Time Irreversibility and Criticality in the Motility of a Flagellate Microorganism

Wan, Kirsty Y.; Goldstein, Raymond E.

doi:10.1103/physrevlett.121.058103

Cited by 58 publications

(87 citation statements)

References 41 publications

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“…It is suggested that the primordium-facing membranelles act as pacemakers [34]. As in some species of algal multiflagellates [36,37], calcium signalling via contractile elements can dynamically reverse the beating direction of the membranelles [38]. Addition of digitoxin and other chemicals directly modulates intermembranellar connectivity leading to a change in MCW wave velocity but affects the beat frequencies to a lesser extent [39].…”

Section: (B) Infraciliature and Hydrodynamic Interactionsmentioning

confidence: 99%

Reorganization of complex ciliary flows around regeneratingStentor coeruleus

Wan

Hürlimann

Fenix

et al. 2019

Phil. Trans. R. Soc. B

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The phenomenon of ciliary coordination has garnered increasing attention in recent decades and multiple theories have been proposed to explain its occurrence in different biological systems. While hydrodynamic interactions are thought to dictate the large-scale coordinated activity of epithelial cilia for fluid transport, it is rather basal coupling that accounts for synchronous swimming gaits in model microeukaryotes such as Chlamydomonas. Unicellular ciliates present a fascinating yet understudied context in which coordination is found to persist in ciliary arrays positioned across millimetre scales on the same cell. Here, we focus on the ciliate Stentor coeruleus , chosen for its large size, complex ciliary organization, and capacity for cellular regeneration. These large protists exhibit ciliary differentiation between cortical rows of short body cilia used for swimming, and an anterior ring of longer, fused cilia called the membranellar band (MB). The oral cilia in the MB beat metachronously to produce strong feeding currents. Remarkably, upon injury, the MB can be shed and regenerated de novo. Here, we follow and track this developmental sequence in its entirety to elucidate the emergence of coordinated ciliary beating: from band formation, elongation, curling and final migration towards the cell anterior. We reveal a complex interplay between hydrodynamics and ciliary restructuring in Stentor , and highlight for the first time the importance of a ring-like topology for achieving long-range metachronism in ciliated structures. This article is part of the Theo Murphy meeting issue ‘Unity and diversity of cilia in locomotion and transport’.

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Section: (B) Infraciliature and Hydrodynamic Interactionsmentioning

confidence: 99%

Reorganization of complex ciliary flows around regeneratingStentor coeruleus

Wan

Hürlimann

Fenix

et al. 2019

Phil. Trans. R. Soc. B

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“…Knowledge of this beat could provide hitherto untapped information for the estimation of non-visible attributes such as the contribution of different metabolic path-ways, and modulation in response to the physical and biochemical environments (Ooi et al, 2014). The capability to capture flagellar movements and associated mechanistic insights has broader applicability in the life sciences including the role of cilia in embryonic development (Smith et al, 2019), swimming of multiflagellate microorganisms (Wan and Goldstein, 2018), the use of high-speed holographic microscopy to image the flagellar waveforms of malaria parasites (Wilson et al, 2013), and even the design of hybrid bio-robots for biomedical applications (Xu et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Rapid sperm capture: High-throughput flagellar waveform analysis

Gallagher

Cupples

Ooi

et al. 2019

Preprint

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The FAST software package and all documentation can be downloaded from www.flagellarCapture.com. Summary 1 Flagella are critical across all eukaryotic life, and the human sperm 2 flagellum is crucial to natural fertility. Existing automated sperm di-3 agnostics (CASA) rely on tracking the sperm head and extrapolating 4 measures. We describe fully-automated tracking and analysis of flag-5 ellar movement for large cell numbers. The analysis is demonstrated 6 on freely-motile cells in low and high viscosity fluids, and validated on 7 published data of tethered cells undergoing pharmacological hyperac-8 tivation. Direct analysis of the flagellar beat reveals that the CASA 9 measure 'beat cross frequency', does not measure beat frequency. A 10 new measurement, track centroid speed, is validated as an accurate 11 differentiator of progressive motility. Coupled with fluid mechanics 12 codes, waveform data enables extraction of experimentally intractable 13 quantities such as energy dissipation, disturbance of the surrounding 14 medium and viscous stresses. We provide a powerful and accessible 15 research tool, enabling connection of the cell's mechanical activity to 16 its motility and effect on its environment. 17 Introduction 18About 100 million men worldwide are suggested to be subfertile (Inhorn and 19 Patrizio, 2015), but for many of them an accurate diagnostic cause remains 20 elusive. The ability of sperm to successfully migrate through the female re-21 productive tract is key to natural fertilisation, however current techniques for 22 assessing sperm motility lack diagnostic power and mechanistic insight. The 23 heterogeneity of human sperm requires tools that can acquire and analyse 24 2 (2018) and associated special issue). Such systems are widely used for vet-25 erinary work and in domestic animal breeding, conservation, and toxicology 26 (Amann and Waberski, 2014), but have not yet made the breakthrough into 27 routine clinical usage. The reasons for this have been discussed elsewhere 28 (Gallagher et al., 2018b). 29 Standard CASA systems produce a motility assessment from the track of 30 the head movement, however this does not enable causative or mechanistic 31 insight because it lacks detail on the movement of the flagellum. Knowledge 32 of this beat could provide hitherto untapped information for the estimation 33 of non-visible attributes such as the contribution of different metabolic path-34 ways, and modulation in response to the physical and biochemical environ-35 ments (Ooi et al., 2014). The capability to capture flagellar movements and 36 associated mechanistic insights has broader applicability in the life sciences 37 including the role of cilia in embryonic development (Smith et al., 2019), 38 swimming of multiflagellate microorganisms (Wan and Goldstein, 2018), the 39 use of high-speed holographic microscopy to image the flagellar waveforms 40 of malaria parasites (Wilson et al., 2013), and even the design of hybrid 41 bio-robots for biomedical applications (Xu et al., 2017).42 The use of comp...

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“…For the same cell, beating can be restricted to a subset of flagella with the remaining flagella quiescent. Asymmetries arising from the actively beating In (e), the octoflagellate Pyramimonas octopus undergoes reorientation following a shock response (see also [26]). (f) A P. parkeae cell presenting a single actively beating flagellum.…”

Section: Gait-switching and Partial-activationmentioning

confidence: 99%

Synchrony and symmetry-breaking in active flagellar coordination

Wan

2019

Phil. Trans. R. Soc. B

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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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Time Irreversibility and Criticality in the Motility of a Flagellate Microorganism

Cited by 58 publications

References 41 publications

Reorganization of complex ciliary flows around regeneratingStentor coeruleus

Reorganization of complex ciliary flows around regeneratingStentor coeruleus

Rapid sperm capture: High-throughput flagellar waveform analysis

Synchrony and symmetry-breaking in active flagellar coordination

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