrary to what occurs in E. coli, swimming speed can be a fundamental determinant of the gradient-seeking capabilities of marine bacteria, and suggest a new model of bacterial chemotaxis.

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Hartl, Benedikt, Maximilian Hübl, Gerhard Kahl, and Andreas Zöttl. "Microswimmers learning chemotaxis with genetic algorithms." Proceedings of the National Academy of Sciences 118, no. 19 (May 4, 2021): e2019683118. http://dx.doi.org/10.1073/pnas.2019683118.

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Various microorganisms and some mammalian cells are able to swim in viscous fluids by performing nonreciprocal body deformations, such as rotating attached flagella or by distorting their entire body. In order to perform chemotaxis (i.e., to move toward and to stay at high concentrations of nutrients), they adapt their swimming gaits in a nontrivial manner. Here, we propose a computational model, which features autonomous shape adaptation of microswimmers moving in one dimension toward high field concentrations. As an internal decision-making machinery, we use artificial neural networks, which control the motion of the microswimmer. We present two methods to measure chemical gradients, spatial and temporal sensing, as known for swimming mammalian cells and bacteria, respectively. Using the genetic algorithm NeuroEvolution of Augmenting Topologies, surprisingly simple neural networks evolve. These networks control the shape deformations of the microswimmers and allow them to navigate in static and complex time-dependent chemical environments. By introducing noisy signal transmission in the neural network, the well-known biased run-and-tumble motion emerges. Our work demonstrates that the evolution of a simple and interpretable internal decision-making machinery coupled to the environment allows navigation in diverse chemical landscapes. These findings are of relevance for intracellular biochemical sensing mechanisms of single cells or for the simple nervous system of small multicellular organisms such as Caenorhabditis elegans.

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Locsei, J. T., and T. J. Pedley. "Run and Tumble Chemotaxis in a Shear Flow: The Effect of Temporal Comparisons, Persistence, Rotational Diffusion, and Cell Shape." Bulletin of Mathematical Biology 71, no. 5 (February 7, 2009): 1089–116. http://dx.doi.org/10.1007/s11538-009-9395-9.

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Kasyap, T. V., and Donald L. Koch. "Instability of an inhomogeneous bacterial suspension subjected to a chemo-attractant gradient." Journal of Fluid Mechanics 741 (February 17, 2014): 619–57. http://dx.doi.org/10.1017/jfm.2013.628.

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AbstractThe stability of a suspension of chemotactic bacteria confined in an infinitely long channel and subjected to a stationary, linear chemo-attractant gradient is investigated. While swimming, individual bacteria exert force dipoles on the fluid, which at the continuum level lead to a stress depending upon the bacterial orientation and number density fields. The presence of the attractant gradient causes bacteria to tumble less frequently when swimming along the gradient, leading to a mean orientation and a non-zero chemotactic drift velocity$U_0$in that direction. At long length and time scales compared to those associated with the persistence of bacterial swimming, fluxes due to chemotaxis and the random run–tumble motion of bacteria balance to yield an exponentially varying number density profile across the channel in the base state. The associated bacterial stress field is also exponentially varying and is normal. This spatially non-uniform base state is unstable to fluctuations in the bacterial concentration field when the scaled bacterial concentration$\beta = (3 C/8) \langle n_0\rangle L^2 H$exceeds a critical value determined by a Péclet number defined as${\mathit{Pe}} = U_0 H/\kappa $. Here,$C$is a non-dimensional dipole strength, which depends on the geometry of the bacterium,$\langle n_0\rangle $is the bacterial concentration averaged across the channel of depth$H$,$L$is the total length of the bacterium,$\kappa $is the bacterial diffusivity, and$\beta _{\mathit{crit}}$is a monotonically decreasing function of${\mathit{Pe}}$, with$\beta _{\mathit{crit}} \sim 720/{\mathit{Pe}}^3$for${\mathit{Pe}} \ll 1$and$\beta _{\mathit{crit}} \sim 2$for${\mathit{Pe}} \gg 1$. The instability is the result of the coupling between the active stress-driven fluid flow and the bacterial concentration, and manifests as rectangular convection patterns. When$\beta $first exceeds$\beta _{\mathit{crit}}$, the unstable wavelengths are large with$\lambda \gg H$and the mode of instability is stationary. Although oscillatory modes appear when$\lambda \leq O(H)$and$\beta > 247$, the most dangerous mode of instability is found to be always stationary with a wavelength$\lambda _m/H \sim {\mathit{Pe}}^{-1}$. To study the coupling between the previously analysed orientation shear instability mechanism of bacterial suspensions and the new chemotaxis-driven instability, a new set of continuum equations that consistently account for weak chemotaxis, rotation of bacteria by weak fluid shear and weak non-continuum effects along with their coupled effects has been derived. The stability analysis of those equations showed that the orientation shear mechanism has only a negligible influence on the critical concentration for the present chemotaxis-induced instability when the suspension depth is large, and it is the latter that has the lowest critical concentration.

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del Carmen Burón-Barral, Maria, Khoosheh K. Gosink, and John S. Parkinson. "Loss- and Gain-of-Function Mutations in the F1-HAMP Region of the Escherichia coli Aerotaxis Transducer Aer." Journal of Bacteriology 188, no. 10 (May 15, 2006): 3477–86. http://dx.doi.org/10.1128/jb.188.10.3477-3486.2006.

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ABSTRACT The Escherichia coli Aer protein contains an N-terminal PAS domain that binds flavin adenine dinucleotide (FAD), senses aerotactic stimuli, and communicates with the output signaling domain. To explore the roles of the intervening F1 and HAMP segments in Aer signaling, we isolated plasmid-borne aerotaxis-defective mutations in a host strain lacking all chemoreceptors of the methyl-accepting chemotaxis protein (MCP) family. Under these conditions, Aer alone established the cell's run/tumble swimming pattern and modulated that behavior in response to oxygen gradients. We found two classes of Aer mutants: null and clockwise (CW) biased. Most mutant proteins exhibited the null phenotype: failure to elicit CW flagellar rotation, no aerosensing behavior in MCP-containing hosts, and no apparent FAD-binding ability. However, null mutants had low Aer expression levels caused by rapid degradation of apparently nonnative subunits. Their functional defects probably reflect the absence of a protein product. In contrast, CW-biased mutant proteins exhibited normal expression levels, wild-type FAD binding, and robust aerosensing behavior in MCP-containing hosts. The CW lesions evidently shift unstimulated Aer output to the CW signaling state but do not block the Aer input-output pathway. The distribution and properties of null and CW-biased mutations suggest that the Aer PAS domain may engage in two different interactions with HAMP and the HAMP-proximal signaling domain: one needed for Aer maturation and another for promoting CW output from the Aer signaling domain. Most aerotaxis-defective null mutations in these regions seemed to affect maturation only, indicating that these two interactions involve structurally distinct determinants.

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Che, Yong-Suk, Takashi Sagawa, Yuichi Inoue, Hiroto Takahashi, Tatsuki Hamamoto, Akihiko Ishijima, and Hajime Fukuoka. "Fluctuations in Intracellular CheY-P Concentration Coordinate Reversals of Flagellar Motors in E. coli." Biomolecules 10, no. 11 (November 12, 2020): 1544. http://dx.doi.org/10.3390/biom10111544.

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Signal transduction utilizing membrane-spanning receptors and cytoplasmic regulator proteins is a fundamental process for all living organisms, but quantitative studies of the behavior of signaling proteins, such as their diffusion within a cell, are limited. In this study, we show that fluctuations in the concentration of the signaling molecule, phosphorylated CheY, constitute the basis of chemotaxis signaling. To analyze the propagation of the CheY-P signal quantitatively, we measured the coordination of directional switching between flagellar motors on the same cell. We analyzed the time lags of the switching of two motors in both CCW-to-CW and CW-to-CCW switching (∆τCCW-CW and ∆τCW-CCW). In wild-type cells, both time lags increased as a function of the relative distance of two motors from the polar receptor array. The apparent diffusion coefficient estimated for ∆τ values was ~9 µm2/s. The distance-dependency of ∆τCW-CCW disappeared upon loss of polar localization of the CheY-P phosphatase, CheZ. The distance-dependency of the response time for an instantaneously applied serine attractant signal also disappeared with the loss of polar localization of CheZ. These results were modeled by calculating the diffusion of CheY and CheY-P in cells in which phosphorylation and dephosphorylation occur in different subcellular regions. We conclude that diffusion of signaling molecules and their production and destruction through spontaneous activity of the receptor array generates fluctuations in CheY-P concentration over timescales of several hundred milliseconds. Signal fluctuation coordinates rotation among flagella and regulates steady-state run-and-tumble swimming of cells to facilitate efficient responses to environmental chemical signals.

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Partridge, Jonathan D., Nguyen T. Q. Nhu, Yann S. Dufour, and Rasika M. Harshey. "Escherichia coliRemodels the Chemotaxis Pathway for Swarming." mBio 10, no. 2 (March 19, 2019). http://dx.doi.org/10.1128/mbio.00316-19.

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ABSTRACTMany flagellated bacteria “swarm” over a solid surface as a dense consortium. In different bacteria, swarming is facilitated by several alterations such as those corresponding to increased flagellum numbers, special stator proteins, or secreted surfactants. We report here a change in the chemosensory physiology of swarmingEscherichia coliwhich alters its normal “run tumble” bias.E. colibacteria taken from a swarm exhibit more highly extended runs (low tumble bias) and higher speeds thanE. colibacteria swimming individually in a liquid medium. The stability of the signaling protein CheZ is higher in swarmers, consistent with the observed elevation of CheZ levels and with the low tumble bias. We show that the tumble bias displayed by wild-type swarmers is the optimal bias for maximizing swarm expansion. In assays performed in liquid, swarm cells have reduced chemotactic performance. This behavior is specific to swarming, is not specific to growth on surfaces, and persists for a generation. Therefore, the chemotaxis signaling pathway is reprogrammed for swarming.IMPORTANCEThe fundamental motile behavior ofE. coliis a random walk, where straight “runs” are punctuated by “tumbles.” This behavior, conferred by the chemotaxis signaling system, is used to track chemical gradients in liquid. Our study results show that when migrating collectively on surfaces,E. colimodifies its chemosensory physiology to decrease its tumble bias (and hence to increase run durations) by post-transcriptional changes that alter the levels of a key signaling protein. We speculate that the low tumble bias may contribute to the observed Lévy walk (LW) trajectories within the swarm, where run durations have a power law distribution. In animals, LW patterns are hypothesized to maximize searches in unpredictable environments. Swarming bacteria face several challenges while moving collectively over a surface—maintaining cohesion, overcoming constraints imposed by a physical substrate, searching for nutrients as a group, and surviving lethal levels of antimicrobials. The altered chemosensory behavior that we describe in this report may help with these challenges.

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Chatterjee, Purba, and Nigel Goldenfeld. "Field-theoretic model for chemotaxis in run and tumble particles." Physical Review E 103, no. 3 (March 4, 2021). http://dx.doi.org/10.1103/physreve.103.032603.

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Mears, Patrick J., Santosh Koirala, Chris V. Rao, Ido Golding, and Yann R. Chemla. "Escherichia coli swimming is robust against variations in flagellar number." eLife 3 (February 11, 2014). http://dx.doi.org/10.7554/elife.01916.

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Bacterial chemotaxis is a paradigm for how environmental signals modulate cellular behavior. Although the network underlying this process has been studied extensively, we do not yet have an end-to-end understanding of chemotaxis. Specifically, how the rotational states of a cell’s flagella cooperatively determine whether the cell ‘runs’ or ‘tumbles’ remains poorly characterized. Here, we measure the swimming behavior of individual E. coli cells while simultaneously detecting the rotational states of each flagellum. We find that a simple mathematical expression relates the cell’s run/tumble bias to the number and average rotational state of its flagella. However, due to inter-flagellar correlations, an ‘effective number’ of flagella—smaller than the actual number—enters into this relation. Data from a chemotaxis mutant and stochastic modeling suggest that fluctuations of the regulator CheY-P are the source of flagellar correlations. A consequence of inter-flagellar correlations is that run/tumble behavior is only weakly dependent on number of flagella.

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Partridge, Jonathan D., Nguyen T. Q. Nhu, Yann S. Dufour, and Rasika M. Harshey. "Tumble Suppression Is a Conserved Feature of Swarming Motility." mBio 11, no. 3 (June 16, 2020). http://dx.doi.org/10.1128/mbio.01189-20.

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ABSTRACT Many bacteria use flagellum-driven motility to swarm or move collectively over a surface terrain. Bacterial adaptations for swarming can include cell elongation, hyperflagellation, recruitment of special stator proteins, and surfactant secretion, among others. We recently demonstrated another swarming adaptation in Escherichia coli, wherein the chemotaxis pathway is remodeled to decrease tumble bias (increase run durations), with running speeds increased as well. We show here that the modification of motility parameters during swarming is not unique to E. coli but is shared by a diverse group of bacteria we examined—Proteus mirabilis, Serratia marcescens, Salmonella enterica, Bacillus subtilis, and Pseudomonas aeruginosa—suggesting that increasing run durations and speeds are a cornerstone of swarming. IMPORTANCE Bacteria within a swarm move characteristically in packs, displaying an intricate swirling motion in which hundreds of dynamic rafts continuously form and dissociate as the swarm colonizes an increasing expanse of territory. The demonstrated property of E. coli to reduce its tumble bias and hence increase its run duration during swarming is expected to maintain and promote side-by-side alignment and cohesion within the bacterial packs. In this study, we observed a similar low tumble bias in five different bacterial species, both Gram positive and Gram negative, each inhabiting a unique habitat and posing unique problems to our health. The unanimous display of an altered run-tumble bias in swarms of all species examined in this investigation suggests that this behavioral adaptation is crucial for swarming.

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Jakuszeit, Theresa, James Lindsey-Jones, François J. Peaudecerf, and Ottavio A. Croze. "Migration and accumulation of bacteria with chemotaxis and chemokinesis." European Physical Journal E 44, no. 3 (March 2021). http://dx.doi.org/10.1140/epje/s10189-021-00009-w.

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Abstract Bacteria can chemotactically migrate up attractant gradients by controlling run-and-tumble motility patterns. In addition to this well-known chemotactic behaviour, several soil and marine bacterial species perform chemokinesis; they adjust their swimming speed according to the local concentration of chemoeffector, with higher speed at higher concentration. A field of attractant then induces a spatially varying swimming speed, which results in a drift towards lower attractant concentrations—contrary to the drift created by chemotaxis. Here, to explore the biological benefits of chemokinesis and investigate its impact on the chemotactic response, we extend a Keller–Segel-type model to include chemokinesis. We apply the model to predict the dynamics of bacterial populations capable of chemokinesis and chemotaxis in chemoeffector fields inspired by microfluidic and agar plate migration assays. We find that chemokinesis combined with chemotaxis not only may enhance the population response with respect to pure chemotaxis, but also modifies it qualitatively. We conclude presenting predictions for bacteria around dynamic finite-size nutrient sources, simulating, e.g. a marine particle or a root. We show that chemokinesis can reduce the measuring bias that is created by a decaying attractant gradient. Graphic abstract

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Vourc'h, Thomas, Julien Léopoldès, and Hassan Peerhossaini. "Light Control of the Diffusion Coefficient of Active Fluids." Journal of Fluids Engineering 142, no. 3 (February 3, 2020). http://dx.doi.org/10.1115/1.4045951.

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Abstract Active fluids refer to the fluids that contain self-propelled particles such as bacteria or microalgae, whose properties differ fundamentally from the passive fluids. Such particles often exhibit an intermittent motion, with high-motility “run” periods broken by low-motility “tumble” periods. The average motion can be modified with external stresses, such as nutrient or light gradients, leading to a directed movement called chemotaxis and phototaxis, respectively. Using cyanobacterium Synechocystis sp. PCC 6803, a model microorganism to study photosynthesis, we track the bacterial response to light stimuli, under isotropic and nonisotropic (directional) conditions. In particular, we investigate how the intermittent motility is influenced by illumination. We find that just after a rise in light intensity, the probability to be in the run state increases. This feature vanishes after a typical characteristic time of about 1 h, when initial probability is recovered. Our results are well described by a mathematical model based on the linear response theory. When the perturbation is anisotropic, we observe a collective motion toward the light source (phototaxis). We show that the bias emerges due to more frequent runs in the direction of the light, whereas the run durations are longer whatever the direction.

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Findlay, Rachel C., Mohamed Osman, Kirstin A. Spence, Paul M. Kaye, Pegine B. Walrad, and Laurence G. Wilson. "High-speed, three-dimensional imaging reveals chemotactic behaviour specific to human-infective Leishmania parasites." eLife 10 (June 28, 2021). http://dx.doi.org/10.7554/elife.65051.

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Cellular motility is an ancient eukaryotic trait, ubiquitous across phyla with roles in predator avoidance, resource access, and competition. Flagellar motility is seen in various parasitic protozoans, and morphological changes in flagella during the parasite life cycle have been observed. We studied the impact of these changes on motility across life cycle stages, and how such changes might serve to facilitate human infection. We used holographic microscopy to image swimming cells of different Leishmania mexicana life cycle stages in three dimensions. We find that the human-infective (metacyclic promastigote) forms display ‘run and tumble’ behaviour in the absence of stimulus, reminiscent of bacterial motion, and that they specifically modify swimming direction and speed to target host immune cells in response to a macrophage-derived stimulus. Non-infective (procyclic promastigote) cells swim more slowly, along meandering helical paths. These findings demonstrate adaptation of swimming phenotype and chemotaxis towards human cells.

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Kirkegaard, Julius B., Ambre Bouillant, Alan O. Marron, Kyriacos C. Leptos, and Raymond E. Goldstein. "Aerotaxis in the closest relatives of animals." eLife 5 (November 24, 2016). http://dx.doi.org/10.7554/elife.18109.

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As the closest unicellular relatives of animals, choanoflagellates serve as useful model organisms for understanding the evolution of animal multicellularity. An important factor in animal evolution was the increasing ocean oxygen levels in the Precambrian, which are thought to have influenced the emergence of complex multicellular life. As a first step in addressing these conditions, we study here the response of the colony-forming choanoflagellate Salpingoeca rosetta to oxygen gradients. Using a microfluidic device that allows spatio-temporal variations in oxygen concentrations, we report the discovery that S. rosetta displays positive aerotaxis. Analysis of the spatial population distributions provides evidence for logarithmic sensing of oxygen, which enhances sensing in low oxygen neighborhoods. Analysis of search strategy models on the experimental colony trajectories finds that choanoflagellate aerotaxis is consistent with stochastic navigation, the statistics of which are captured using an effective continuous version based on classical run-and-tumble chemotaxis.

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Kinosita, Yoshiaki, Tsubasa Ishida, Myu Yoshida, Rie Ito, Yusuke V. Morimoto, Kazuki Goto, Richard M. Berry, Takayuki Nishizaka, and Yoshiyuki Sowa. "Distinct chemotactic behavior in the original Escherichia coli K-12 depending on forward-and-backward swimming, not on run-tumble movements." Scientific Reports 10, no. 1 (September 28, 2020). http://dx.doi.org/10.1038/s41598-020-72429-1.

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Abstract Most motile bacteria are propelled by rigid, helical, flagellar filaments and display distinct swimming patterns to explore their favorable environments. Escherichia coli cells have a reversible rotary motor at the base of each filament. They exhibit a run-tumble swimming pattern, driven by switching of the rotational direction, which causes polymorphic flagellar transformation. Here we report a novel swimming mode in E. coli ATCC10798, which is one of the original K-12 clones. High-speed tracking of single ATCC10798 cells showed forward and backward swimming with an average turning angle of 150°. The flagellar helicity remained right-handed with a 1.3 μm pitch and 0.14 μm helix radius, which is consistent with the feature of a curly type, regardless of motor switching; the flagella of ATCC10798 did not show polymorphic transformation. The torque and rotational switching of the motor was almost identical to the E. coli W3110 strain, which is a derivative of K-12 and a wild-type for chemotaxis. The single point mutation of N87K in FliC, one of the filament subunits, is critical to the change in flagellar morphology and swimming pattern, and lack of flagellar polymorphism. E. coli cells expressing FliC(N87K) sensed ascending a chemotactic gradient in liquid but did not spread on a semi-solid surface. Based on these results, we concluded that a flagellar polymorphism is essential for spreading in structured environments.

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Journal articles on the topic 'Run-and-tumble chemotaxis'

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