Publications

2006
Luo, L., Clark, D., Biron, D., Mahadevan, L. & Samuel, A. Sensorimotor control during isothermal tracking in Caenorhabditis elegans. Journal of Experimental Biology 209, 23, 4652-4662 (2006). WebsiteAbstract
In order to purposefully navigate their environments, animals rely on precise coordination between their sensory and motor systems. The integrated performance of circuits for sensorimotor control may be analyzed by quantifying an animal's motile behavior in defined sensory environments. Here,we analyze the ability of the nematode C. elegans to crawl isothermally in spatial thermal gradients by quantifying the trajectories of individual worms responding to defined spatiotemporal thermal gradients. We show that sensorimotor control during isothermal tracking may be summarized as a strategy in which the worm changes the curvature of its propulsive undulations in response to temperature changes measured at its head. We show that a concise mathematical model for this strategy for sensorimotor control is consistent with the exquisite stability of the worm's isothermal alignment in spatial thermal gradients as well as its more complex trajectories in spatiotemporal thermal gradients.
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2005
Samuel, A. & Sengupta, P. Sensorimotor integration: locating locomotion in neural circuits. Current Biology 15, 9, R341-R343 (2005). Publisher's VersionAbstract
Neural components of the circuits that transform sensory cues into changes in motor activities are largely unknown. Several recent studies have now functionally mapped the sensorimotor circuits responsible for locomotion behaviors under defined environmental conditions in the nematode Caenorhabditis elegans.
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2004
Colosimo, M., et al. Identification of Thermosensory and Olfactory Neuron-Specific Genes via Expression Profiling of Single Neuron Types. Current Biology 14, 24, 2245-2251 (2004). Publisher's VersionAbstract
Most C. elegans sensory neuron types consist of a single bilateral pair of neurons, and respond to a unique set of sensory stimuli. Although genes required for the development and function of individual sensory neuron types have been identified in forward genetic screens, these approaches are unlikely to identify genes that when mutated result in subtle or pleiotropic phenotypes. Here, we describe a complementary approach to identify sensory neuron type-specific genes via microarray analysis using RNA from sorted AWB olfactory and AFD thermosensory neurons. The expression patterns of subsets of these genes were further verified in vivo. Genes identified by this analysis encode 7-transmembrane receptors, kinases, and nuclear factors including dac-1, which encodes a homolog of the highly conserved Dachshund protein [1]dac-1 is expressed in a subset of sensory neurons including the AFD neurons and is regulated by the TTX-1 OTX homeodomain protein [2]. On thermal gradients, dac-1 mutants fail to suppress a cryophilic drive but continue to track isotherms at the cultivation temperature, representing the first genetic separation of these AFD-mediated behaviors. Expression profiling of single neuron types provides a rapid, powerful, and unbiased method for identifying neuron-specific genes whose functions can then be investigated in vivo.
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2003
Samuel, A.D.T., Silva, R.A. & Murthy, V.N. Synaptic Activity of the AFD Neuron inCaenorhabditis elegans Correlates with Thermotactic Memory. Journal of Neuroscience 23, 2, 373–376 (2003). Publisher's VersionAbstract
Thermotactic behavior in Caenorhabditis elegans is sensitive to both a worm’s ambient temperature (Tamb) and its memory of the temperature of its cultivation (Tcult). The AFD neuron is part of a neural circuit that underlies thermotactic behavior. By monitoring the fluorescence of pH-sensitive green fluorescent protein localized to synaptic vesicles, we measured the rate of the synaptic release of AFD in worms cultivated at temperatures between 15 and 25°C, and subjected to fixed, ambient temperatures in the same range. We found that the rate of AFD synaptic release is high if either Tamb >Tcult orTamb <Tcult, but AFD synaptic release is low if Tamb ≅Tcult. This suggests that AFD encodes a direct comparison between Tamb andTcult.
2001
Samuel, A.D.T., Murthy, V.N. & Hengartner, M.O. Calcium dynamics during fertilization in C. elegans. BMC Developmental Biology 1, 8 (2001). Publisher's VersionAbstract
Of the animals typically used to study fertilization-induced calcium dynamics, none is as accessible to genetics and molecular biology as the model organism Caenorhabditis elegans. Motivated by the experimental possibilities inherent in using such a well-established model organism, we have characterized fertilization-induced calcium dynamics in C. elegans.
bmc_developmental_2001.pdf
Samuel, A.D.T., Peterson, J.D. & Reese, T.S. Envelope structure of Synechococcus sp. WH8113, a nonflagellated swimming cyanobacterium. BMC Microbiology 1, 4 (2001). Publisher's VersionAbstract
Many bacteria swim by rotating helical flagellar filaments [1]. Waterbury et al. [15] discovered an exception, strains of the cyanobacterium Synechococcus that swim without flagella or visible changes in shape. Other species of cyanobacteria glide on surfaces [2,7]. The hypothesis that Synechococcus might swim using traveling surface waves [6,13] prompted this investigation.
bmc_microbiology_2001.pdf
1999
Turner, L., Samuel, A.D.T., Stern, A.S. & Berg, H.C. Temperature Dependence of Switching of the Bacterial Flagellar Motor by the Protein CheY13DK106YW. Biophysical Journal 77, 1, 597-603 (1999). Publisher's VersionAbstract
The behavior of the bacterium Escherichia coli is controlled by switching of the flagellar rotary motor between the two rotational states, clockwise (CW) and counterclockwise (CCW). The molecular mechanism for switching remains unknown, but binding of the response regulator CheY-P to the motor component FliM enhances CW rotation. This effect is mimicked by the unphosphorylated double mutant CheY13DK106YW (CheY**). To learn more about switching, we measured the fraction of time that a motor spends in the CW state (the CW bias) at different concentrations of CheY** and at different temperatures. From the CW bias, we computed the standard free energy change of switching. In the absence of CheY, this free energy change is a linear function of temperature (Turner et al., 1996. Biophys. J. 71:2227–2233). In the presence of CheY**, it is nonlinear. However, the data can be fit by models in which binding of each molecule of CheY** shifts the difference in free energy between CW and CCW states by a fixed amount. The shift increases linearly from ∼0.3kT per molecule at 5°C to ∼0.9kT at 25°C, where k is Boltzmann's constant and T is 289 Kelvin (= 16°C). The entropy and enthalpy contributions to this shift are about −0.031kT/°C and 0.10kT, respectively.
turner_biophysical_1999.pdf
Samuel, A.D.T., et al. Flagellar determinants of bacterial sensitivity to χ-phage. Proceedings of the National Academy of Sciences 96, 17, 9863–9866 (1999). Publisher's VersionAbstract
Bacteriophage χ is known to infect motile strains of enteric bacteria by adsorbing randomly along the length of a flagellar filament and then injecting its DNA into the bacterial cell at the filament base. Here, we provide evidence for a “nut and bolt” model for translocation of phage along the filament: the tail fiber of χ fits the grooves formed by helical rows of flagellin monomers, and active flagellar rotation forces the phage to follow the grooves as a nut follows the threads of a bolt.
pnas_1999.pdf
Mahadevan, L., Ryu, W.S. & Samuel, A.D.T. Tumbling cards. Physics of Fluids 11, 1, 1-3 (1999). Publisher's VersionAbstract
When a stiff rectangular card is dropped in still air with its long axis horizontal, it often settles into a regular mode of motion; while revolving around its long axis it descends along a path that is inclined to the vertical at a nearly constant angle. We show experimentally that the tumbling frequency Omega of a card of length \(l\), width \(w\) and thickness \(d (l≫w≫d)(l≫w≫d)\) scales as Omega ~ d1/2w-1, consistent with a simple dimensional argument that balances the drag against gravity.
physics_of_fluids_1999.pdf
1998
Mahadevan, L., Ryu, W.S. & Samuel, A.D.T. Fluid ‘rope trick’ investigated . Nature 392, 140, (1998). Publisher's VersionAbstract
Buckling instabilities can arise from competition between axial compression and bending in slender objects. These are not restricted to solids, but also occur with fluids with free surfaces1,4, in geophysics5 and in materials processing6. Here we consider a classic demonstration of fluid buckling7.
nature_1998.pdf
1997
Samuel, A.D.T. & Berg, H.C. Statistical kinetics of the bacterial flagellar motor. Physical Review E 55, 6, 7801-7804 (1997). Publisher's VersionAbstract
The statistical behavior of the bacterial flagellar motor matches that of a Poisson stepper that takes at least 400 steps per revolution. Using this fact, we study the effect of motor stochastics on experiments in which fluorescent motors, initially synchronized by polarization photobleaching, become uncorrelated.
physreve.55.7801_1997.pdf
1996
Stone, H.A. & Samuel, A.D.T. Propulsion of Microorganisms by Surface Distortions. Physical Review Letters 77, 19, 4102-4104 (1996). Publisher's VersionAbstract
Swimming strategies of microorganisms must conform to the principles of self-propulsion at low Reynolds numbers. Here we relate the translational and rotational speeds to the surface motions of a swimmer and, for spheres, make evident novel constraints on mechanisms for propulsion. The results are applied to a cyanobacterium, an organism whose motile mechanism is unknown, by considering incompressible streaming of the cell surface and oscillatory, tangential surface deformations. Finally, swimming efficiency using tangential motions is related to the surface velocities and a bound on the efficiency is obtained.
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Samuel, A.D. & Berg, H.C. Torque-generating units of the bacterial flagellar motor step independently. Biophysical Journal 71, 2, 918-923 (1996). Publisher's VersionAbstract
Measurements of the variance in rotation period of tethered cells as a function of mean rotation rate have shown that the flagellar motor of Escherichia coli is a stepping motor. Here, by measurement of the variance in rotation period as a function of the number of active torque-generating units, it is shown that each unit steps independently.
Ehlers, K.M., Samuel, A.D., Berg, H.C. & Montgomery, R. Do cyanobacteria swim using traveling surface waves?. Proceedings of the National Academy of Sciences 93, 16, 8340–8343 (1996). Publisher's VersionAbstract
Bacteria that swim without the benefit of flagella might do so by generating longitudinal or transverse surface waves. For example, swimming speeds of order 25 microns/s are expected for a spherical cell propagating longitudinal waves of 0.2 micron length, 0.02 micron amplitude, and 160 microns/s speed. This problem was solved earlier by mathematicians who were interested in the locomotion of ciliates and who considered the undulations of the envelope swept out by ciliary tips. A new solution is given for spheres propagating sinusoidal waveforms rather than Legendre polynomials. The earlier work is reviewed and possible experimental tests are suggested.
1995
Samuel, A.D. & Berg, H.C. Fluctuation analysis of rotational speeds of the bacterial flagellar motor. Proceedings of the National Academy of Sciences 92, 8, 3502–3506 (1995). Publisher's VersionAbstract
We measured the dependence of the variance in the rotation rate of tethered cells of Escherichia coli on the mean rotation rate over a regime in which the motor generates constant torque. This dependence was compared with that of broken motors. In either case, motor torque was augmented with externally applied torque. We show that, in contrast to broken motors, functioning motors in this regime do not freely rotationally diffuse and that the variance measurements are consistent with the predicted values of a stepping mechanism with exponentially distributed waiting times (a Poisson stepper) that steps approximately 400 times per revolution.

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