Cold seawater induces early sexual developmental stages in the BPG axis of European eel males

Abstract Background The impossibility of closing the life cycle of the European eel (Anguilla anguilla) in captivity troubles the future of this critically endangered species. In addition, the European eel is a highly valued and demanded resource, thus the successful closing of its life cycle would...

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Main Authors: Rozenfeld, Christoffer, García-Carpintero, Víctor, Pérez, Luz, Gallego, Victor, Herranz-Jusdado, Juan, Tveiten, Helge, Johnsen, Helge, Fontaine, Romain, Finn-Arne Weltzien, Cañizares, Joaquín, Asturiano, Juan, Peñaranda, David
Format: Article in Journal/Newspaper
Language:unknown
Published: Figshare 2019
Subjects:
Online Access:https://dx.doi.org/10.6084/m9.figshare.c.4585571.v1
https://springernature.figshare.com/collections/Cold_seawater_induces_early_sexual_developmental_stages_in_the_BPG_axis_of_European_eel_males/4585571/1
id ftdatacite:10.6084/m9.figshare.c.4585571.v1
record_format openpolar
spelling ftdatacite:10.6084/m9.figshare.c.4585571.v1 2023-05-15T13:28:23+02:00 Cold seawater induces early sexual developmental stages in the BPG axis of European eel males Rozenfeld, Christoffer García-Carpintero, Víctor Pérez, Luz Gallego, Victor Herranz-Jusdado, Juan Tveiten, Helge Johnsen, Helge Fontaine, Romain Finn-Arne Weltzien Cañizares, Joaquín Asturiano, Juan Peñaranda, David 2019 https://dx.doi.org/10.6084/m9.figshare.c.4585571.v1 https://springernature.figshare.com/collections/Cold_seawater_induces_early_sexual_developmental_stages_in_the_BPG_axis_of_European_eel_males/4585571/1 unknown Figshare https://dx.doi.org/10.1186/s12864-019-5969-6 https://dx.doi.org/10.6084/m9.figshare.c.4585571 CC BY 4.0 https://creativecommons.org/licenses/by/4.0 CC-BY Genetics FOS Biological sciences Molecular Biology Physiology 59999 Environmental Sciences not elsewhere classified FOS Earth and related environmental sciences Ecology 69999 Biological Sciences not elsewhere classified Developmental Biology Inorganic Chemistry FOS Chemical sciences Science Policy Collection article 2019 ftdatacite https://doi.org/10.6084/m9.figshare.c.4585571.v1 https://doi.org/10.1186/s12864-019-5969-6 https://doi.org/10.6084/m9.figshare.c.4585571 2021-11-05T12:55:41Z Abstract Background The impossibility of closing the life cycle of the European eel (Anguilla anguilla) in captivity troubles the future of this critically endangered species. In addition, the European eel is a highly valued and demanded resource, thus the successful closing of its life cycle would have a substantial economic and ecological impact. With the aim of obtaining the highest gamete quality, the study of the effects of environmental factors, such as temperature, on reproductive performance may prove valuable. This is especially true for the exposure to cold water, which has been reported to improve sexual development in multiple other Actinopterygii species. Results European eel males treated with cold seawater (10 °C, T10) for 2 weeks showed an increase in the proliferation and differentiation of spermatogonial cells until the differentiated spermatogonial type A cell stage, and elevated testosterone and 11-ketotestosterone plasma levels. Transcriptomes from the tissues of the brain-pituitary-gonad (BPG) axis of T10 samples revealed a differential gene expression profile compared to the other experimental groups, with clustering in a principal component analysis and in heat maps of all differentially expressed genes. Furthermore, a functional analysis of differentially expressed genes revealed enriched gene ontology terms involved in the regulation of circadian rhythm, histone modification, meiotic nuclear division, and others. Conclusions Cold seawater treatment had a clear effect on the activity of the BPG-axis of European eel males. In particular, our cold seawater treatment induces the synchronization and increased proliferation and differentiation of specific spermatogonial cells. In the transcriptomic results, genes related to thermoception were observed. This thermoception may have caused the observed effects through epigenetic mechanisms, since all analysed tissues further revealed differentially expressed genes involved in histone modification. The presented results support our hypothesis that a low temperature seawater treatment induces an early sexual developmental stage in European eels. This hypothesis is logical given that the average temperature experienced by eels in the early stages of their oceanic reproductive migration is highly similar to that of this cold seawater treatment. Further studies are needed to test whether a cold seawater treatment can improve the response of European eels to artificial hormonal treatment, as the results suggest. Article in Journal/Newspaper Anguilla anguilla European eel DataCite Metadata Store (German National Library of Science and Technology)
institution Open Polar
collection DataCite Metadata Store (German National Library of Science and Technology)
op_collection_id ftdatacite
language unknown
topic Genetics
FOS Biological sciences
Molecular Biology
Physiology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
Ecology
69999 Biological Sciences not elsewhere classified
Developmental Biology
Inorganic Chemistry
FOS Chemical sciences
Science Policy
spellingShingle Genetics
FOS Biological sciences
Molecular Biology
Physiology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
Ecology
69999 Biological Sciences not elsewhere classified
Developmental Biology
Inorganic Chemistry
FOS Chemical sciences
Science Policy
Rozenfeld, Christoffer
García-Carpintero, Víctor
Pérez, Luz
Gallego, Victor
Herranz-Jusdado, Juan
Tveiten, Helge
Johnsen, Helge
Fontaine, Romain
Finn-Arne Weltzien
Cañizares, Joaquín
Asturiano, Juan
Peñaranda, David
Cold seawater induces early sexual developmental stages in the BPG axis of European eel males
topic_facet Genetics
FOS Biological sciences
Molecular Biology
Physiology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
Ecology
69999 Biological Sciences not elsewhere classified
Developmental Biology
Inorganic Chemistry
FOS Chemical sciences
Science Policy
description Abstract Background The impossibility of closing the life cycle of the European eel (Anguilla anguilla) in captivity troubles the future of this critically endangered species. In addition, the European eel is a highly valued and demanded resource, thus the successful closing of its life cycle would have a substantial economic and ecological impact. With the aim of obtaining the highest gamete quality, the study of the effects of environmental factors, such as temperature, on reproductive performance may prove valuable. This is especially true for the exposure to cold water, which has been reported to improve sexual development in multiple other Actinopterygii species. Results European eel males treated with cold seawater (10 °C, T10) for 2 weeks showed an increase in the proliferation and differentiation of spermatogonial cells until the differentiated spermatogonial type A cell stage, and elevated testosterone and 11-ketotestosterone plasma levels. Transcriptomes from the tissues of the brain-pituitary-gonad (BPG) axis of T10 samples revealed a differential gene expression profile compared to the other experimental groups, with clustering in a principal component analysis and in heat maps of all differentially expressed genes. Furthermore, a functional analysis of differentially expressed genes revealed enriched gene ontology terms involved in the regulation of circadian rhythm, histone modification, meiotic nuclear division, and others. Conclusions Cold seawater treatment had a clear effect on the activity of the BPG-axis of European eel males. In particular, our cold seawater treatment induces the synchronization and increased proliferation and differentiation of specific spermatogonial cells. In the transcriptomic results, genes related to thermoception were observed. This thermoception may have caused the observed effects through epigenetic mechanisms, since all analysed tissues further revealed differentially expressed genes involved in histone modification. The presented results support our hypothesis that a low temperature seawater treatment induces an early sexual developmental stage in European eels. This hypothesis is logical given that the average temperature experienced by eels in the early stages of their oceanic reproductive migration is highly similar to that of this cold seawater treatment. Further studies are needed to test whether a cold seawater treatment can improve the response of European eels to artificial hormonal treatment, as the results suggest.
format Article in Journal/Newspaper
author Rozenfeld, Christoffer
García-Carpintero, Víctor
Pérez, Luz
Gallego, Victor
Herranz-Jusdado, Juan
Tveiten, Helge
Johnsen, Helge
Fontaine, Romain
Finn-Arne Weltzien
Cañizares, Joaquín
Asturiano, Juan
Peñaranda, David
author_facet Rozenfeld, Christoffer
García-Carpintero, Víctor
Pérez, Luz
Gallego, Victor
Herranz-Jusdado, Juan
Tveiten, Helge
Johnsen, Helge
Fontaine, Romain
Finn-Arne Weltzien
Cañizares, Joaquín
Asturiano, Juan
Peñaranda, David
author_sort Rozenfeld, Christoffer
title Cold seawater induces early sexual developmental stages in the BPG axis of European eel males
title_short Cold seawater induces early sexual developmental stages in the BPG axis of European eel males
title_full Cold seawater induces early sexual developmental stages in the BPG axis of European eel males
title_fullStr Cold seawater induces early sexual developmental stages in the BPG axis of European eel males
title_full_unstemmed Cold seawater induces early sexual developmental stages in the BPG axis of European eel males
title_sort cold seawater induces early sexual developmental stages in the bpg axis of european eel males
publisher Figshare
publishDate 2019
url https://dx.doi.org/10.6084/m9.figshare.c.4585571.v1
https://springernature.figshare.com/collections/Cold_seawater_induces_early_sexual_developmental_stages_in_the_BPG_axis_of_European_eel_males/4585571/1
genre Anguilla anguilla
European eel
genre_facet Anguilla anguilla
European eel
op_relation https://dx.doi.org/10.1186/s12864-019-5969-6
https://dx.doi.org/10.6084/m9.figshare.c.4585571
op_rights CC BY 4.0
https://creativecommons.org/licenses/by/4.0
op_rightsnorm CC-BY
op_doi https://doi.org/10.6084/m9.figshare.c.4585571.v1
https://doi.org/10.1186/s12864-019-5969-6
https://doi.org/10.6084/m9.figshare.c.4585571
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