Coccolithophore biomineralization: New questions, new answers
Colin Brownleea*, Glen Wheelera and Alison R Taylorb
From the aMarine Biological Association, The Laboratory, Citadel Hill, Plymouth PL1 2PB,
UK and bDepartment of Biology and Marine Biology, University of North Carolina Wilmington,
North Carolina 28403, USA
Summary
Coccolithophores are unicellular phytoplankton that are characterised by the presence
intricately formed calcite scales (coccoliths) on their surfaces. 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 organisation 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 organised recruitment of conserved
transport processes.
© 2015. This manuscript version is made available under the Elsevier user license
http://www.elsevier.com/open-access/userlicense/1.0/
, 1. Introduction
Coccolithophores are single celled marine photosynthetic protists belonging to the
Haptophyte division of the chromalveolate eukaryotes. They are significant components of
the marine phytoplankton with certain species, such as the cosmopolitan Emiliania huxleyi
able to form massive blooms in temperate and sub-polar waters. Because of this their
ecology, physiology and palaeontology have been well-studied. Coccolithophores also
present a paradigm for the study of calcification mechanisms. The ease with which certain
species can be cultured, he relative tractability of a unicellular calcification system that
produces intricate calcium carbonate structures (coccoliths) allows questions relating to the
biological control of crystal formation and morphology to be addressed.
Coccolithophore calcification has received considerable attention in recent years with many
studies directed to the potential impacts of ocean acidification – the decrease in ocean pH
associated with the dissolution of anthopogenically-derived CO2 into the surface ocean.
While these studies have generally not directly addressed questions relating to better
mechanistic understanding of coccolithophore calcification, they have revealed a number of
features of coccolithophore biology (e.g. strain variability, plasticity of calcification response,
genetic adaptation, species differences) that are pertinent to the calcification mechanism
[e.g. 1-3]. Nevertheless, important questions remain to be answered in order to fully
elucidate the cellular drivers and regulators of calcification that are essential for
understanding the roles of coccolithophores in the ecology of the oceans, predicting
responses to changing ocean chemistry and realising the potential of coccolithophores for
biotechnological applications.
2. The essentials of coccolithophore calcification
Well preserved coccoliths can be found well preserved in sedimentary records 220 Ma and
molecular clock studies estimate that the first calcifying haptophytes (calcihaptophytes)
, originated ~330 Ma [4]. This suggests that coccolithophores evolved under ocean carbonate
chemistry conditions that were significantly different from those of the present day. Most
studies of coccolithophore calcification mechanisms have focussed on the ―model‖ species
E. huxleyi which is easily isolated and cultured, with a large body of physiological data
derived from culture experiments. These advantages, together with a fully sequenced
genome [5] and an array of additional genomic resources have led to significant advances in
understanding the biology and physiology of coccolithophores.The calcite coccoliths of
diploid E. huxleyi cells are exquisitely sculpted complex multi- crystalline plates that are
formed via crystal growth, uniquely, in an intracellular compartment, the coccolith vesicle
(CV). Mature coccoliths are secreted to the cell surface where they form an outer coat
(coccosphere) (Figure 1). In many species (with the exception of E. huxleyi) the haploid
phase produces simpler holococcoliths, formed from rhomohedral crystalline units most
likely, in an extracellular space [6]. Nevertheless, the diploid heterococcolith producing life
cycle stage represents the diploid calcifying stage that is predominantly found in natural
populations and is the dominates production of particulate inorganic carbon in the oceans.
3. The determinants of coccolith morphology.
The wide range of coccolith shapes and sizes produced by different species suggests a
range of functional roles as well as species-specific cellular factors that determine coccolith
morphology. In order to understand the regulation of coccolith morphology it is necessary to
understand the cell structures and physiology that are brought into play during coccolith
development. Ultrastructural studies of E. huxleyi show the CV to be derived from Golgi
cisternae [7]. Coccolith growth proceeds as the CV matures and completed coccoliths are
secreted to the cell surface in a single exocytotic event [8]. Coccolith growth begins with the
nucleation of calcite crystals with alternating orientations (V and R units) in a circular
arrangement known as the protococcolith ring [7]. The coccolith matures into a distal
(upper) shield and outer tube formed of V-units. The lower proximal shield, inner tube and
central area elements are derived from R-units. The two unit types alternate with each other
Colin Brownleea*, Glen Wheelera and Alison R Taylorb
From the aMarine Biological Association, The Laboratory, Citadel Hill, Plymouth PL1 2PB,
UK and bDepartment of Biology and Marine Biology, University of North Carolina Wilmington,
North Carolina 28403, USA
Summary
Coccolithophores are unicellular phytoplankton that are characterised by the presence
intricately formed calcite scales (coccoliths) on their surfaces. 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 organisation 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 organised recruitment of conserved
transport processes.
© 2015. This manuscript version is made available under the Elsevier user license
http://www.elsevier.com/open-access/userlicense/1.0/
, 1. Introduction
Coccolithophores are single celled marine photosynthetic protists belonging to the
Haptophyte division of the chromalveolate eukaryotes. They are significant components of
the marine phytoplankton with certain species, such as the cosmopolitan Emiliania huxleyi
able to form massive blooms in temperate and sub-polar waters. Because of this their
ecology, physiology and palaeontology have been well-studied. Coccolithophores also
present a paradigm for the study of calcification mechanisms. The ease with which certain
species can be cultured, he relative tractability of a unicellular calcification system that
produces intricate calcium carbonate structures (coccoliths) allows questions relating to the
biological control of crystal formation and morphology to be addressed.
Coccolithophore calcification has received considerable attention in recent years with many
studies directed to the potential impacts of ocean acidification – the decrease in ocean pH
associated with the dissolution of anthopogenically-derived CO2 into the surface ocean.
While these studies have generally not directly addressed questions relating to better
mechanistic understanding of coccolithophore calcification, they have revealed a number of
features of coccolithophore biology (e.g. strain variability, plasticity of calcification response,
genetic adaptation, species differences) that are pertinent to the calcification mechanism
[e.g. 1-3]. Nevertheless, important questions remain to be answered in order to fully
elucidate the cellular drivers and regulators of calcification that are essential for
understanding the roles of coccolithophores in the ecology of the oceans, predicting
responses to changing ocean chemistry and realising the potential of coccolithophores for
biotechnological applications.
2. The essentials of coccolithophore calcification
Well preserved coccoliths can be found well preserved in sedimentary records 220 Ma and
molecular clock studies estimate that the first calcifying haptophytes (calcihaptophytes)
, originated ~330 Ma [4]. This suggests that coccolithophores evolved under ocean carbonate
chemistry conditions that were significantly different from those of the present day. Most
studies of coccolithophore calcification mechanisms have focussed on the ―model‖ species
E. huxleyi which is easily isolated and cultured, with a large body of physiological data
derived from culture experiments. These advantages, together with a fully sequenced
genome [5] and an array of additional genomic resources have led to significant advances in
understanding the biology and physiology of coccolithophores.The calcite coccoliths of
diploid E. huxleyi cells are exquisitely sculpted complex multi- crystalline plates that are
formed via crystal growth, uniquely, in an intracellular compartment, the coccolith vesicle
(CV). Mature coccoliths are secreted to the cell surface where they form an outer coat
(coccosphere) (Figure 1). In many species (with the exception of E. huxleyi) the haploid
phase produces simpler holococcoliths, formed from rhomohedral crystalline units most
likely, in an extracellular space [6]. Nevertheless, the diploid heterococcolith producing life
cycle stage represents the diploid calcifying stage that is predominantly found in natural
populations and is the dominates production of particulate inorganic carbon in the oceans.
3. The determinants of coccolith morphology.
The wide range of coccolith shapes and sizes produced by different species suggests a
range of functional roles as well as species-specific cellular factors that determine coccolith
morphology. In order to understand the regulation of coccolith morphology it is necessary to
understand the cell structures and physiology that are brought into play during coccolith
development. Ultrastructural studies of E. huxleyi show the CV to be derived from Golgi
cisternae [7]. Coccolith growth proceeds as the CV matures and completed coccoliths are
secreted to the cell surface in a single exocytotic event [8]. Coccolith growth begins with the
nucleation of calcite crystals with alternating orientations (V and R units) in a circular
arrangement known as the protococcolith ring [7]. The coccolith matures into a distal
(upper) shield and outer tube formed of V-units. The lower proximal shield, inner tube and
central area elements are derived from R-units. The two unit types alternate with each other
