Spermatozoa motility in bivalves: Signaling, flagellar beating behavior, and energetics

WOS:000476579700004 International audience Though bivalve mollusks are keystone species and major species groups in aquaculture production worldwide, gamete biology is still largely unknown. This review aims to provide a synthesis of current knowledge in the field of sperm biology, including spermat...

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Published in:Theriogenology
Main Authors: Boulais, Myrina, Demoy-Schneider, Marina, Alavi, Sayyed Mohammad Hadi, Cosson, Jacky
Other Authors: Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM), Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Ecosystèmes Insulaires Océaniens (UMR 241) (EIO), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de la Polynésie Française (UPF)-Institut Louis Malardé Papeete (ILM), Institut de Recherche pour le Développement (IRD), University of Tehran, University of South Bohemia, ANR-11-INBS-0003,CRB-Anim,Réseau de Centres de Ressources Biologiques pour les animaux domestiques(2011), European Project: 245119,EC:FP7:KBBE,FP7-KBBE-2009-3,REPROSEED(2010)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2019
Subjects:
ACL
pH
Online Access:https://hal.science/hal-02749005
https://hal.science/hal-02749005/document
https://hal.science/hal-02749005/file/S0093691X19302493.pdf
https://doi.org/10.1016/j.theriogenology.2019.06.025
id ftinsu:oai:HAL:hal-02749005v1
record_format openpolar
institution Open Polar
collection Institut national des sciences de l'Univers: HAL-INSU
op_collection_id ftinsu
language English
topic ACL
fertilization
sea-urchin
pacific oyster
pecten-maximus
energy-metabolism
Adenosine triphosphate (ATP)
fresh-water clam
Ion signaling
oyster pinctada-margaritifera
pH
scallop
serotonin
Serotonin (5-HT)
sperm motility
Spermatozoa motility
Spermatozoa velocity
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
spellingShingle ACL
fertilization
sea-urchin
pacific oyster
pecten-maximus
energy-metabolism
Adenosine triphosphate (ATP)
fresh-water clam
Ion signaling
oyster pinctada-margaritifera
pH
scallop
serotonin
Serotonin (5-HT)
sperm motility
Spermatozoa motility
Spermatozoa velocity
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
Boulais, Myrina
Demoy-Schneider, Marina
Alavi, Sayyed Mohammad Hadi
Cosson, Jacky
Spermatozoa motility in bivalves: Signaling, flagellar beating behavior, and energetics
topic_facet ACL
fertilization
sea-urchin
pacific oyster
pecten-maximus
energy-metabolism
Adenosine triphosphate (ATP)
fresh-water clam
Ion signaling
oyster pinctada-margaritifera
pH
scallop
serotonin
Serotonin (5-HT)
sperm motility
Spermatozoa motility
Spermatozoa velocity
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
description WOS:000476579700004 International audience Though bivalve mollusks are keystone species and major species groups in aquaculture production worldwide, gamete biology is still largely unknown. This review aims to provide a synthesis of current knowledge in the field of sperm biology, including spermatozoa motility, flagellar beating, and energy metabolism; and to illustrate cellular signaling controlling spermatozoa motility initiation in bivalves. Serotonin (5-HT) induces hyper-motility in spermatozoa via a 5-HT receptor, suggesting a serotoninergic system in the male reproductive tract that might regulate sperm physiology. Acidic pH and high concentration of K+ are inhibitory factors of spermatozoa motility in the testis. Motility is initiated at spawning by a Na+-dependent alkalization of intracellular pH mediated by a Na+/H+ exchanger. Increase of 5-HT in the testis and decrease of extracellular K+ when sperm is released in seawater induce hyperpolarization of spermatozoa membrane potential mediated by K+ efflux and associated with an increase in intracellular Ca2+ via opening of voltage-dependent Ca2+ channels under alkaline conditions. These events activate dynein ATPases and Ca2+/calmodulin-dependent proteins resulting in flagellar beating. It may be possible that 5-HT is also involved in intracellular CAMP rise controlling cAMP-dependent protein kinase phosphorylation in the flagellum. Once motility is triggered, flagellum beats in asymmetric wave pattern leading to circular trajectories of spermatozoa. Three different flagellar wave characteristics are reported, including "full", "twitching", and "declining" propagation of wave, which are described and illustrated in the present review. Mitochondrial respiration, ATP content, and metabolic pathways producing ATP in bivalve spermatozoa are discussed. Energy metabolism of Pacific oyster spermatozoa differs from previously studied marine species since oxidative phosphorylation synthetizes a stable level of ATP throughout 24-h motility period and the end ...
author2 Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR)
Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM)
Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)
Ecosystèmes Insulaires Océaniens (UMR 241) (EIO)
Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de la Polynésie Française (UPF)-Institut Louis Malardé Papeete (ILM)
Institut de Recherche pour le Développement (IRD)
University of Tehran
University of South Bohemia
ANR-11-INBS-0003,CRB-Anim,Réseau de Centres de Ressources Biologiques pour les animaux domestiques(2011)
European Project: 245119,EC:FP7:KBBE,FP7-KBBE-2009-3,REPROSEED(2010)
format Article in Journal/Newspaper
author Boulais, Myrina
Demoy-Schneider, Marina
Alavi, Sayyed Mohammad Hadi
Cosson, Jacky
author_facet Boulais, Myrina
Demoy-Schneider, Marina
Alavi, Sayyed Mohammad Hadi
Cosson, Jacky
author_sort Boulais, Myrina
title Spermatozoa motility in bivalves: Signaling, flagellar beating behavior, and energetics
title_short Spermatozoa motility in bivalves: Signaling, flagellar beating behavior, and energetics
title_full Spermatozoa motility in bivalves: Signaling, flagellar beating behavior, and energetics
title_fullStr Spermatozoa motility in bivalves: Signaling, flagellar beating behavior, and energetics
title_full_unstemmed Spermatozoa motility in bivalves: Signaling, flagellar beating behavior, and energetics
title_sort spermatozoa motility in bivalves: signaling, flagellar beating behavior, and energetics
publisher HAL CCSD
publishDate 2019
url https://hal.science/hal-02749005
https://hal.science/hal-02749005/document
https://hal.science/hal-02749005/file/S0093691X19302493.pdf
https://doi.org/10.1016/j.theriogenology.2019.06.025
geographic Pacific
geographic_facet Pacific
genre Pacific oyster
genre_facet Pacific oyster
op_source ISSN: 0093-691X
Theriogenology
https://hal.science/hal-02749005
Theriogenology, 2019, 136, pp.15-27. ⟨10.1016/j.theriogenology.2019.06.025⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1016/j.theriogenology.2019.06.025
info:eu-repo/grantAgreement/EC/FP7/245119/EU/REsearch to improve PROduction of SEED of established and emerging bivalve species in European hatcheries/REPROSEED
hal-02749005
https://hal.science/hal-02749005
https://hal.science/hal-02749005/document
https://hal.science/hal-02749005/file/S0093691X19302493.pdf
doi:10.1016/j.theriogenology.2019.06.025
PII: S0093-691X(19)30249-3
op_rights http://creativecommons.org/licenses/by-nc/
info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.1016/j.theriogenology.2019.06.025
container_title Theriogenology
container_volume 136
container_start_page 15
op_container_end_page 27
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spelling ftinsu:oai:HAL:hal-02749005v1 2024-04-14T08:18:02+00:00 Spermatozoa motility in bivalves: Signaling, flagellar beating behavior, and energetics Boulais, Myrina Demoy-Schneider, Marina Alavi, Sayyed Mohammad Hadi Cosson, Jacky Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Ecosystèmes Insulaires Océaniens (UMR 241) (EIO) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de la Polynésie Française (UPF)-Institut Louis Malardé Papeete (ILM) Institut de Recherche pour le Développement (IRD) University of Tehran University of South Bohemia ANR-11-INBS-0003,CRB-Anim,Réseau de Centres de Ressources Biologiques pour les animaux domestiques(2011) European Project: 245119,EC:FP7:KBBE,FP7-KBBE-2009-3,REPROSEED(2010) 2019 https://hal.science/hal-02749005 https://hal.science/hal-02749005/document https://hal.science/hal-02749005/file/S0093691X19302493.pdf https://doi.org/10.1016/j.theriogenology.2019.06.025 en eng HAL CCSD Elsevier info:eu-repo/semantics/altIdentifier/doi/10.1016/j.theriogenology.2019.06.025 info:eu-repo/grantAgreement/EC/FP7/245119/EU/REsearch to improve PROduction of SEED of established and emerging bivalve species in European hatcheries/REPROSEED hal-02749005 https://hal.science/hal-02749005 https://hal.science/hal-02749005/document https://hal.science/hal-02749005/file/S0093691X19302493.pdf doi:10.1016/j.theriogenology.2019.06.025 PII: S0093-691X(19)30249-3 http://creativecommons.org/licenses/by-nc/ info:eu-repo/semantics/OpenAccess ISSN: 0093-691X Theriogenology https://hal.science/hal-02749005 Theriogenology, 2019, 136, pp.15-27. ⟨10.1016/j.theriogenology.2019.06.025⟩ ACL fertilization sea-urchin pacific oyster pecten-maximus energy-metabolism Adenosine triphosphate (ATP) fresh-water clam Ion signaling oyster pinctada-margaritifera pH scallop serotonin Serotonin (5-HT) sperm motility Spermatozoa motility Spermatozoa velocity [SDE.BE]Environmental Sciences/Biodiversity and Ecology info:eu-repo/semantics/article Journal articles 2019 ftinsu https://doi.org/10.1016/j.theriogenology.2019.06.025 2024-03-21T17:17:23Z WOS:000476579700004 International audience Though bivalve mollusks are keystone species and major species groups in aquaculture production worldwide, gamete biology is still largely unknown. This review aims to provide a synthesis of current knowledge in the field of sperm biology, including spermatozoa motility, flagellar beating, and energy metabolism; and to illustrate cellular signaling controlling spermatozoa motility initiation in bivalves. Serotonin (5-HT) induces hyper-motility in spermatozoa via a 5-HT receptor, suggesting a serotoninergic system in the male reproductive tract that might regulate sperm physiology. Acidic pH and high concentration of K+ are inhibitory factors of spermatozoa motility in the testis. Motility is initiated at spawning by a Na+-dependent alkalization of intracellular pH mediated by a Na+/H+ exchanger. Increase of 5-HT in the testis and decrease of extracellular K+ when sperm is released in seawater induce hyperpolarization of spermatozoa membrane potential mediated by K+ efflux and associated with an increase in intracellular Ca2+ via opening of voltage-dependent Ca2+ channels under alkaline conditions. These events activate dynein ATPases and Ca2+/calmodulin-dependent proteins resulting in flagellar beating. It may be possible that 5-HT is also involved in intracellular CAMP rise controlling cAMP-dependent protein kinase phosphorylation in the flagellum. Once motility is triggered, flagellum beats in asymmetric wave pattern leading to circular trajectories of spermatozoa. Three different flagellar wave characteristics are reported, including "full", "twitching", and "declining" propagation of wave, which are described and illustrated in the present review. Mitochondrial respiration, ATP content, and metabolic pathways producing ATP in bivalve spermatozoa are discussed. Energy metabolism of Pacific oyster spermatozoa differs from previously studied marine species since oxidative phosphorylation synthetizes a stable level of ATP throughout 24-h motility period and the end ... Article in Journal/Newspaper Pacific oyster Institut national des sciences de l'Univers: HAL-INSU Pacific Theriogenology 136 15 27