Nitric oxide mediates metabolic functions in the bivalve Arctica islandica under hypoxia

The free radical nitric oxide (NO) is a powerful metabolic regulator in vertebrates and invertebrates. At cellular concentrations in the nanomolar range, and simultaneously reduced internal oxygen partial pressures (pO2), NO completely inhibits cytochrome-c-oxidase (CytOx) activity and hence mitocho...

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Published in:PLOS ONE
Main Authors: Strahl, Julia, Abele, Doris
Format: Article in Journal/Newspaper
Language:unknown
Published: PUBLIC LIBRARY SCIENCE 2020
Subjects:
Online Access:https://epic.awi.de/id/eprint/52322/
https://epic.awi.de/id/eprint/52322/1/Strahl_Abele_2020_PlosOne.pdf
https://hdl.handle.net/10013/epic.18d4da16-2f95-4be3-93e7-d414a440423e
id ftawi:oai:epic.awi.de:52322
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spelling ftawi:oai:epic.awi.de:52322 2024-09-15T17:54:28+00:00 Nitric oxide mediates metabolic functions in the bivalve Arctica islandica under hypoxia Strahl, Julia Abele, Doris 2020-05-07 application/pdf https://epic.awi.de/id/eprint/52322/ https://epic.awi.de/id/eprint/52322/1/Strahl_Abele_2020_PlosOne.pdf https://hdl.handle.net/10013/epic.18d4da16-2f95-4be3-93e7-d414a440423e unknown PUBLIC LIBRARY SCIENCE https://epic.awi.de/id/eprint/52322/1/Strahl_Abele_2020_PlosOne.pdf Strahl, J. orcid:0000-0001-9496-4019 and Abele, D. orcid:0000-0002-5766-5017 (2020) Nitric oxide mediates metabolic functions in the bivalve Arctica islandica under hypoxia , PLoS ONE, 15 (5), e0232360 . doi:10.1371/journal.pone.0232360 <https://doi.org/10.1371/journal.pone.0232360> , hdl:10013/epic.18d4da16-2f95-4be3-93e7-d414a440423e info:eu-repo/semantics/openAccess EPIC3PLoS ONE, PUBLIC LIBRARY SCIENCE, 15(5), pp. e0232360, ISSN: 1932-6203 Article isiRev info:eu-repo/semantics/article 2020 ftawi https://doi.org/10.1371/journal.pone.0232360 2024-06-24T04:24:41Z The free radical nitric oxide (NO) is a powerful metabolic regulator in vertebrates and invertebrates. At cellular concentrations in the nanomolar range, and simultaneously reduced internal oxygen partial pressures (pO2), NO completely inhibits cytochrome-c-oxidase (CytOx) activity and hence mitochondrial- and whole-tissue respiration. The infaunal clam Arctica islandica regulates pO2 of hemolymph and mantle cavity water to mean values of <5 kPa, even in a completely oxygen-saturated environment of 21 kPa. These low internal pO2 values support a longer NO lifespan and NO accumulation in the body fluids and can thus trigger a depression of metabolic rate in the clams. Measurable amounts of NO formation were detected in hemocyte cells (~110 pmol NO 100−1 hemocytes h-1 at 6 kPa), which was not prevented in the presence of the NO synthase inhibitor L-NAME, and in the gill filaments of A. islandica. Adding a NO donor to intact gills and tissue homogenate significantly inhibited gill respiration and CytOx activity below 10 kPa. Meanwhile, the addition of the NO-oxidation product nitrite did not affect metabolic rates. The high nitrite levels found in the hemolymph of experimental mussels under anoxia do not indicate cellular NO production, but could be an indication of nitrate reduction by facultative anaerobic bacteria associated with tissue and/or hemolymph biofilms. Our results suggest that NO plays an important role in the initiation of metabolic depression during self-induced burrowing and shell closure of A. islandica. Furthermore, NO appears to reduce mitochondrial oxygen radical formation during surfacing and cellular reoxygenation after prolonged periods of hypoxia and anoxia. Article in Journal/Newspaper Arctica islandica Alfred Wegener Institute for Polar- and Marine Research (AWI): ePIC (electronic Publication Information Center) PLOS ONE 15 5 e0232360
institution Open Polar
collection Alfred Wegener Institute for Polar- and Marine Research (AWI): ePIC (electronic Publication Information Center)
op_collection_id ftawi
language unknown
description The free radical nitric oxide (NO) is a powerful metabolic regulator in vertebrates and invertebrates. At cellular concentrations in the nanomolar range, and simultaneously reduced internal oxygen partial pressures (pO2), NO completely inhibits cytochrome-c-oxidase (CytOx) activity and hence mitochondrial- and whole-tissue respiration. The infaunal clam Arctica islandica regulates pO2 of hemolymph and mantle cavity water to mean values of <5 kPa, even in a completely oxygen-saturated environment of 21 kPa. These low internal pO2 values support a longer NO lifespan and NO accumulation in the body fluids and can thus trigger a depression of metabolic rate in the clams. Measurable amounts of NO formation were detected in hemocyte cells (~110 pmol NO 100−1 hemocytes h-1 at 6 kPa), which was not prevented in the presence of the NO synthase inhibitor L-NAME, and in the gill filaments of A. islandica. Adding a NO donor to intact gills and tissue homogenate significantly inhibited gill respiration and CytOx activity below 10 kPa. Meanwhile, the addition of the NO-oxidation product nitrite did not affect metabolic rates. The high nitrite levels found in the hemolymph of experimental mussels under anoxia do not indicate cellular NO production, but could be an indication of nitrate reduction by facultative anaerobic bacteria associated with tissue and/or hemolymph biofilms. Our results suggest that NO plays an important role in the initiation of metabolic depression during self-induced burrowing and shell closure of A. islandica. Furthermore, NO appears to reduce mitochondrial oxygen radical formation during surfacing and cellular reoxygenation after prolonged periods of hypoxia and anoxia.
format Article in Journal/Newspaper
author Strahl, Julia
Abele, Doris
spellingShingle Strahl, Julia
Abele, Doris
Nitric oxide mediates metabolic functions in the bivalve Arctica islandica under hypoxia
author_facet Strahl, Julia
Abele, Doris
author_sort Strahl, Julia
title Nitric oxide mediates metabolic functions in the bivalve Arctica islandica under hypoxia
title_short Nitric oxide mediates metabolic functions in the bivalve Arctica islandica under hypoxia
title_full Nitric oxide mediates metabolic functions in the bivalve Arctica islandica under hypoxia
title_fullStr Nitric oxide mediates metabolic functions in the bivalve Arctica islandica under hypoxia
title_full_unstemmed Nitric oxide mediates metabolic functions in the bivalve Arctica islandica under hypoxia
title_sort nitric oxide mediates metabolic functions in the bivalve arctica islandica under hypoxia
publisher PUBLIC LIBRARY SCIENCE
publishDate 2020
url https://epic.awi.de/id/eprint/52322/
https://epic.awi.de/id/eprint/52322/1/Strahl_Abele_2020_PlosOne.pdf
https://hdl.handle.net/10013/epic.18d4da16-2f95-4be3-93e7-d414a440423e
genre Arctica islandica
genre_facet Arctica islandica
op_source EPIC3PLoS ONE, PUBLIC LIBRARY SCIENCE, 15(5), pp. e0232360, ISSN: 1932-6203
op_relation https://epic.awi.de/id/eprint/52322/1/Strahl_Abele_2020_PlosOne.pdf
Strahl, J. orcid:0000-0001-9496-4019 and Abele, D. orcid:0000-0002-5766-5017 (2020) Nitric oxide mediates metabolic functions in the bivalve Arctica islandica under hypoxia , PLoS ONE, 15 (5), e0232360 . doi:10.1371/journal.pone.0232360 <https://doi.org/10.1371/journal.pone.0232360> , hdl:10013/epic.18d4da16-2f95-4be3-93e7-d414a440423e
op_rights info:eu-repo/semantics/openAccess
op_doi https://doi.org/10.1371/journal.pone.0232360
container_title PLOS ONE
container_volume 15
container_issue 5
container_start_page e0232360
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