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A Voltage-Gated H+ Channel Underlying pH Homeostasis in Calcifying Coccolithophores

A Voltage-Gated H+ Channel Underlying pH Homeostasis in Calcifying Coccolithophores
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 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. Furthermore, the presence of Hv1 class ion channels in a wide range of extant eukaryote groups indicates they evolved in an early common ancestor.

1544-9173
e1001085
Falkowski, Paul G.
d2805085-f0d9-4a6a-bf40-0b8a71dc8ea9
Taylor, Alison R.
a20791ff-9a08-4fb9-b484-2e39368f7789
Chrachri, Abdul
4c8a3ca0-7e80-42f4-a3be-dd2dae8583ba
Wheeler, Glen
13488538-691c-438f-88fe-e2d5e0d38278
Goddard, Helen
a52c7fe7-a882-45dd-8da6-309e86c5b9d0
Brownlee, Colin
2af37c1c-b2bf-4832-8370-d9c35e7b3385
Falkowski, Paul G.
d2805085-f0d9-4a6a-bf40-0b8a71dc8ea9
Taylor, Alison R.
a20791ff-9a08-4fb9-b484-2e39368f7789
Chrachri, Abdul
4c8a3ca0-7e80-42f4-a3be-dd2dae8583ba
Wheeler, Glen
13488538-691c-438f-88fe-e2d5e0d38278
Goddard, Helen
a52c7fe7-a882-45dd-8da6-309e86c5b9d0
Brownlee, Colin
2af37c1c-b2bf-4832-8370-d9c35e7b3385

Falkowski, Paul G., Taylor, Alison R., Chrachri, Abdul, Wheeler, Glen, Goddard, Helen and Brownlee, Colin (2011) A Voltage-Gated H+ Channel Underlying pH Homeostasis in Calcifying Coccolithophores. PLoS Biology, 9 (6), e1001085. (doi:10.1371/journal.pbio.1001085).

Record type: Article

Abstract

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. Furthermore, the presence of Hv1 class ion channels in a wide range of extant eukaryote groups indicates they evolved in an early common ancestor.

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Published date: 21 June 2011
Organisations: Ocean and Earth Science

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Local EPrints ID: 340274
URI: https://eprints.soton.ac.uk/id/eprint/340274
ISSN: 1544-9173
PURE UUID: 58b8d476-7126-4799-8367-f6f541ffd5c8

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Date deposited: 18 Jun 2012 13:49
Last modified: 02 Dec 2019 20:57

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