Flagellar energetics from high-resolution imaging of beating patterns in tethered mouse sperm

  1. Ashwin Nandagiri
  2. Avinash Satish Gaikwad
  3. David L Potter
  4. Reza Nosrati
  5. Julio Soria
  6. Moira K O'Bryan
  7. Sameer Jadhav
  8. Ranganathan Prabhakar  Is a corresponding author
  1. IITB-Monash Research Academy/ IIT Bombay/ Monash University, India
  2. University of Melbourne, Australia
  3. Monash University, Australia
  4. IITB-Monash Research Academy, India

Abstract

We demonstrate a technique for investigating the energetics of flagella or cilia. We record the planar beating of tethered mouse sperm at high-resolution. Beating waveforms are reconstructed using Proper Orthogonal Decomposition of the centerline tangent-angle profiles. Energy conservation is employed to obtain the mechanical power exerted by the dynein motors from the observed kinematics. A large proportion of the mechanical power exerted by the dynein motors is dissipated internally by the motors themselves. There could also be significant dissipation within the passive structures of the flagellum. The total internal dissipation is considerably greater than the hydrodynamic dissipation in the aqueous medium outside. The net power input from the dynein motors in sperm from Crisp2-knockout mice is significantly smaller than in wildtype samples, indicating that ion-channel regulation by cysteine-rich secretory proteins (CRISPs) controls energy flows powering the axoneme.

Data availability

Source data files for all results figures have been provided.Videos of the WT and KO mice sperm samples are available for public access and download from the Monash University Research Repository (Ref. 64: DOI: 10.26180/5f50562bb322b)MATLAB Codes used to analyze the data to produce the results in the manuscript are available for public access and download from the Monash University Research Repository (Ref. 64: DOI: 10.26180/14045816}

Article and author information

Author details

  1. Ashwin Nandagiri

    Department of Chemical Engineering, IIT Bombay/Department of Mechanical & Aerospace Engineering, Monash University, IITB-Monash Research Academy/ IIT Bombay/ Monash University, Mumbai, India
    Competing interests
    The authors declare that no competing interests exist.
  2. Avinash Satish Gaikwad

    School of BioSciences, University of Melbourne, Clayton, Australia
    Competing interests
    The authors declare that no competing interests exist.
  3. David L Potter

    Monash Micro-Imaging, Monash University, Parkville, Australia
    Competing interests
    The authors declare that no competing interests exist.
  4. Reza Nosrati

    Department of Mechanical & Aerospace Engineering, Monash University, Clayton, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1461-229X
  5. Julio Soria

    Department of Mechanical & Aerospace Engineering, Monash University, Clayton, Australia
    Competing interests
    The authors declare that no competing interests exist.
  6. Moira K O'Bryan

    School of BioSciences, University of Melbourne, Parkville, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7298-4940
  7. Sameer Jadhav

    Department of Chemical Engineering, IITB-Monash Research Academy, Mumbai, India
    Competing interests
    The authors declare that no competing interests exist.
  8. Ranganathan Prabhakar

    Department of Mechanical & Aerospace Engineering, Monash University, Clayton, Australia
    For correspondence
    prabhakar.ranganathan@monash.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7357-4222

Funding

Australian Research Council (DP190100343)

  • Reza Nosrati
  • Ranganathan Prabhakar

Australian Research Council (DP200100659)

  • Moira K O'Bryan

Department of Biotechnology, Ministry of Science and Technology, India (BT/PR13442/MED/32/440/2015)

  • Sameer Jadhav

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

Reviewing Editor

  1. Raymond E Goldstein, University of Cambridge, United Kingdom

Ethics

Animal experimentation: This study was peformed in strict accordance with the Australian Code of Practice for the Care and Use of Animals for Scientific Purposes. All of the animals were handled according to institutional animal care and use protocols approved by the Monash Animal Ethics committee (Approval # MARP/2014/084).

Version history

  1. Received: August 27, 2020
  2. Accepted: April 29, 2021
  3. Accepted Manuscript published: April 30, 2021 (version 1)
  4. Version of Record published: May 27, 2021 (version 2)

Copyright

© 2021, Nandagiri 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.

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  1. Ashwin Nandagiri
  2. Avinash Satish Gaikwad
  3. David L Potter
  4. Reza Nosrati
  5. Julio Soria
  6. Moira K O'Bryan
  7. Sameer Jadhav
  8. Ranganathan Prabhakar
(2021)
Flagellar energetics from high-resolution imaging of beating patterns in tethered mouse sperm
eLife 10:e62524.
https://doi.org/10.7554/eLife.62524

Share this article

https://doi.org/10.7554/eLife.62524

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