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Dynamic force measurements on swimming Chlamydomonas cells using micropipette force sensors

MPS-Authors
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Böddeker,  Thomas J.
Group Dynamics of fluid and biological interfaces, Department of Dynamics of Complex Fluids, Max Planck Institute for Dynamics and Self-Organization, Max Planck Society;

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Karpitschka,  Stefan A.
Group Fluidics in heterogeneous environments, Department of Dynamics of Complex Fluids, Max Planck Institute for Dynamics and Self-Organization, Max Planck Society;

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Kreis,  Christian Titus
Group Dynamics of fluid and biological interfaces, Department of Dynamics of Complex Fluids, Max Planck Institute for Dynamics and Self-Organization, Max Planck Society;

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Magdelaine,  Quentin
Group Dynamics of fluid and biological interfaces, Department of Dynamics of Complex Fluids, Max Planck Institute for Dynamics and Self-Organization, Max Planck Society;

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Bäumchen,  Oliver
Group Dynamics of fluid and biological interfaces, Department of Dynamics of Complex Fluids, Max Planck Institute for Dynamics and Self-Organization, Max Planck Society;

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Citation

Böddeker, T. J., Karpitschka, S. A., Kreis, C. T., Magdelaine, Q., & Bäumchen, O. (2020). Dynamic force measurements on swimming Chlamydomonas cells using micropipette force sensors. Interface: Journal of the Royal Society, 17: 20190580. doi:10.1098/rsif.2019.0580.


Cite as: https://hdl.handle.net/21.11116/0000-0005-7B98-6
Abstract
Flagella and cilia are cellular appendages that inherit essential functions of
microbial life including sensing and navigating the environment. In order to
propel a swimming microorganism they displace the surrounding fluid by
means of periodic motions, while precisely timed modulations of their beating
patterns enable the cell to steer towards or away from specific locations. Characterizing
the dynamic forces, however, is challenging and typically relies on
indirect experimental approaches. Here, we present direct in vivo measurements
of the dynamic forces of motile Chlamydomonas reinhardtii cells in
controlled environments. The experiments are based on partially aspirating
a living microorganism at the tip of a micropipette force sensor and optically
recording the micropipette’s position fluctuations with high temporal and
sub-pixel spatial resolution. Spectral signal analysis allows for isolating the
cell-generated dynamic forces caused by the periodic motion of the flagella
from background noise. We provide an analytic, elasto-hydrodynamic
model for the micropipette force sensor and describe how to obtain the micropipette’s
full frequency response function from a dynamic force calibration.
Using this approach, we measure the amplitude of the oscillatory forces
during the swimming activity of individual Chlamydomonas reinhardtii cells
of 26 ± 5 pN, resulting from the coordinated flagellar beating with a frequency
of 49 ± 5 Hz. This dynamic micropipette force sensor technique generalizes the
applicability of micropipettes as force sensors from static to dynamic force
measurements, yielding a force sensitivity in the piconewton range. In
addition to measurements in bulk liquid environment, we study the dynamic
forces of the biflagellated microswimmer in the vicinity of a solid/liquid interface.
As we gradually decrease the distance of the swimming microbe to the
interface, we measure a significantly enhanced force transduction at distances
larger than the maximum extent of the beating flagella, highlighting the
importance of hydrodynamic interactions for scenarios in which flagellated
microorganisms encounter surfaces.