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Register a new userSynchrony and symmetry-breaking in active flagellar coordination
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Authors
Kirsty Y. Wan
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Living creatures exhibit a remarkable diversity of locomotion mechanisms, evolving structures specialised for interacting with their environment. In the vast majority of cases, locomotor behaviours such as flying, crawling, and running, are orchestrated by nervous systems. Surprisingly, microorganisms can enact analogous movement gaits for swimming using multiple, fast-moving cellular protrusions called cilia and flagella. Here, I demonstrate intermittency, reversible rhythmogenesis, and gait mechanosensitivity in algal flagella, to reveal the active nature of locomotor patterning. In addition to maintaining free-swimming gaits, I show that the algal flagellar apparatus functions as a central pattern generator which encodes the beating of each flagellum in a network in a distinguishable manner. The latter provides a novel symmetry-breaking mechanism for cell reorientation. These findings imply that the capacity to generate and coordinate complex locomotor patterns does not require neural circuitry but rather the minimal ingredients are present in simple unicellular organisms.
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The flexibility of the bacterial flagellar hook is believed to have substantial consequences for microorganism locomotion. Using a simplified model of a rigid flagellum and a flexible hook, we show that the paths of axisymmetric cell bodies driven by a single flagellum in Stokes flow are generically helical. Phase-averaged resistance and mobility tensors are produced to describe the flagellar hydrodynamics, and a helical rod model which retains a coupling between translation and rotation is identified as a distinguished asymptotic limit. A supercritical Hopf bifurcation in the flagellar orientation beyond a critical ratio of flagellar motor torque to hook bending stiffness, which is set by the spontaneous curvature of the flexible hook, the shape of the cell body, and the flagellum geometry, can have a dramatic effect on the cells trajectory through the fluid. Although the equilibrium hook angle can result in a wide variance in the trajectorys helical pitch, we find a very consistent prediction for the trajectorys helical amplitude using parameters relevant to swimming P. aeruginosa cells.
The near-surface swimming patterns of bacteria are strongly determined by the hydrodynamic interactions between bacteria and the surface, which trap bacteria in smooth circular trajectories that lead to inefficient surface exploration. Here, we show by combining experiments and a data-driven mathematical model that surface exploration of enterohemorrhagic Escherichia coli (EHEC) -- a pathogenic strain of E. coli causing serious illnesses such as bloody diarrhea -- results from a complex interplay between motility and transient surface adhesion events. These events allow EHEC to break the smooth circular trajectories and regulate their transport properties by the use stop-adhesion events that lead to a characteristic intermittent motion on surfaces. We find that the experimentally measured frequency of stop-adhesion events in EHEC is located at the value predicted by the developed mathematical model that maximizes bacterial surface diffusivity. We indicate that these results and the developed model apply to other bacterial strains on different surfaces, which suggests that swimming bacteria use transient adhesion to regulate surface motion.
In a classic paper, Edward Purcell analysed the dynamics of flagellated bacterial swimmers and derived a geometrical relationship which optimizes the propulsion efficiency. Experimental measurements for wild-type bacterial species E. coli have revealed that they closely satisfy this geometric optimality. However, the dependence of the flagellar motor speed on the load and more generally the role of the torque-speed characteristics of the flagellar motor is not considered in Purcells original analysis. Here we derive a tuned condition representing a match between the flagella geometry and the torque-speed characteristics of the flagellar motor to maximize the bacterial swimming speed for a given load. This condition is independent of the geometric optimality condition derived by Purcell and interestingly this condition is not satisfied by wild-type E. coli which swim 2-3 times slower than the maximum possible speed given the amount of available motor torque. Our analysis also reveals the existence of an anomalous propulsion regime, where the swim speed increases with increasing load (drag). Finally, we present experimental data which supports our analysis.
Groups of beating flagella or cilia often synchronize so that neighboring filaments have identical frequencies and phases. A prime example is provided by the unicellular biflagellate Chlamydomonas reinhardtii, which typically displays synchronous in-phase beating in a low-Reynolds number version of breaststroke swimming. We report here the discovery that ptx1, a flagellar dominance mutant of C. reinhardtii, can exhibit synchronization in precise antiphase, as in the freestyle swimming stroke. Long-duration high-speed imaging shows that ptx1 flagella switch stochastically between in-phase and antiphase states, and that the latter has a distinct waveform and significantly higher frequency, both of which are strikingly similar to those found during phase slips that stochastically interrupt in-phase beating of the wildtype. Possible mechanisms underlying these observations are discussed.
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