Sperm chemotaxis is driven by the slope of the chemoattractant concentration field

  1. Héctor Vicente Ramírez-Gómez
  2. Vilma Jimenez Sabinina
  3. Martín Velázquez Pérez
  4. Carmen Beltran
  5. Jorge Carneiro
  6. Christopher D Wood
  7. Idan Tuval
  8. Alberto Darszon  Is a corresponding author
  9. Adán Guerrero  Is a corresponding author
  1. Instituto de Biotecnología, Universidad Nacional Autónoma de México, Mexico
  2. European Molecular Biology Laboratory, Germany
  3. Instituto Gulbenkian de Ciência, Portugal
  4. Universidad Nacional Autónoma de México, Mexico
  5. IMEDEA (UIB-CSIC), Spain

Abstract

Spermatozoa of marine invertebrates are attracted to their conspecific female gamete by diffusive molecules, called chemoattractants, released from the egg investments in a process known as chemotaxis. The information from the egg chemoattractant concentration field is decoded into intracellular Ca2+ concentration ([Ca2+]i) changes that regulate the internal motors that shape the flagellum as it beats. By studying sea urchin species-specific differences in sperm chemoattractant-receptor characteristics we show that receptor density constrains the steepness of the chemoattractant concentration gradient detectable by spermatozoa. Through analyzing different chemoattractant gradient forms, we demonstrate for the first time that Strongylocentrotus purpuratus sperm are chemotactic and this response is consistent with frequency entrainment of two coupled physiological oscillators: i) the stimulus function and ii) the [Ca2+]i changes. We demonstrate that the slope of the chemoattractant gradients provides the coupling force between both oscillators, arising as a fundamental requirement for sperm chemotaxis.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Héctor Vicente Ramírez-Gómez

    Genética del Desarrollo y Fisiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4526-4689
  2. Vilma Jimenez Sabinina

    Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9390-1646
  3. Martín Velázquez Pérez

    Genética del Desarrollo y Fisiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  4. Carmen Beltran

    Genética del Desarrollo y Fisiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9344-7618
  5. Jorge Carneiro

    Instituto Gulbenkian de Ciência, Oeiras, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  6. Christopher D Wood

    Departamento de Genética del Desarrollo y Fisiología Molecular, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  7. Idan Tuval

    Marine Ecology and Physics, IMEDEA (UIB-CSIC), Esporles, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6629-0851
  8. Alberto Darszon

    Genética del Desarrollo y Fisiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    For correspondence
    darszon@ibt.unam.mx
    Competing interests
    The authors declare that no competing interests exist.
  9. Adán Guerrero

    Laboratorio Nacional de Microscopía Avanzada, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    For correspondence
    adanog@ibt.unam.mx
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4389-5516

Funding

Consejo Nacional de Ciencia y Tecnología (Fronteras 71,Ciencia basica 252213 y 255914)

  • Adán Guerrero

Consejo Nacional de Ciencia y Tecnología (Fronteras 71,Ciencia basica 252213 y 255914)

  • Alberto Darszon

Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México (IA202417,IN205516,IN206016,IN215519 and IN112514)

  • Adán Guerrero

Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México (IA202417,IN205516,IN206016,IN215519 and IN112514)

  • Alberto Darszon

Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México (IA202417,IN205516,IN206016,IN215519 and IN112514)

  • Carmen Beltran

Ministerio de Economía y Competitividad (FIS2013-48444-C2-1-P,FIS2016-77692-C2-1- P)

  • Idan Tuval

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: All of the animals were handled according to approved institutional animal care and use committee protocols (# 44, 142, 188, 193, 285) of the Instituto de Biotecnología of the Universidad Nacional Autónoma de México.

Version history

  1. Received: July 25, 2019
  2. Accepted: March 6, 2020
  3. Accepted Manuscript published: March 9, 2020 (version 1)
  4. Version of Record published: March 24, 2020 (version 2)

Copyright

© 2020, Ramírez-Gómez 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. Héctor Vicente Ramírez-Gómez
  2. Vilma Jimenez Sabinina
  3. Martín Velázquez Pérez
  4. Carmen Beltran
  5. Jorge Carneiro
  6. Christopher D Wood
  7. Idan Tuval
  8. Alberto Darszon
  9. Adán Guerrero
(2020)
Sperm chemotaxis is driven by the slope of the chemoattractant concentration field
eLife 9:e50532.
https://doi.org/10.7554/eLife.50532

Share this article

https://doi.org/10.7554/eLife.50532

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