Bacterial Tracking of Motile Algae Assisted by Algal Cell’s Vorticity Field

Locsei, J. T.; Pedley, T. J.

doi:10.1007/s00248-008-9468-6

Cited by 15 publications

(12 citation statements)

References 46 publications

(63 reference statements)

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“…2B, Inset and Table S1). This result is in line with predictions from recent theoretical models for E. coli and V. alginolyticus (18,20) and, to the best of our knowledge, represents the first experimental quantification of the dependence of the chemotactic velocity on the swimming speed. The steady-state chemotactic velocities ranged from V C = 0.2-3.5 μm/s (Fig.…”

Section: Strong Chemotaxis At High Swimming Speeds Results From Reducedsupporting

confidence: 91%

Speed-dependent chemotactic precision in marine bacteria

Son

Menolascina

Stocker

2016

Proc. Natl. Acad. Sci. U.S.A.

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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°r eversals 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 populationlevel 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.otility is an essential component of chemotaxis (1), the ability of organisms to sense chemical gradients and swim toward more favorable conditions, for example, to find dissolved or particulate nutrients, colonize and infect hosts, or evade noxious substances (2). Most of our knowledge of bacterial chemotaxis comes from the study of Escherichia coli, a bacterium that inhabits the lower intestine of warm-blooded animals and swims using multiple (4-10) flagella (2). Counterclockwise (CCW) rotation of all motors causes the flagella to bundle and to propel the cell into a nearly straight "run" at 10-30 μm/s (2). A change in swimming direction occurs when one or more motors switch to clockwise (CW) rotation, disrupting the flagellar bundle and leading to a nearly random reorientation or "tumble" (2). The key to success in E. coli's chemotaxis strategy is the bacterium's ability to control the switching frequency between CCW and CW flagellar rotation, giving rise to the well-known run-and-tumble swimming pattern (2). In this process, the swimming speed remains largely unchanged, and despite the bacterium's ability to sense mechanical stimuli (3), it is generally held that its chemotaxis depends only on the sensing of chemical stimuli. Consequently, the swimming speed has not been considered to af...

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Section: Strong Chemotaxis At High Swimming Speeds Results From Reducedsupporting

confidence: 91%

Speed-dependent chemotactic precision in marine bacteria

Son

Menolascina

Stocker

2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Yet our results suggest that the diversity in a population should be extremely weak in the integral of the response γ and stronger in the memory λ and the running time τ r . Indeed, variations in the rotational diffusivity D of individual bacteria are expected at the level of both thermal (6) and mechanical (39) contributions. It is known that the diversity of τ r is appreciable; it will be of interest to gather experimental data on the correlations among variations in τ r and those in D and λ.…”

Section: Discussionmentioning

confidence: 99%

Bacterial strategies for chemotaxis response

Celani

Vergassola

2010

Proc. Natl. Acad. Sci. U.S.A.

185

228

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Regular environmental conditions allow for the evolution of specifically adapted responses, whereas complex environments usually lead to conflicting requirements upon the organism's response. A relevant instance of these issues is bacterial chemotaxis, where the evolutionary and functional reasons for the experimentally observed response to chemoattractants remain a riddle. Sensing and motility requirements are in fact optimized by different responses, which strongly depend on the chemoattractant environmental profiles. It is not clear then how those conflicting requirements quantitatively combine and compromise in shaping the chemotaxis response. Here we show that the experimental bacterial response corresponds to the maximin strategy that ensures the highest minimum uptake of chemoattractants for any profile of concentration. We show that the maximin response is the unique one that always outcompetes motile but nonchemotactic bacteria. The maximin strategy is adapted to the variable environments experienced by bacteria, and we explicitly show its emergence in simulations of bacterial populations in a chemostat. Finally, we recast the contrast of evolution in regular vs. complex environments in terms of minimax vs. maximin game-theoretical strategies. Our results are generally relevant to biological optimization principles and provide a systematic possibility to get around the need to know precisely the statistics of environmental fluctuations.biological optimization | E. coli | evolution | game theory | strategy

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“…This is the case for sinking marine snow particles and fecal pellets (93) but potentially also for swimming phytoplankton cells (19,108). The release of solutes, coupled with the movement relative to the water, distorts the otherwise nearly spherical diffusion boundary layer into a cometlike plume ( Fig.…”

Section: Ephemeral Nutrient Pulsesmentioning

confidence: 99%

“…Consequently, these experimental observations indicate that the chemosensory capabilities of marine bacteria may exceed what previous theory had predicted. However, while this impressive "chasing" ability was initially attributed to chemotaxis alone, one subsequent theoretical study has suggested that the origin of the phenomenon might be purely hydrodynamic, whereby the fluid velocity gradients in the wake of the swimming alga reorient bacteria so that they remain in the wake (108). While this remains an interesting possibility, the very sharp turns executed by the chasing bacteria still suggest an active behavior, leaving this topic open for further investigation.…”

Section: Chemotaxis Toward Phytoplanktonmentioning

confidence: 99%

Ecology and Physics of Bacterial Chemotaxis in the Ocean

Stocker

Seymour

2012

Microbiol Mol Biol Rev

248

214

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SUMMARYIntuitively, it may seem that from the perspective of an individual bacterium the ocean is a vast, dilute, and largely homogeneous environment. Microbial oceanographers have typically considered the ocean from this point of view. In reality, marine bacteria inhabit a chemical seascape that is highly heterogeneous down to the microscale, owing to ubiquitous nutrient patches, plumes, and gradients. Exudation and excretion of dissolved matter by larger organisms, lysis events, particles, animal surfaces, and fluxes from the sediment-water interface all contribute to create strong and pervasive heterogeneity, where chemotaxis may provide a significant fitness advantage to bacteria. The dynamic nature of the ocean imposes strong selective pressures on bacterial foraging strategies, and many marine bacteria indeed display adaptations that characterize their chemotactic motility as “high performance” compared to that of enteric model organisms. Fast swimming speeds, strongly directional responses, and effective turning and steering strategies ensure that marine bacteria can successfully use chemotaxis to very rapidly respond to chemical gradients in the ocean. These fast responses are advantageous in a broad range of ecological processes, including attaching to particles, exploiting particle plumes, retaining position close to phytoplankton cells, colonizing host animals, and hovering at a preferred height above the sediment-water interface. At larger scales, these responses can impact ocean biogeochemistry by increasing the rates of chemical transformation, influencing the flux of sinking material, and potentially altering the balance of biomass incorporation versus respiration. This review highlights the physical and ecological processes underpinning bacterial motility and chemotaxis in the ocean, describes the current state of knowledge of chemotaxis in marine bacteria, and summarizes our understanding of how these microscale dynamics scale up to affect ecosystem-scale processes in the sea.

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Bacterial Tracking of Motile Algae Assisted by Algal Cell’s Vorticity Field

Cited by 15 publications

References 46 publications

Speed-dependent chemotactic precision in marine bacteria

Speed-dependent chemotactic precision in marine bacteria

Bacterial strategies for chemotaxis response

Ecology and Physics of Bacterial Chemotaxis in the Ocean

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