Swimming under elevated hydrostatic pressure increases glycolytic activity in gas gland cells of the European eel.

In spite of many decades of research, the spawning migration of the European eel Anguilla anguilla from the European coast to the Sargasso Sea remains a mystery. In particular, the role of the swimbladder as a buoyancy regulating structure is not yet understood. In this study, we exercised silver ee...

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Main Authors: Gabriel Schneebauer, Constantin Lindemann, Victoria Drechsel, Lasse Marohn, Klaus Wysujack, Elena Santidrian, Ron Dirks, Reinhold Hanel, Bernd Pelster
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0239627
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spelling doaj-86bcefb00ba049bb9e00ea542d27aa512021-03-03T22:07:22ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-01159e023962710.1371/journal.pone.0239627Swimming under elevated hydrostatic pressure increases glycolytic activity in gas gland cells of the European eel.Gabriel SchneebauerConstantin LindemannVictoria DrechselLasse MarohnKlaus WysujackElena SantidrianRon DirksReinhold HanelBernd PelsterIn spite of many decades of research, the spawning migration of the European eel Anguilla anguilla from the European coast to the Sargasso Sea remains a mystery. In particular, the role of the swimbladder as a buoyancy regulating structure is not yet understood. In this study, we exercised silver eels in a swim tunnel under elevated hydrostatic pressure. The transcriptome of gas gland tissue of these exercised eels was then compared to the known transcriptome of not exercised (control) silver eel gas gland cells. Due to the high infection rate of the eel population with the swimbladder parasite Anguillicola crassus, the comparison also included an exercised group of silver eels with a heavily damaged swimbladder, and we compared the previously published transcriptome of not exercised silver eels with a highly damaged swimbladder with the exercised group of silver eels with a heavily damaged swimbladder. The comparisons of unexercised (control) silver eels with exercised silver eels with functional swimbladder (EF), as well as with exercised silver eels with damaged swimbladder (ED), both showed a significant elevation in transcripts related to glycolytic enzymes. This could also be observed within the comparison of unexercised silver eels with a highly infected swimbladder with exercised eels with a damaged swimbladder (DED). In contrast to EF, in ED a significant elevation in transcript numbers of mitochondrial NADH dehydrogenase was observed. While in EF the transcriptional changes suggested that acid production and secretion was enhanced, in ED these changes appeared to be related to thickened tissue and thus elevated diffusion distances. The remarkable number of differentially expressed transcripts coding for proteins connected to cAMP-dependent signaling pathways indicated that metabolic control in gas gland cells includes cAMP-dependent pathways. In contrast to ED, in EF significant transcriptional changes could be related to the reconstruction of the extracellular matrix, while in ED tissue repair and inflammation was more pronounced. Surprisingly, in exercised eels hypoxia inducible transcription factor expression was elevated. In EF, a large number of genes related to the circadian clock were transcriptionally modified, which may be connected to the circadian vertical migrations observed during the spawning migration.https://doi.org/10.1371/journal.pone.0239627
collection DOAJ
language English
format Article
sources DOAJ
author Gabriel Schneebauer
Constantin Lindemann
Victoria Drechsel
Lasse Marohn
Klaus Wysujack
Elena Santidrian
Ron Dirks
Reinhold Hanel
Bernd Pelster
spellingShingle Gabriel Schneebauer
Constantin Lindemann
Victoria Drechsel
Lasse Marohn
Klaus Wysujack
Elena Santidrian
Ron Dirks
Reinhold Hanel
Bernd Pelster
Swimming under elevated hydrostatic pressure increases glycolytic activity in gas gland cells of the European eel.
PLoS ONE
author_facet Gabriel Schneebauer
Constantin Lindemann
Victoria Drechsel
Lasse Marohn
Klaus Wysujack
Elena Santidrian
Ron Dirks
Reinhold Hanel
Bernd Pelster
author_sort Gabriel Schneebauer
title Swimming under elevated hydrostatic pressure increases glycolytic activity in gas gland cells of the European eel.
title_short Swimming under elevated hydrostatic pressure increases glycolytic activity in gas gland cells of the European eel.
title_full Swimming under elevated hydrostatic pressure increases glycolytic activity in gas gland cells of the European eel.
title_fullStr Swimming under elevated hydrostatic pressure increases glycolytic activity in gas gland cells of the European eel.
title_full_unstemmed Swimming under elevated hydrostatic pressure increases glycolytic activity in gas gland cells of the European eel.
title_sort swimming under elevated hydrostatic pressure increases glycolytic activity in gas gland cells of the european eel.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2020-01-01
description In spite of many decades of research, the spawning migration of the European eel Anguilla anguilla from the European coast to the Sargasso Sea remains a mystery. In particular, the role of the swimbladder as a buoyancy regulating structure is not yet understood. In this study, we exercised silver eels in a swim tunnel under elevated hydrostatic pressure. The transcriptome of gas gland tissue of these exercised eels was then compared to the known transcriptome of not exercised (control) silver eel gas gland cells. Due to the high infection rate of the eel population with the swimbladder parasite Anguillicola crassus, the comparison also included an exercised group of silver eels with a heavily damaged swimbladder, and we compared the previously published transcriptome of not exercised silver eels with a highly damaged swimbladder with the exercised group of silver eels with a heavily damaged swimbladder. The comparisons of unexercised (control) silver eels with exercised silver eels with functional swimbladder (EF), as well as with exercised silver eels with damaged swimbladder (ED), both showed a significant elevation in transcripts related to glycolytic enzymes. This could also be observed within the comparison of unexercised silver eels with a highly infected swimbladder with exercised eels with a damaged swimbladder (DED). In contrast to EF, in ED a significant elevation in transcript numbers of mitochondrial NADH dehydrogenase was observed. While in EF the transcriptional changes suggested that acid production and secretion was enhanced, in ED these changes appeared to be related to thickened tissue and thus elevated diffusion distances. The remarkable number of differentially expressed transcripts coding for proteins connected to cAMP-dependent signaling pathways indicated that metabolic control in gas gland cells includes cAMP-dependent pathways. In contrast to ED, in EF significant transcriptional changes could be related to the reconstruction of the extracellular matrix, while in ED tissue repair and inflammation was more pronounced. Surprisingly, in exercised eels hypoxia inducible transcription factor expression was elevated. In EF, a large number of genes related to the circadian clock were transcriptionally modified, which may be connected to the circadian vertical migrations observed during the spawning migration.
url https://doi.org/10.1371/journal.pone.0239627
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