Coccolithophores occupy a special position within the marine phytoplankton because of their production of intricate calcite scales, or coccoliths. Coccolithophores are major contributors to global ...ocean calcification and long-term carbon fluxes. The intracellular production of coccoliths requires modifications to cellular ultrastructure and metabolism that are surveyed here. In addition to calcification, which appears to have evolved with a diverse range of functions, several other remarkable features that likely underpin the ecological and evolutionary success of coccolithophores have recently been uncovered. These include complex and varied life cycle strategies related to abiotic and biotic interactions as well as a range of novel metabolic pathways and nutritional strategies. Together with knowledge of coccolithophore genetic and physiological variability, these findings are beginning to shed new light on species diversity, distribution, and ecological adaptation. Further advances in genetics and functional characterization at the cellular level will likely to lead to a rapid increase in this understanding.
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.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
The Venus flytrap possesses modified leaves that can snap shut fast enough to catch a fly. A new study identifies the major components of the toolkit that allows the flytrap to fire action ...potentials, illustrating how different ion channels and transporters are recruited to give rise to this unique plant behavioural response.
Coccolithophores are important calcifying phytoplankton predicted to be impacted by changes in ocean carbonate chemistry caused by the absorption of anthropogenic CO2. However, it is difficult to ...disentangle the effects of the simultaneously changing carbonate system parameters (CO2, bicarbonate, carbonate and protons) on the physiological responses to elevated CO2.
Here, we adopted a multifactorial approach at constant pH or CO2 whilst varying dissolved inorganic carbon (DIC) to determine physiological and transcriptional responses to individual carbonate system parameters.
We show that Emiliania huxleyi is sensitive to low CO2 (growth and photosynthesis) and low bicarbonate (calcification) as well as low pH beyond a limited tolerance range, but is much less sensitive to elevated CO2 and bicarbonate. Multiple up-regulated genes at low DIC bear the hallmarks of a carbon-concentrating mechanism (CCM) that is responsive to CO2 and bicarbonate but not to pH.
Emiliania huxleyi appears to have evolved mechanisms to respond to limiting rather than elevated CO2. Calcification does not function as a CCM, but is inhibited at low DIC to allow the redistribution of DIC from calcification to photosynthesis. The presented data provides a significant step in understanding how E. huxleyi will respond to changing carbonate chemistry at a cellular level.
Biomineralization by marine phytoplankton, such as the silicifying diatoms and calcifying coccolithophores, plays an important role in carbon and nutrient cycling in the oceans. Silicification and ...calcification are distinct cellular processes with no known common mechanisms. It is thought that coccolithophores are able to outcompete diatoms in Si-depleted waters, which can contribute to the formation of coccolithophore blooms. Here we show that an expanded family of diatom-like silicon transporters (SITs) are present in both silicifying and calcifying haptophyte phytoplankton, including some globally important coccolithophores. Si is required for calcification in these coccolithophores, indicating that Si uptake contributes to the very different forms of biomineralization in diatoms and coccolithophores. Significantly, SITs and the requirement for Si are absent from highly abundant bloom-forming coccolithophores, such as Emiliania huxleyi. These very different requirements for Si in coccolithophores are likely to have major influence on their competitive interactions with diatoms and other siliceous phytoplankton.
Rapid Na+/Ca2+-based action potentials govern essential cellular functions in eukaryotes, from the motile responses of unicellular protists, such as Paramecium 1, 2, to complex animal neuromuscular ...activity 3. A key innovation underpinning this fundamental signaling process has been the evolution of four-domain voltage-gated Na+/Ca2+ channels (4D-Cavs/Navs). These channels are widely distributed across eukaryote diversity 4, albeit several eukaryotes, including land plants and fungi, have lost voltage-sensitive 4D-Cav/Navs 5–7. Because these lineages appear to lack rapid Na+/Ca2+-based action potentials, 4D-Cav/Navs are generally considered necessary for fast Na+/Ca2+-based signaling 7. However, the cellular mechanisms underpinning the membrane physiology of many eukaryotes remain unexamined. Eukaryotic phytoplankton critically influence our climate as major primary producers. Several taxa, including the globally abundant diatoms, exhibit membrane excitability 8–10. We previously demonstrated that certain diatom genomes encode 4D-Cav/Navs 4 but also proteins of unknown function, resembling prokaryote single-domain, voltage-gated Na+ channels (BacNavs) 4. Here, we show that single-domain channels are actually broadly distributed across major eukaryote phytoplankton lineages and represent three novel classes of single-domain channels, which we refer collectively to as EukCats. Functional characterization of diatom EukCatAs indicates that they are voltage-gated Na+- and Ca2+-permeable channels, with rapid kinetics resembling metazoan 4D-Cavs/Navs. In Phaeodactylum tricornutum, which lacks 4D-Cav/Navs, EukCatAs underpin voltage-activated Ca2+ signaling important for membrane excitability, and mutants exhibit impaired motility. EukCatAs therefore provide alternative mechanisms for rapid Na+/Ca2+ signaling in eukaryotes and may functionally replace 4D-Cavs/Navs in pennate diatoms. Marine phytoplankton thus possess unique signaling mechanisms that may be key to environmental sensing in the oceans.
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•Novel class of single-domain, voltage-gated channels (EukCatAs) identified in diatoms•EukCatAs are fast voltage-gated Na+- and Ca2+-permeable channels•EukCatAs underpin voltage-activated Ca2+ signaling and membrane excitability•EukCatAs may have functionally replaced 4D-Cav/Nav channels in pennate diatoms
Diatoms exhibit fast animal-like action potentials, but many species lack 4D-Cav/Nav channels that underpin membrane excitability in animals. Diatoms do encode novel 1D voltage-gated channels (EukCatAs). Helliwell, Chrachri et al. show that EukCatAs are fast Na+ and Ca2+ channels that provide alternative mechanisms for rapid signaling in eukaryotes.
The production of calcium carbonate by coccolithophores (haptophytes) contributes significantly to global biogeochemical cycling. The recent identification of a silicifying haptophyte, Prymnesium ...neolepis, has provided new insight into the evolution of biomineralisation in this lineage. However, the cellular mechanisms of biomineralisation in both calcifying and silicifying haptophytes remain poorly understood. To look for commonalities between these two biomineralisation systems in haptophytes, we have determined the role of actin and tubulin in the formation of intracellular biomineralised scales in the coccolithophore, Coccolithus braarudii and in P. neolepis. We find that disruption of the actin network interferes with secretion of the biomineralised elements in both C. braarudii and P. neolepis. In contrast, disruption of the microtubule network does not prevent secretion of the silica scales in P. neolepis but results in production of abnormally small silica scales and also results in the increased formation of malformed coccoliths in C. braarudii. We conclude that the cytoskeleton plays a crucial role in biomineralisation in both silicifying and calcifying haptophytes. There are some important similarities in the contribution of the cytoskeleton to these different forms of biomineralisation, suggesting that common cellular mechanisms may have been recruited to perform similar roles in both lineages.
Photosynthesis by marine diatoms plays a major role in the global carbon cycle, although the precise mechanisms of dissolved inorganic carbon (DIC) uptake remain unclear. A lack of direct ...measurements of carbonate chemistry at the cell surface has led to uncertainty over the underlying membrane transport processes and the role of external carbonic anhydrase (eCA). Here we identify rapid and substantial photosynthesis-driven increases in pH and CO
primarily due to the activity of eCA at the cell surface of the large diatom Odontella sinensis using direct simultaneous microelectrode measurements of pH and CO
along with modelling of cell surface inorganic carbonate chemistry. Our results show that eCA acts to maintain cell surface CO
concentrations, making a major contribution to DIC supply in O. sinensis. Carbonate chemistry at the cell surface is therefore highly dynamic and strongly dependent on cell size, morphology and the carbonate chemistry of the bulk seawater.
Coccolithophores are unicellular phytoplankton that are characterized by the presence intricately formed calcite scales (coccoliths) on their surfaces. In most cases coccolith formation is an ...entirely intracellular process – crystal growth is confined within a Golgi-derived vesicle. A wide range of coccolith morphologies can be found amongst the different coccolithophore groups. This review discusses the cellular factors that regulate coccolith production, from the roles of organic components, endomembrane organization and cytoskeleton to the mechanisms of delivery of substrates to the calcifying compartment. New findings are also providing important information on how the delivery of substrates to the calcification site is co-ordinated with the removal of H+ that are a bi-product of the calcification reaction. While there appear to be a number of species-specific features of the structural and biochemical components underlying coccolith formation, the fluxes of Ca2+ and a HCO3− required to support coccolith formation appear to involve spatially organized recruitment of conserved transport processes.
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