A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores.
Marine coccolithophorid phytoplankton are major producers of biogenic calcite, playing a significant role in the global carbon cycle. Predicting the impacts of ocean acidification on coccolithophore calcification has received much recent attention and requires improved knowledge of cellular calcific...
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ftdoajarticles:oai:doaj.org/article:9467541660b142939ca5487992848b81 2023-05-15T17:50:50+02:00 A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores. Alison R Taylor Abdul Chrachri Glen Wheeler Helen Goddard Colin Brownlee 2011-06-01T00:00:00Z https://doi.org/10.1371/journal.pbio.1001085 https://doaj.org/article/9467541660b142939ca5487992848b81 EN eng Public Library of Science (PLoS) https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21713028/pdf/?tool=EBI https://doaj.org/toc/1544-9173 https://doaj.org/toc/1545-7885 1544-9173 1545-7885 doi:10.1371/journal.pbio.1001085 https://doaj.org/article/9467541660b142939ca5487992848b81 PLoS Biology, Vol 9, Iss 6, p e1001085 (2011) Biology (General) QH301-705.5 article 2011 ftdoajarticles https://doi.org/10.1371/journal.pbio.1001085 2022-12-31T07:39:31Z Marine coccolithophorid phytoplankton are major producers of biogenic calcite, playing a significant role in the global carbon cycle. Predicting the impacts of ocean acidification on coccolithophore calcification has received much recent attention and requires improved knowledge of cellular calcification mechanisms. Uniquely amongst calcifying organisms, coccolithophores produce calcified scales (coccoliths) in an intracellular compartment and secrete them to the cell surface, requiring large transcellular ionic fluxes to support calcification. In particular, intracellular calcite precipitation using HCO₃⁻ as the substrate generates equimolar quantities of H+ that must be rapidly removed to prevent cytoplasmic acidification. We have used electrophysiological approaches to identify a plasma membrane voltage-gated H+ conductance in Coccolithus pelagicus ssp braarudii with remarkably similar biophysical and functional properties to those found in metazoans. We show that both C. pelagicus and Emiliania huxleyi possess homologues of metazoan H(v)1 H+ channels, which function as voltage-gated H+ channels when expressed in heterologous systems. Homologues of the coccolithophore H+ channels were also identified in a diversity of eukaryotes, suggesting a wide range of cellular roles for the H(v)1 class of proteins. Using single cell imaging, we demonstrate that the coccolithophore H+ conductance mediates rapid H+ efflux and plays an important role in pH homeostasis in calcifying cells. The results demonstrate a novel cellular role for voltage gated H+ channels and provide mechanistic insight into biomineralisation by establishing a direct link between pH homeostasis and calcification. As the coccolithophore H+ conductance is dependent on the trans-membrane H+ electrochemical gradient, this mechanism will be directly impacted by, and may underlie adaptation to, ocean acidification. The presence of this H+ efflux pathway suggests that there is no obligate use of H+ derived from calcification for intracellular CO₂ ... Article in Journal/Newspaper Ocean acidification Directory of Open Access Journals: DOAJ Articles PLoS Biology 9 6 e1001085 |
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Directory of Open Access Journals: DOAJ Articles |
op_collection_id |
ftdoajarticles |
language |
English |
topic |
Biology (General) QH301-705.5 |
spellingShingle |
Biology (General) QH301-705.5 Alison R Taylor Abdul Chrachri Glen Wheeler Helen Goddard Colin Brownlee A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores. |
topic_facet |
Biology (General) QH301-705.5 |
description |
Marine coccolithophorid phytoplankton are major producers of biogenic calcite, playing a significant role in the global carbon cycle. Predicting the impacts of ocean acidification on coccolithophore calcification has received much recent attention and requires improved knowledge of cellular calcification mechanisms. Uniquely amongst calcifying organisms, coccolithophores produce calcified scales (coccoliths) in an intracellular compartment and secrete them to the cell surface, requiring large transcellular ionic fluxes to support calcification. In particular, intracellular calcite precipitation using HCO₃⁻ as the substrate generates equimolar quantities of H+ that must be rapidly removed to prevent cytoplasmic acidification. We have used electrophysiological approaches to identify a plasma membrane voltage-gated H+ conductance in Coccolithus pelagicus ssp braarudii with remarkably similar biophysical and functional properties to those found in metazoans. We show that both C. pelagicus and Emiliania huxleyi possess homologues of metazoan H(v)1 H+ channels, which function as voltage-gated H+ channels when expressed in heterologous systems. Homologues of the coccolithophore H+ channels were also identified in a diversity of eukaryotes, suggesting a wide range of cellular roles for the H(v)1 class of proteins. Using single cell imaging, we demonstrate that the coccolithophore H+ conductance mediates rapid H+ efflux and plays an important role in pH homeostasis in calcifying cells. The results demonstrate a novel cellular role for voltage gated H+ channels and provide mechanistic insight into biomineralisation by establishing a direct link between pH homeostasis and calcification. As the coccolithophore H+ conductance is dependent on the trans-membrane H+ electrochemical gradient, this mechanism will be directly impacted by, and may underlie adaptation to, ocean acidification. The presence of this H+ efflux pathway suggests that there is no obligate use of H+ derived from calcification for intracellular CO₂ ... |
format |
Article in Journal/Newspaper |
author |
Alison R Taylor Abdul Chrachri Glen Wheeler Helen Goddard Colin Brownlee |
author_facet |
Alison R Taylor Abdul Chrachri Glen Wheeler Helen Goddard Colin Brownlee |
author_sort |
Alison R Taylor |
title |
A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores. |
title_short |
A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores. |
title_full |
A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores. |
title_fullStr |
A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores. |
title_full_unstemmed |
A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores. |
title_sort |
voltage-gated h+ channel underlying ph homeostasis in calcifying coccolithophores. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2011 |
url |
https://doi.org/10.1371/journal.pbio.1001085 https://doaj.org/article/9467541660b142939ca5487992848b81 |
genre |
Ocean acidification |
genre_facet |
Ocean acidification |
op_source |
PLoS Biology, Vol 9, Iss 6, p e1001085 (2011) |
op_relation |
https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21713028/pdf/?tool=EBI https://doaj.org/toc/1544-9173 https://doaj.org/toc/1545-7885 1544-9173 1545-7885 doi:10.1371/journal.pbio.1001085 https://doaj.org/article/9467541660b142939ca5487992848b81 |
op_doi |
https://doi.org/10.1371/journal.pbio.1001085 |
container_title |
PLoS Biology |
container_volume |
9 |
container_issue |
6 |
container_start_page |
e1001085 |
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1766157734986645504 |