Sperm chemotaxis is driven by the slope of the chemoattractant concentration field
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.
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All data generated or analyzed during this study are included in the manuscript and supporting files.
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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.
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.
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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Further reading
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- Computational and Systems Biology
- Physics of Living Systems
Explaining biodiversity is a fundamental issue in ecology. A long-standing puzzle lies in the paradox of the plankton: many species of plankton feeding on a limited variety of resources coexist, apparently flouting the competitive exclusion principle (CEP), which holds that the number of predator (consumer) species cannot exceed that of the resources at a steady state. Here, we present a mechanistic model and demonstrate that intraspecific interference among the consumers enables a plethora of consumer species to coexist at constant population densities with only one or a handful of resource species. This facilitated biodiversity is resistant to stochasticity, either with the stochastic simulation algorithm or individual-based modeling. Our model naturally explains the classical experiments that invalidate the CEP, quantitatively illustrates the universal S-shaped pattern of the rank-abundance curves across a wide range of ecological communities, and can be broadly used to resolve the mystery of biodiversity in many natural ecosystems.
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- Computational and Systems Biology
- Physics of Living Systems
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.