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.

Metrics

  • 3,250
    views
  • 315
    downloads
  • 10
    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. 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

Further reading

    1. Computational and Systems Biology
    2. Physics of Living Systems
    Taegon Chung, Iksoo Chang, Sangyeol Kim
    Research Article

    Locomotion is a fundamental behavior of Caenorhabditis elegans (C. elegans). Previous works on kinetic simulations of animals helped researchers understand the physical mechanisms of locomotion and the muscle-controlling principles of neuronal circuits as an actuator part. It has yet to be understood how C. elegans utilizes the frictional forces caused by the tension of its muscles to perform sequenced locomotive behaviors. Here, we present a two-dimensional rigid body chain model for the locomotion of C. elegans by developing Newtonian equations of motion for each body segment of C. elegans. Having accounted for friction-coefficients of the surrounding environment, elastic constants of C. elegans, and its kymogram from experiments, our kinetic model (ElegansBot) reproduced various locomotion of C. elegans such as, but not limited to, forward-backward-(omega turn)-forward locomotion constituting escaping behavior and delta-turn navigation. Additionally, ElegansBot precisely quantified the forces acting on each body segment of C. elegans to allow investigation of the force distribution. This model will facilitate our understanding of the detailed mechanism of various locomotive behaviors at any given friction-coefficients of the surrounding environment. Furthermore, as the model ensures the performance of realistic behavior, it can be used to research actuator-controller interaction between muscles and neuronal circuits.

    1. Physics of Living Systems
    Giulio Facchini, Alann Rathery ... Andrea Perna
    Research Article

    Termites build complex nests which are an impressive example of self-organization. We know that the coordinated actions involved in the construction of these nests by multiple individuals are primarily mediated by signals and cues embedded in the structure of the nest itself. However, to date there is still no scientific consensus about the nature of the stimuli that guide termite construction, and how they are sensed by termites. In order to address these questions, we studied the early building behavior of Coptotermes gestroi termites in artificial arenas, decorated with topographic cues to stimulate construction. Pellet collections were evenly distributed across the experimental setup, compatible with a collection mechanism that is not affected by local topography, but only by the distribution of termite occupancy (termites pick pellets at the positions where they are). Conversely, pellet depositions were concentrated at locations of high surface curvature and at the boundaries between different types of substrate. The single feature shared by all pellet deposition regions was that they correspond to local maxima in the evaporation flux. We can show analytically and we confirm experimentally that evaporation flux is directly proportional to the local curvature of nest surfaces. Taken together, our results indicate that surface curvature is sufficient to organize termite building activity and that termites likely sense curvature indirectly through substrate evaporation. Our findings reconcile the apparently discordant results of previous studies.