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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Autores principales:	Alison R Taylor, Abdul Chrachri, Glen Wheeler, Helen Goddard, Colin Brownlee
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2011
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/9467541660b142939ca5487992848b81
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spelling	oai:doaj.org-article:9467541660b142939ca5487992848b812021-11-18T05:36:08ZA voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores.1544-91731545-788510.1371/journal.pbio.1001085https://doaj.org/article/9467541660b142939ca5487992848b812011-06-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21713028/pdf/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Marine 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 generation. Furthermore, the presence of H(v)1 class ion channels in a wide range of extant eukaryote groups indicates they evolved in an early common ancestor.Alison R TaylorAbdul ChrachriGlen WheelerHelen GoddardColin BrownleePublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 9, Iss 6, p e1001085 (2011)
institution	DOAJ
collection	DOAJ
language	EN
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.
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 generation. Furthermore, the presence of H(v)1 class ion channels in a wide range of extant eukaryote groups indicates they evolved in an early common ancestor.
format	article
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://doaj.org/article/9467541660b142939ca5487992848b81
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A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores.

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