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Cell Turnover and Detritus Production in Marine Sponges from Tropical and Temperate Benthic Ecosystems

This study describes in vivo cell turnover (the balance between cell proliferation and cell loss) in eight marine sponge species from tropical coral reef, mangrove and temperate Mediterranean reef ecosystems. Cell proliferation was determined through the incorporation of 5-bromo-2′-deoxyuridine (Brd...

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Autores principales: Alexander, Brittany E., Liebrand, Kevin, Osinga, Ronald, van der Geest, Harm G., Admiraal, Wim, Cleutjens, Jack P. M., Schutte, Bert, Verheyen, Fons, Ribes, Marta, van Loon, Emiel, de Goeij, Jasper M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4188633/
https://www.ncbi.nlm.nih.gov/pubmed/25289641
http://dx.doi.org/10.1371/journal.pone.0109486
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author Alexander, Brittany E.
Liebrand, Kevin
Osinga, Ronald
van der Geest, Harm G.
Admiraal, Wim
Cleutjens, Jack P. M.
Schutte, Bert
Verheyen, Fons
Ribes, Marta
van Loon, Emiel
de Goeij, Jasper M.
author_facet Alexander, Brittany E.
Liebrand, Kevin
Osinga, Ronald
van der Geest, Harm G.
Admiraal, Wim
Cleutjens, Jack P. M.
Schutte, Bert
Verheyen, Fons
Ribes, Marta
van Loon, Emiel
de Goeij, Jasper M.
author_sort Alexander, Brittany E.
collection PubMed
description This study describes in vivo cell turnover (the balance between cell proliferation and cell loss) in eight marine sponge species from tropical coral reef, mangrove and temperate Mediterranean reef ecosystems. Cell proliferation was determined through the incorporation of 5-bromo-2′-deoxyuridine (BrdU) and measuring the percentage of BrdU-positive cells after 6 h of continuous labeling (10 h for Chondrosia reniformis). Apoptosis was identified using an antibody against active caspase-3. Cell loss through shedding was studied quantitatively by collecting and weighing sponge-expelled detritus and qualitatively by light microscopy of sponge tissue and detritus. All species investigated displayed substantial cell proliferation, predominantly in the choanoderm, but also in the mesohyl. The majority of coral reef species (five) showed between 16.1±15.9% and 19.0±2.0% choanocyte proliferation (mean±SD) after 6 h and the Mediterranean species, C. reniformis, showed 16.6±3.2% after 10 h BrdU-labeling. Monanchora arbuscula showed lower choanocyte proliferation (8.1±3.7%), whereas the mangrove species Mycale microsigmatosa showed relatively higher levels of choanocyte proliferation (70.5±6.6%). Choanocyte proliferation in Haliclona vansoesti was variable (2.8–73.1%). Apoptosis was negligible and not the primary mechanism of cell loss involved in cell turnover. All species investigated produced significant amounts of detritus (2.5–18% detritus bodyweight(−1)·d(−1)) and cell shedding was observed in seven out of eight species. The amount of shed cells observed in histological sections may be related to differences in residence time of detritus within canals. Detritus production could not be directly linked to cell shedding due to the degraded nature of expelled cellular debris. We have demonstrated that under steady-state conditions, cell turnover through cell proliferation and cell shedding are common processes to maintain tissue homeostasis in a variety of sponge species from different ecosystems. Cell turnover is hypothesized to be the main underlying mechanism producing sponge-derived detritus, a major trophic resource transferred through sponges in benthic ecosystems, such as coral reefs.
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spelling pubmed-41886332014-10-10 Cell Turnover and Detritus Production in Marine Sponges from Tropical and Temperate Benthic Ecosystems Alexander, Brittany E. Liebrand, Kevin Osinga, Ronald van der Geest, Harm G. Admiraal, Wim Cleutjens, Jack P. M. Schutte, Bert Verheyen, Fons Ribes, Marta van Loon, Emiel de Goeij, Jasper M. PLoS One Research Article This study describes in vivo cell turnover (the balance between cell proliferation and cell loss) in eight marine sponge species from tropical coral reef, mangrove and temperate Mediterranean reef ecosystems. Cell proliferation was determined through the incorporation of 5-bromo-2′-deoxyuridine (BrdU) and measuring the percentage of BrdU-positive cells after 6 h of continuous labeling (10 h for Chondrosia reniformis). Apoptosis was identified using an antibody against active caspase-3. Cell loss through shedding was studied quantitatively by collecting and weighing sponge-expelled detritus and qualitatively by light microscopy of sponge tissue and detritus. All species investigated displayed substantial cell proliferation, predominantly in the choanoderm, but also in the mesohyl. The majority of coral reef species (five) showed between 16.1±15.9% and 19.0±2.0% choanocyte proliferation (mean±SD) after 6 h and the Mediterranean species, C. reniformis, showed 16.6±3.2% after 10 h BrdU-labeling. Monanchora arbuscula showed lower choanocyte proliferation (8.1±3.7%), whereas the mangrove species Mycale microsigmatosa showed relatively higher levels of choanocyte proliferation (70.5±6.6%). Choanocyte proliferation in Haliclona vansoesti was variable (2.8–73.1%). Apoptosis was negligible and not the primary mechanism of cell loss involved in cell turnover. All species investigated produced significant amounts of detritus (2.5–18% detritus bodyweight(−1)·d(−1)) and cell shedding was observed in seven out of eight species. The amount of shed cells observed in histological sections may be related to differences in residence time of detritus within canals. Detritus production could not be directly linked to cell shedding due to the degraded nature of expelled cellular debris. We have demonstrated that under steady-state conditions, cell turnover through cell proliferation and cell shedding are common processes to maintain tissue homeostasis in a variety of sponge species from different ecosystems. Cell turnover is hypothesized to be the main underlying mechanism producing sponge-derived detritus, a major trophic resource transferred through sponges in benthic ecosystems, such as coral reefs. Public Library of Science 2014-10-07 /pmc/articles/PMC4188633/ /pubmed/25289641 http://dx.doi.org/10.1371/journal.pone.0109486 Text en © 2014 Alexander et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Alexander, Brittany E.
Liebrand, Kevin
Osinga, Ronald
van der Geest, Harm G.
Admiraal, Wim
Cleutjens, Jack P. M.
Schutte, Bert
Verheyen, Fons
Ribes, Marta
van Loon, Emiel
de Goeij, Jasper M.
Cell Turnover and Detritus Production in Marine Sponges from Tropical and Temperate Benthic Ecosystems
title Cell Turnover and Detritus Production in Marine Sponges from Tropical and Temperate Benthic Ecosystems
title_full Cell Turnover and Detritus Production in Marine Sponges from Tropical and Temperate Benthic Ecosystems
title_fullStr Cell Turnover and Detritus Production in Marine Sponges from Tropical and Temperate Benthic Ecosystems
title_full_unstemmed Cell Turnover and Detritus Production in Marine Sponges from Tropical and Temperate Benthic Ecosystems
title_short Cell Turnover and Detritus Production in Marine Sponges from Tropical and Temperate Benthic Ecosystems
title_sort cell turnover and detritus production in marine sponges from tropical and temperate benthic ecosystems
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4188633/
https://www.ncbi.nlm.nih.gov/pubmed/25289641
http://dx.doi.org/10.1371/journal.pone.0109486
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