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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ftpubmed:oai:pubmedcentral.nih.gov:3119654 2023-05-15T17:50:48+02:00 A Voltage-Gated H+ Channel Underlying pH Homeostasis in Calcifying Coccolithophores Taylor, Alison R. Chrachri, Abdul Wheeler, Glen Goddard, Helen Brownlee, Colin 2011-06 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3119654 http://www.ncbi.nlm.nih.gov/pubmed/21713028 https://doi.org/10.1371/journal.pbio.1001085 en eng Public Library of Science http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3119654 http://www.ncbi.nlm.nih.gov/pubmed/21713028 http://dx.doi.org/10.1371/journal.pbio.1001085 Taylor et al. 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 credited. CC-BY Research Article Text 2011 ftpubmed https://doi.org/10.1371/journal.pbio.1001085 2013-09-03T16:16:32Z 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 Hv1 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 Hv1 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 generation. ... Text Ocean acidification PubMed Central (PMC) PLoS Biology 9 6 e1001085 |
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Research Article Taylor, Alison R. Chrachri, Abdul Wheeler, Glen Goddard, Helen Brownlee, Colin A Voltage-Gated H+ Channel Underlying pH Homeostasis in Calcifying Coccolithophores |
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Research Article |
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 Hv1 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 Hv1 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 generation. ... |
format |
Text |
author |
Taylor, Alison R. Chrachri, Abdul Wheeler, Glen Goddard, Helen Brownlee, Colin |
author_facet |
Taylor, Alison R. Chrachri, Abdul Wheeler, Glen Goddard, Helen Brownlee, Colin |
author_sort |
Taylor, Alison R. |
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 |
publishDate |
2011 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3119654 http://www.ncbi.nlm.nih.gov/pubmed/21713028 https://doi.org/10.1371/journal.pbio.1001085 |
genre |
Ocean acidification |
genre_facet |
Ocean acidification |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3119654 http://www.ncbi.nlm.nih.gov/pubmed/21713028 http://dx.doi.org/10.1371/journal.pbio.1001085 |
op_rights |
Taylor et al. 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 credited. |
op_rightsnorm |
CC-BY |
op_doi |
https://doi.org/10.1371/journal.pbio.1001085 |
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PLoS Biology |
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9 |
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6 |
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e1001085 |
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1766157707111301120 |