Emiliania huxleyi and other coccolithophores

Jeremy R. Young, Palaeontology Dept., The Natural History Museum, London SW7 5BD

Coccolithophores are minute (5-20µm) unicellar algae of the Division (or phylum) Haptophyta, characterised by bearing an exoskeleton of calcareous plates, coccoliths. Other haptophytes are non-calcifying, well-known genera include Phaeocystis, Prymnesium, Pavlova and Chrysochromulina. They are all characterised by possessing golden-brown chloroplasts, two smooth flagella and a third flagellum-like organelle the haptonema. The haptonema shows distinctive coiling behaviour and has a quite different microtubular sub-structure to flagella. Molecular genetic data has shown that the Haptophytes are a discrete group from other algal protists, they probably diverged during the Pre-Cambrian (>600Ma) protist radiation and acquired chloroplasts subsequently (possibly in the Late Palaeozoic, ca 300-400Ma) as result of secondary endosymbiosis. Calcification was evolved still later, giving rise to the coccolithophores, both molecular clock and geological evidence suggest this happened in the Early Mesozoic (ca 250Ma).

Ecology
There are several neritic species and one freshwater species but the group is predominantly planktonic with maximum diversity and maximum abundance relative to other phytoplankton in open ocean oligotrophic waters where they are often form a major proportion of the phytoplankton biomass. In eutrophic environments are usually less important, being outcompeted by diatoms in particular. Nonetheless spectacular blooms of one species, Emiliania huxleyi do often occur and have attracted much interest since they are readily detected by satellite imagery as a result of the high reflectivity of the bloom waters. These blooms typically occur in late spring and early summer following onset of stable stratification, and depletion of silicate and phosphate by preceding diatom blooms.

Life-cycle and coccolith types
There are two main types of coccoliths, with quite different modes of biomineralisation. Heterococcoliths are formed of a radial array of complex calcite (CaCO3) crystals and are produced inside the cell. By contrast holococcoliths are formed of numerous minute euhedral crystallites arranged in continuous arrays and calcify outside the cell. It has long been known that both coccolith types are formed by on species, Coccolithus pelagicus in different phases of the life-cycle. More recently it has been shown that this is very common pattern shown by numerous, probably most species, and that the holococcolith phase is consistently haploid whist the heterococcolith bearing phase is diploid. In some species, notably including E.huxleyi, only heterococcoliths are produced, the alternate phase being non-calcifying, the heterococcolith phase is always diploid, however.
Unusually both the haploid and diploid phases of coccolithophores are capable of reproducing asexually more or less indefinitely. Hence a typical coccolithophore species has two well-differentiated life-cycle phases. The haploid phase appears to be adapted to more oligotrophic conditions, is always motile and at least in some cases is mixotrophic. The heterococcolith phase by contrast is often non-motile and probably typically autotrophic and adapted to more eutrophic conditions. It seems likely that the two phase life cycle is a key adaptation of the group although as is often the case with such observations understanding of this adaptation is rather nebulous.

Geological importance
Globally coccolithophores produce phenomenal numbers of coccoliths, being formed of carbonate these only dissolve rather slowly in the water column. Consequently coccolith carbonate accumulates across most of the ocean floor, indeed coccoliths form the single largest component of oceanic oozes. As result they are a significant player in the global carbon cycle and have attracted considerable research interest in consequence. Perhaps less obviously the fossil record of coccoliths is of enormous geological value. As very widespread fossils they are of great value in biostratigraphy, the dating of sedimentary rocks. Indeed a couple of hundred professional geologists are employed worldwide in the oil industry and academic science identifying fossil coccoliths. Key to this is that fact that coccoliths are made of calcite and so show strong interference figures in cross polarised light allowing rapid identification in light microscopy - siliceous or organic fossils this small cannot really be usefully studied. The fossil record of coccoliths is also increasingly used in studies of oceanographic and climate change in the geological record.

Emiliania huxleyi
E. huxleyi is the single most common coccolithophore, in blooms it can reach abundances of several million cells per litre and E. huxleyi blooms occur regularly very year across large areas of the North Atlantic and North Sea. Perhaps even more remarkably E. huxleyi is virtually ubiquitous in surface waters, it occurs at temperatures from near freezing to over 30°C and so from equatorial to arctic latitudes, in lowered and raised salinity conditions (ca 20-40ppt), and in both eutrophic and oligotrophic conditions and throughout the photic zone (ca 0-100m). Indeed a random sampling of surface waters from across the worlds ocean would probably find E. huxleyi present at abundances of >100cells/litre from >90% of samples. This wide occurrence is likely to indicate that it is genetically diverse possibly including multiple cryptic species, as has been inferred from fine scale morphological and culture studies. However, the species is very recently evolved (its’ geological first occurrence is only 250,000 years ago), and no differentiation has been detected in stable genes. Hence it is a rather remarkable indicator of rapid evolutionary diversification.

It also is an easily cultured species and can be found in most algal culture collections. Consequently it has become something of a laboratory rat species, it is the default coccolithophore in comparative studies and the process and biochemistry of calcification in it has been widely studied. During the 1990s the species was successfully used as the focus of interdisciplinary studies lead by Prof Peter Westbroek - the EHUX and GEM projects.

Information
EHUX web site - a multi-authored site exploring the disparate strands of research on this species. A very valuable resource.
http://www.soc.soton.ac.uk/SOES/STAFF/tt/eh/

International Nannoplankton Association - home site of the INA, the society for coccolithophore study. Includes terminology guide, generic-level classification, details of email list, comprehensive links.
http://www.nhm.ac.uk/hosted_sites/ina/index.html

CODENET - website from recent EU project on coccolithophores, includes listing of largest available culture collection.
http://www.nhm.ac.uk/hosted_sites/ina/CODENET/index.html

Images
Remote sensing of coccolithophore blooms images

EMIDAS - the largest online database of coccolithophore images, from ETH-Zurich
http://www.emidas.ethz.ch/

CODENET Guide images - rapidly browsable collection of selected images illustrating extant coccolithophores.
http://www.nhm.ac.uk/hosted_sites/ina/CODENET/GuideImages/index.html

Calcite Palace - large collection of images of fossil species.
http://www.nhm.ac.uk/hosted_sites/ina/CalcitePalace/index.htm

Nannoplankton in colour - some elegant false-coloured SEM images
http://www.nhm.ac.uk/hosted_sites/ina/colourcoccos/index.htm

References
this list gives the most recent and useful reviews and will form a guide into other literature.
Bown, P.R., 1998. Calcareous Nannofossil Biostratigraphy. British Micropalaeontological Society Publication Series. Chapman & Hall, 315 pp. -- Key synthesis of data on fossil coccoliths.

Cros, L. and Fortuño, J.-M., 2002. Atlas of northwestern Mediterranean coccolithophores. Scientia Marina, 66 (suppl. 1): 7-182. -- Beautifully illustrated monograph of modern species.

Green J.C. and Leadbeater B.S.C. (Editors) 1994. The Haptophyte Algae. Systematics Association Special Volumes. Clarendon Press, Oxford, pp. 1-21. -- review volume focused on cell biology and systematics.

Paasche, E., 2002. A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions. Phycologia, 40(6): 503-529. -- Review paper on E. huxleyi, an excellent introduction to research on this species and the literature on it.

Winter, A. and Siesser, W.G., 1994. Coccolithophores. Cambridge University Press, Cambridge. -- Review volume, focused on biodiversity, ecology and sedimentation.

Young, J.R., Davis, S.A., Bown, P.R. and Mann, S., 1999. Coccolith ultrastructure and biomineralisation. Journal of Structural Biology, 126: 195-215. -- Review of biomineralisation.

Young, J.R. and Thierstein, H.R. (Editors), 2000. Nannoplankton ecology and palaeoecology. Proceedings of the INA7 conference, Puerto Rico 1998. Marine Micropaleontology, 39, 1-316 pp-- Proceedings volume with numerous papers on modern coccolithophores.

E huxleyi blooms along the shelf break off the NW European coast, May 21 2001.	Rhabdosphaera clavigera	Syracosphara anthos heterococcolith phase
Emiliania huxleyi	Syracosphara anthos holococcolith phase - formerly known as Periphyllophora mirabilis.	Michaelsarsia elegans