Cargando…

pH Regulation and Tissue Coordination Pathways Promote Calcium Carbonate Bioerosion by Excavating Sponges

Coral reefs are threatened by a multitude of environmental and biotic influences. Among these, excavating sponges raise particular concern since they bore into coral skeleton forming extensive cavities which lead to weakening and loss of reef structures. Sponge bioerosion is achieved by a combinatio...

Descripción completa

Detalles Bibliográficos
Autores principales: Webb, Alice E., Pomponi, Shirley A., van Duyl, Fleur C., Reichart, Gert-Jan, de Nooijer, Lennart J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6345815/
https://www.ncbi.nlm.nih.gov/pubmed/30679551
http://dx.doi.org/10.1038/s41598-018-36702-8
_version_ 1783389631837896704
author Webb, Alice E.
Pomponi, Shirley A.
van Duyl, Fleur C.
Reichart, Gert-Jan
de Nooijer, Lennart J.
author_facet Webb, Alice E.
Pomponi, Shirley A.
van Duyl, Fleur C.
Reichart, Gert-Jan
de Nooijer, Lennart J.
author_sort Webb, Alice E.
collection PubMed
description Coral reefs are threatened by a multitude of environmental and biotic influences. Among these, excavating sponges raise particular concern since they bore into coral skeleton forming extensive cavities which lead to weakening and loss of reef structures. Sponge bioerosion is achieved by a combination of chemical dissolution and mechanical chip removal and ocean acidification has been shown to accelerate bioerosion rates. However, despite the ecological relevance of sponge bioerosion, the exact chemical conditions in which dissolution takes place and how chips are removed remain elusive. Using fluorescence microscopy, we show that intracellular pH is lower at etching sites compared to ambient seawater and the sponge’s tissue. This is realised through the extension of filopodia filled with low intracellular pH vesicles suggesting that protons are actively transported into this microenvironment to promote CaCO(3) dissolution. Furthermore, fusiform myocyte-like cells forming reticulated pathways were localised at the interface between calcite and sponge. Such cells may be used by sponges to contract a conductive pathway to remove chips possibly instigated by excess Ca(2+) at the boring site. The mechanism underlying CaCO(3) dissolution by sponges provides new insight into how environmental conditions can enhance dissolution and improves predictions of future rates of coral dissolution due to sponge activity.
format Online
Article
Text
id pubmed-6345815
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-63458152019-01-29 pH Regulation and Tissue Coordination Pathways Promote Calcium Carbonate Bioerosion by Excavating Sponges Webb, Alice E. Pomponi, Shirley A. van Duyl, Fleur C. Reichart, Gert-Jan de Nooijer, Lennart J. Sci Rep Article Coral reefs are threatened by a multitude of environmental and biotic influences. Among these, excavating sponges raise particular concern since they bore into coral skeleton forming extensive cavities which lead to weakening and loss of reef structures. Sponge bioerosion is achieved by a combination of chemical dissolution and mechanical chip removal and ocean acidification has been shown to accelerate bioerosion rates. However, despite the ecological relevance of sponge bioerosion, the exact chemical conditions in which dissolution takes place and how chips are removed remain elusive. Using fluorescence microscopy, we show that intracellular pH is lower at etching sites compared to ambient seawater and the sponge’s tissue. This is realised through the extension of filopodia filled with low intracellular pH vesicles suggesting that protons are actively transported into this microenvironment to promote CaCO(3) dissolution. Furthermore, fusiform myocyte-like cells forming reticulated pathways were localised at the interface between calcite and sponge. Such cells may be used by sponges to contract a conductive pathway to remove chips possibly instigated by excess Ca(2+) at the boring site. The mechanism underlying CaCO(3) dissolution by sponges provides new insight into how environmental conditions can enhance dissolution and improves predictions of future rates of coral dissolution due to sponge activity. Nature Publishing Group UK 2019-01-24 /pmc/articles/PMC6345815/ /pubmed/30679551 http://dx.doi.org/10.1038/s41598-018-36702-8 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Webb, Alice E.
Pomponi, Shirley A.
van Duyl, Fleur C.
Reichart, Gert-Jan
de Nooijer, Lennart J.
pH Regulation and Tissue Coordination Pathways Promote Calcium Carbonate Bioerosion by Excavating Sponges
title pH Regulation and Tissue Coordination Pathways Promote Calcium Carbonate Bioerosion by Excavating Sponges
title_full pH Regulation and Tissue Coordination Pathways Promote Calcium Carbonate Bioerosion by Excavating Sponges
title_fullStr pH Regulation and Tissue Coordination Pathways Promote Calcium Carbonate Bioerosion by Excavating Sponges
title_full_unstemmed pH Regulation and Tissue Coordination Pathways Promote Calcium Carbonate Bioerosion by Excavating Sponges
title_short pH Regulation and Tissue Coordination Pathways Promote Calcium Carbonate Bioerosion by Excavating Sponges
title_sort ph regulation and tissue coordination pathways promote calcium carbonate bioerosion by excavating sponges
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6345815/
https://www.ncbi.nlm.nih.gov/pubmed/30679551
http://dx.doi.org/10.1038/s41598-018-36702-8
work_keys_str_mv AT webbalicee phregulationandtissuecoordinationpathwayspromotecalciumcarbonatebioerosionbyexcavatingsponges
AT pomponishirleya phregulationandtissuecoordinationpathwayspromotecalciumcarbonatebioerosionbyexcavatingsponges
AT vanduylfleurc phregulationandtissuecoordinationpathwayspromotecalciumcarbonatebioerosionbyexcavatingsponges
AT reichartgertjan phregulationandtissuecoordinationpathwayspromotecalciumcarbonatebioerosionbyexcavatingsponges
AT denooijerlennartj phregulationandtissuecoordinationpathwayspromotecalciumcarbonatebioerosionbyexcavatingsponges