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.
Highlights
Coccolithophores represent a pan-global group of oceanic phytoplankton, often forming massive monospecific blooms in oceanic waters
C. pelagicus expresses a homologue of animal voltage-gated H+ channels and exhibits an H+-selective conductance that is activated by depolarization and dependent upon the H+ electrochemical gradient
As with metazoan H+ channels [17,28], the properties of the C. pelagicus H+ conductance appear ideally suited to mediating rapid H+ efflux during metabolic acidosis [28]
Summary
Coccolithophores represent a pan-global group of oceanic phytoplankton, often forming massive monospecific blooms in oceanic waters. These unicellular eukaryote algae produce highly intricate calcium carbonate scales, known as coccoliths, and are the most numerous calcifying organisms in our oceans. Abundant species such as Emiliania huxleyi and Coccolithus pelagicus spp braarudii [1] play fundamental roles in long-term carbon deposition, marine biogeochemical cycling, and atmospheric chemistry through their direct effects on surface ocean alkalinity and through ballasting of organic carbon fluxes to deeper waters [2]. Improved knowledge of coccolithophore cell biology is necessary for both predicting the physiological consequences of ocean acidification and identifying experimental versus physiological sources of variability observed in experimental manipulations on this ubiquitous group of phytoplankton
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