Ciliary chemosensitivity is enhanced by cilium geometry and motility

  1. David Hickey
  2. Andrej Vilfan  Is a corresponding author
  3. Ramin Golestanian  Is a corresponding author
  1. Max Planck Institute for Dynamics and Self-Organization, Germany

Abstract

Cilia are hairlike organelles involved in both sensory functions and motility. We discuss the question of whether the location of chemical receptors on cilia provides an advantage in terms of sensitivity and whether motile sensory cilia have a further advantage. Using a simple advection-diffusion model, we compute the capture rates of diffusive molecules on a cilium. Because of its geometry, a non-motile cilium in a quiescent fluid has a capture rate equivalent to a circular absorbing region with ~4x its surface area. When the cilium is exposed to an external shear flow, the equivalent surface area increases to ~6x. Alternatively, if the cilium beats in a non-reciprocal way in an otherwise quiescent fluid, its capture rate increases with the beating frequency to the power of 1/3. Altogether, our results show that the protruding geometry of a cilium could be one of the reasons why so many receptors are located on cilia. They also point to the advantage of combining motility with chemical reception.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 3 and 4.

Article and author information

Author details

  1. David Hickey

    Living Matter Physics, Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Andrej Vilfan

    Living Matter Physics, Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany
    For correspondence
    andrej.vilfan@ds.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8985-6072
  3. Ramin Golestanian

    Department of Living Matter Physics, Max Planck Institute for Dynamics and Self-Organization, Goettingen, Germany
    For correspondence
    Ramin.Golestanian@ds.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3149-4002

Funding

Max-Planck-Gesellschaft

  • David Hickey
  • Andrej Vilfan
  • Ramin Golestanian

Javna Agencija za Raziskovalno Dejavnost RS (P1-0099)

  • Andrej Vilfan

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2021, Hickey et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 990
    views
  • 198
    downloads
  • 8
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. David Hickey
  2. Andrej Vilfan
  3. Ramin Golestanian
(2021)
Ciliary chemosensitivity is enhanced by cilium geometry and motility
eLife 10:e66322.
https://doi.org/10.7554/eLife.66322

Share this article

https://doi.org/10.7554/eLife.66322

Further reading

    1. Computational and Systems Biology
    2. Physics of Living Systems
    Divyoj Singh, Sriram Ramaswamy ... Mohd Suhail Rizvi
    Research Article

    Planar cell polarity (PCP) – tissue-scale alignment of the direction of asymmetric localization of proteins at the cell-cell interface – is essential for embryonic development and physiological functions. Abnormalities in PCP can result in developmental imperfections, including neural tube closure defects and misaligned hair follicles. Decoding the mechanisms responsible for PCP establishment and maintenance remains a fundamental open question. While the roles of various molecules – broadly classified into “global” and “local” modules – have been well-studied, their necessity and sufficiency in explaining PCP and connecting their perturbations to experimentally observed patterns have not been examined. Here, we develop a minimal model that captures the proposed features of PCP establishment – a global tissue-level gradient and local asymmetric distribution of protein complexes. The proposed model suggests that while polarity can emerge without a gradient, the gradient not only acts as a global cue but also increases the robustness of PCP against stochastic perturbations. We also recapitulated and quantified the experimentally observed features of swirling patterns and domineering non-autonomy, using only three free model parameters - the rate of protein binding to membrane, the concentration of PCP proteins, and the gradient steepness. We explain how self-stabilizing asymmetric protein localizations in the presence of tissue-level gradient can lead to robust PCP patterns and reveal minimal design principles for a polarized system.

    1. Computational and Systems Biology
    2. Physics of Living Systems
    Maria Cristina Cannarsa, Filippo Liguori ... Roberto Di Leonardo
    Research Article

    Synthetic genetic oscillators can serve as internal clocks within engineered cells to program periodic expression. However, cell-to-cell variability introduces a dispersion in the characteristics of these clocks that drives the population to complete desynchronization. Here, we introduce the optorepressilator, an optically controllable genetic clock that combines the repressilator, a three-node synthetic network in E. coli, with an optogenetic module enabling to reset, delay, or advance its phase using optical inputs. We demonstrate that a population of optorepressilators can be synchronized by transient green light exposure or entrained to oscillate indefinitely by a train of short pulses, through a mechanism reminiscent of natural circadian clocks. Furthermore, we investigate the system’s response to detuned external stimuli observing multiple regimes of global synchronization. Integrating experiments and mathematical modeling, we show that the entrainment mechanism is robust and can be understood quantitatively from single cell to population level.