The Protoplasmic Viscosity of <i>Paramecium</i>

Brown, Ralph H.

doi:10.1242/jeb.17.3.317

“…Plugging in the relevant numbers (

N,

m,

m/s,

s

), it shows that the viscosity of the cytoplasm has to be as large as 0.12 Pa-s to dissipate the input energy, which is 120 times larger than the viscosity of the water. This number is also in direct contradiction to the previously measured cytoplasm viscosity in other ciliates or protists, which is about 0.005–0.05 Pa-s ( 13 , 14 ). These contradictions suggest that it is not possible to dissipate the energy just by the fluid shear in the cytoplasm if the cytoplasm were completely filled with liquid without structures.…”

Section: Existing Mechanisms Fail To Explain the Energy Dissipation I...contrasting

confidence: 99%

Topological damping in an ultrafast giant cell

Chang,

Prakash

2023

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

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Cellular systems are known to exhibit some of the fastest movements in biology, but little is known as to how single cells can dissipate this energy rapidly and adapt to such large accelerations without disrupting internal architecture. To address this, we investigate Spirostomum ambiguum —a giant cell (1–4 mm in length) well-known to exhibit ultrafast contractions (50% of body length) within 5 ms with a peak acceleration of 15 g . Utilizing transmitted electron microscopy and confocal imaging, we identify an association of rough endoplasmic reticulum (RER) and vacuoles throughout the cell—forming a contiguous fenestrated membrane architecture that topologically entangles these two organelles. A nearly uniform interorganelle spacing of 60 nm is observed between RER and vacuoles, closely packing the entire cell. Inspired by the entangled organelle structure, we study the mechanical properties of entangled deformable particles using a vertex-based model, with all simulation parameters matching 10 dimensionless numbers to ensure dynamic similarity. We demonstrate how entangled deformable particles respond to external loads by an increased viscosity against squeezing and help preserve spatial relationships. Because this enhanced damping arises from the entanglement of two networks incurring a strain-induced jamming transition at subcritical volume fractions, which is demonstrated through the spatial correlation of velocity direction, we term this phenomenon “topological damping.” Our findings suggest a mechanical role of RER-vacuolar meshwork as a metamaterial capable of damping an ultrafast contraction event.

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“…Note that we use the term "cytoplasmic viscosity" as an effective viscosity for the energy dissipation within the spore, and we are not referring to the viscosity of any particular space within the spore. However, there is no reported measurement regarding the cytoplasmic viscosity of any microsporidian species so far, and previously reported values of cytoplasmic viscosity in other cell types fall into a very wide range (Verkman, 2002 ;Luby-Phelps, 1999 ;Ridgway et al, 2008 ;Swaminathan et al, 1997 ;Brown, 1940 ;Kamitsubo et al, 1989 ;Kalwarczyk et al, 2012 ;Wang et al, 2019 ). We therefore rst computed the result assuming the cytoplasmic viscosity to be 0.05 Pa-sec (Brown, 1940 ), a middle ground value based on the previously reported range in other cell types, and we later re-calculated our predictions using different cytoplasmic viscosity values covering the entire reported range, to assess how much our results vary depending on the degree of uncertainty in the value of cyto-plasmic viscosity.…”

Section: Developing a Mathematical Model For Pt Energeticsmentioning

confidence: 99%

Energetics of the Microsporidian Polar Tube Invasion Machinery

Chang,

Davydov,

Jaroenlak

et al. 2023

Preprint

0

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Microsporidia are eukaryotic, obligate intracellular parasites that infect a wide range of hosts, leading to health and economic burdens worldwide. Microsporidia use an unusual invasion organelle called the polar tube (PT), which is ejected from a dormant spore at ultra-fast speeds, to infect host cells. The mechanics of PT ejection are impressive. Anncaliia algerae microsporidia spores (3-4 µm in size) shoot out a 100-nm-wide PT at a speed of 300 µm/sec, creating a shear rate of 3000 sec−1. The infectious cargo, which contains two nuclei, is shot through this narrow tube for a distance of ∼60-140 µm (Jaroenlak et al., 2020) and into the host cell. Considering the large hydraulic resistance in an extremely thin tube and the low-Reynolds-number nature of the process, it is not known how microsporidia can achieve this ultrafast event. In this study, we use Serial Block-Face Scanning Electron Microscopy to capture 3-dimensional snapshots of A. algerae spores in different states of the PT ejection process. Grounded in these data, we propose a theoretical framework starting with a systematic exploration of possible topological connectivity amongst organelles, and assess the energy requirements of the resulting models. We perform PT ring experiments in media of varying viscosity, and use the results to rank our proposed hypotheses based on their predicted energy requirement. We also present a possible mechanism for cargo translocation, and quantitatively compare our predictions to experimental observations. Our study provides a comprehensive biophysical analysis of the energy dissipation of microsporidian infection process and demonstrates the extreme limits of cellular hydraulics. Microsporidia are a group of spore-forming, intracellular parasites that infect a wide range of hosts (including humans). Once triggered, microsporidian spores (3-4 µm in size) shoot out a specialized organelle called the polar tube (PT) (60-140 µm long, 100 nm wide) at ultrafast speed (300 µm/sec), penetrating host cells and acting as a conduit for the transport of infectious cargo. Although this process has fascinated biologists for a century, the biophysical mechanisms underlying PT extrusion are not understood. We thus take a data-driven approach to generate models for the physical basis of PT ring and cargo transport through the PT. Our approach here demonstrates the extreme limits of cellular hydraulics and the potential applications of biophysical approaches to other cellular architectures.

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“…However, there is no reported measurement regarding the cytoplasmic viscosity of any microsporidian species so far, and previously reported values of cytoplasmic viscosity in other cell types fall into a very wide range. [30][31][32][33][34][35][36][37] We therefore first computed the result assuming the cytoplasmic viscosity to be 0.05 Pa-sec, 34 a middle ground value based on the previously reported range in other cell types, and we later re-calculated our predictions using different cytoplasmic viscosity values covering the entire reported range, to assess how much our results vary depending on the degree of uncertainty in the value of cytoplasmic viscosity. We measured the viscosity of the germination buffer and modified formulations using a commercial rheometer (Fig 4C, see Method section for details).…”

Section: Developing a Mathematical Model For Pt Energeticsmentioning

confidence: 99%

Energetics of the Microsporidian Polar Tube Invasion Machinery

Chang

¹

,

Davydov

²

,

Jaroenlak

³

et al. 2023

Preprint

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Microsporidia are eukaryotic, obligate intracellular parasites that infect a wide range of hosts, leading to health and economic burdens worldwide. Microsporidia use an unusual invasion organelle called the polar tube (PT), which is ejected from a dormant spore at ultra-fast speeds, to infect host cells. The mechanics of PT ejection are impressive. Anncaliia algerae microsporidia spores (3-4 μm in size) shoot out a 100-nm-wide PT at a speed of 300 μm/sec, creating a shear rate of 3000 1/sec. The infectious cargo, which contains two nuclei, is shot through this narrow tube for a distance of ~60-140 μm and into the host cell. Considering the large hydraulic resistance in an extremely thin tube and the low-Reynolds-number nature of the process, it is not known how microsporidia can achieve this ultrafast event. In this study, we use Serial Block-Face Scanning Electron Microscopy to capture 3-dimensional snapshots of A. algerae spores in different states of the PT ejection process. Grounded in these data, we propose a theoretical framework starting with a systematic exploration of possible topological connectivity amongst organelles, and assess the energy requirements of the resulting models. We perform PT firing experiments in media of varying viscosity, and use the results to rank our proposed hypotheses based on their predicted energy requirement, pressure and power. We also present a possible mechanism for cargo translocation, and quantitatively compare our predictions to experimental observations. Our study provides a comprehensive biophysical analysis of the energy dissipation of microsporidian infection process and demonstrates the extreme limits of cellular hydraulics.

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The Protoplasmic Viscosity of Paramecium

Cited by 21 publications

References 9 publications

Topological damping in an ultrafast giant cell

Topological damping in an ultrafast giant cell

Energetics of the Microsporidian Polar Tube Invasion Machinery

Energetics of the Microsporidian Polar Tube Invasion Machinery

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