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Coccolithophore biomineralization: New questions, new answers

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coccolithophore biomineralization new questions
2 the essentials of coccolithophore calcification
the determinants of coccolith morphology

Institution Coccolithophore biomineralization
Course Coccolithophore biomineralization

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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

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