Skip to main content
SpringerLink
Log in

Pigment diversity of coccolithophores in relation to taxonomy, phylogeny and ecological preferences

  • Chapter
Coccolithophores

Summary

Pigment analyses can be employed to study distribution, abundance and composition of natural phytoplankton populations using a chemotaxonomic approach. Cultured haptophytes have played a relevant role in advances in this analytical field and many pigments described in the literature were first detected in members of this algal group. The present chapter provides an historical overview of pigment detection in the Haptophyta and contains new data on their distribution in cultured coccolithophores (some of which not previously cultured), analysed in the context of the EC funded CODENET project. This comparative HPLC study was conducted with the largest (73 monoclonal strains) and most diverse (36 species representing ten families and four orders, including six holococcolithophores) hapto-phyte sample set ever subjected to a comparative study. The observed extraordinary diversity in the pigment composition (based on ten carotenoids, five polar- and three non-polar chlorophyll types) appeared closely related to current taxonomy and published phylogeny. Chi a and the accessory pigments MgDVP, Chl c 2, Ddx, Dtx and β, β-carotene comprised the common haptophyte pigment load. Based on ecological preferences, all species synthesised either Chl c 1 (littoral, benthic or brackish waters) or HFx (open-ocean and non-littoral coastal environments). HFx thus recovered its previously questioned status as a straightforward marker for haptophyte distribution in offshore habitats. Haploid and diploid life-cycle stages (analysed separately for the first time in both Coccolithus and Emilianid) yielded identical pigment compositions. This provided further evidence for an evolutionary origin of pigment content, rather than short-term temporal adaptations to environmental conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Andersen RA, Bidigare RR, Keller MD, Latasa M (1996) A comparison of HPLC pigment signatures and electron microscopic observations for oligotrophic waters of the North Atlantic and Pacific Oceans. Deep-Sea Res II 43: 517–537

    Google Scholar 

  • Arpin N, Svec WA, Liaaen-Jensen S (1976) New fucoxanthin-related carotenoids from Coccolithus huxleyi. Phytochemistry 15: 529–532

    Article  Google Scholar 

  • Baumann KH, Young JR, Cachao M, Ziveri P (2000) Biometric study of Coccolithus pelagicus and its paleoenvironmental utility. J Nannoplankton Res 22: 82

    Google Scholar 

  • Budzikiewicz H, Taraz K (1971) Chlorophyll c. Tetrahedron Lett 27: 1447–1460

    Article  Google Scholar 

  • Carr MR, Tarran GA, Burkill PH (1996) Discrimination of marine phytoplankton species through the statistical analysis of their flow cytometric signatures. J Plankton Res 18: 1225–1238

    Article  Google Scholar 

  • Cros L, Fortuno JM (2002) Atlas of Northwestern Mediterranean Coccolithophores. Sci Mar Supplement 1 66: 1–186

    Google Scholar 

  • Delwiche CF, Palmer JD (1997) The origin of plastids and their spread via second symbiosis. In: Bhattacharya (ed) Origins of algae and their plastids. Springer-Verlag Wien New York, pp 53–86

    Chapter  Google Scholar 

  • Demers S, Roy S, Gagnon R, Vignault C (1991) Rapid light-induced changes in cell fluorescence and in xanthophyll cycle pigments in Alexandrium excavatum (Dinophyceae) and Thalassiosira pseudonana (Bacillariophyceae): a photo-protection mechanism. Mar Ecol Progr Ser 76: 185–193

    Article  Google Scholar 

  • Díez B, Pedros-Alio C, Massana R (2001a) Study of genetic diversity of eukaryotic pico-plankton in different oceanic regions by Small-Subunit rRNA gene cloning and sequencing. Appl Environ Microbiol 67: 2932–2941

    Article  Google Scholar 

  • Díez B, Pedros-Alio C, Marsh TL, Massana R (2001b) Application of denaturing gradient gel electrophoresis (DGGE) to study diversity of marine picoeukaryotic assemblages and comparison of DGGE with other molecular techniques. Appl Environ Microbiol 67: 2942–2951

    Article  Google Scholar 

  • Dougherty RC, Strain HH, Svec WA, Uphaus RA, Katz JJ (1970) The structure properties and distribution of chlorophyll c. J Am Chem Soc 92: 2826–2833

    Article  Google Scholar 

  • Egeland ES, Haxo FT, Guillard RRL, Liaaen-Jensen S (1999) Search for other carotenoids with 3-hydroxy-4-keto-5,6-epoxy end group-carotenoids of an unidentified microalga. Abstracts 12th International Carotenoid Symposium, Cairns, Australia, p 39

    Google Scholar 

  • Egeland ES, Garrido JL, Zapata M, Maestro MA, Liaaen-Jensen S (2000) Algal carotenoids. Part 64. 1 Structure and chemistry of 4-keto-19’-hexanoyloxyfucoxanthin with a novel carotenoid end group. J Chem Soc, Perkin Trans 1: 1223–1230

    Article  Google Scholar 

  • Everitt DA, Wright SW, Volkman JK, Thomas DP, Lindstrom EJ (1990) Phytoplankton community compositions in the western equatorial Pacific determinated from chlorophyll and carotenoid distributions. Deep-Sea Res 37: 975–997

    Article  Google Scholar 

  • Falkowski PG, Raven JA (1997) An introduction to photosynthesis in aquatic systems. In: Falkowski PG, Raven JA (eds) Aquatic Photosynthesis. Blackwell Science, pp 1–32

    Google Scholar 

  • Fawley MW (1989) A new form of chlorophyll c involved in light-harvesting. Plant Physiol 91:727–732

    Article  Google Scholar 

  • Fookes CJR, Jeffrey SW (1989) The structure of chlorophyll c 3 a novel marine photosyn-thetic pigment. J Chem Soc Chem Commun 23: 1827–1828

    Article  Google Scholar 

  • Fresnel J, Billard C (1991) Pleurochrysis placolithoides sp. nov. (Prymnesiophyceae), a new marine coccolithophorid with remarks on the status of Cricolith-bearing species. Brit Phycol J 26: 67–80

    Article  Google Scholar 

  • Fujiwara S, Tsuzuki M, Kawachi M, Minaka N, Inouye I (2001) Molecular phylogeny of the Haptophyta based on the rbcL gene and sequences variation in the spacer region of the rubisco Operon. J Phycol 37: 121–129

    Article  Google Scholar 

  • Garrido JL (1997) Análisis de pigmentos de microalgas marinas mediante cromatografía líquida. Desarrollo metodológica y aplicación al estudio de la dotación pigmentaria de la división Haptophyta. PhD Thesis, University of Vigo, Spain 256 pp

    Google Scholar 

  • Garrido JL, Zapata M (1993) High performance liquid chromatographic separation of polar and non-polar chlorophyll pigments from algae using a wide pore polymeric octadesyl silica column. J High Res Chrom 16: 229–233

    Article  Google Scholar 

  • Garrido JL, Zapata M (1998) Detection of new pigments from Emiliania huxleyi (Prymnesiophyceae) by High-performance liquid chromatography liquid chromatography-mass spectrometry visible spectroscopy and fast atom bombardment mass spectrometry. J Phycol 34: 70–78

    Article  Google Scholar 

  • Garrido JL, Zapata M (in press) Chlorophyll Analysis by New HPLC Methods. In: Grimm B, Porra RJ, Rüdiger W, Scheer H (eds) Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics and Biological Functions. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Garrido JL, Zapata M, Muñiz S (1995) Spectral characterization of new chlorophyll c pigments isolated from Emiliania huxleyi (Prymnesiophyceae) by high performance liquid chromatography. J Phycol 31: 761–768

    Article  Google Scholar 

  • Garrido JL, Otero J, Maestro MA, Zapata M (2000) The main non-polar chlorophyll c form in Emiliania huxleyi (Prymnesiophyceae) is a chlorophyll c 2-monogalactosyl-diacyl-glyceride ester: a mass spectrometry study. J Phycol 36: 497–505

    Article  Google Scholar 

  • Geisen M, Billard C, Broerse ATC, Cros L, Probert I, Young JR (2002) Life-cycle associations involving pairs of holococcolithophorid species: intraspecific variation or cryptic speciation? Eur J Phycol 37: 531–550

    Article  Google Scholar 

  • Gieskes WWC, Kraay GW (1983a) Dominance of Cryptophyceae during the phytoplankton spring bloom in the central North Sea detected by HPLC analysis of pigments. Mar Biol 75: 179–185

    Article  Google Scholar 

  • Gieskes WWC, Kraay GW (1983b) Unknown chlorophyll a derivatives in the North Sea and the tropical Atlantic Ocean revealed by HPLC analysis. Limnol Oceanogr 28: 757–766

    Article  Google Scholar 

  • Gieskes WWC, Kraay GW (1986) Analysis of phytoplankton pigments by HPLC before, during and after mass occurrence of the microflagellate Corymbellus aureus during the spring bloom in the open northern North Sea in 1983. Mar Biol 92: 45–52

    Article  Google Scholar 

  • Holm-Hansen O, Lorenzen CJ, Holmes RW, Strickl, JDH (1965) Fluorometric determination of chlorophyll. J Conseil 301: 3–15

    Article  Google Scholar 

  • Hooks CE, Bidigare RR, Keller MD, Guillard RRL (1988) Coccoid eukaryotic marine ultraplankters with four different HPLC pigment signatures. J Phycol 24: 571–580

    Google Scholar 

  • Inouye I, Chihara M (1983) Ultrastructure and taxonomy of Jomonlithus littoralis gen. et sp. nov. (Class Prymnesiophyceae), a coccolithophorid from the Northwest Pacific. Bot Mag Tokyo 96: 365–376

    Article  Google Scholar 

  • Jeffrey SW (1969) Properties of two spectral different components in chlorophyll c preparations. Biochem Biophys Acta 177: 456–467

    Article  Google Scholar 

  • Jeffrey SW (1972) Preparation and some properties of crystaline chlorophyll c, and c 2 from marine algae. Biochem Biophys Acta 279: 15–33

    Article  Google Scholar 

  • Jeffrey SW (1974) Profiles of photosynthetic pigments in the ocean using thin-layer chromatography. Mar Biol 26: 101–110

    Article  Google Scholar 

  • Jeffrey SW (1981) An improved thin-layer chromatographic technique for marine phytoplankton pigments. Limnol Oceanogr 26: 191–197

    Article  Google Scholar 

  • Jeffrey SW, Allen MB (1964) Pigments growth and photosynthesis in cultures of two Chrysomonads, Coccolithus huxleyi and a Hymenomonas sp. J Gen Microbiol 36: 277–288

    Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrometric equations for determining chlorophylls a, b, c 1 and c 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167: 191–194

    Google Scholar 

  • Jeffrey SW, Vesk M (1997) Introduction to marine phytoplankton and their pigment signatures. In: Jeffrey SW, Mantoura RFC, Wright SW (eds) Phytoplankton pigments in oceanography: guidelines to modern methods. UNESCO Publishing, Paris, pp 37–84

    Google Scholar 

  • Jeffrey SW, Wright SW (1987) A new spectrally distinct component in preparations of chlorophyll c from the microalga Emiliania huxleyi (Prymnesiophyceae). Biochem Biophys Acta 894: 80–188

    Google Scholar 

  • Jeffrey SW, Wright SW (1994) Photosynthetic pigments in the Haptophyta. In: Green J, Leadbeater B (eds) The haptophyte Algae. Oxford University Press Oxford, pp 111–132

    Google Scholar 

  • Jeffrey SW, Mantoura RFC, Bjornland T (1997a) Data for the identification of 47 phyto-plankton pigments In: Jeffrey SW, Mantoura RFC, Wright SW (eds) Phytoplankton pigments in oceanography: guidelines to modern methods. UNESCO Publishing, Paris, pp 449–559

    Google Scholar 

  • Jeffrey SW, Mantoura RFC, Wright SW (1997b) Phytoplankton pigments in oceanography: guidelines to modern methods. UNESCO Publishing, Paris, 661 pp

    Google Scholar 

  • Jensen A, Sakshaug E (1973) Studies on the phytoplankton ecology of the Trondheim Fjord 3 Chloroplasts pigments in relation to abundance and physiological state of the phytoplankton. J Exp Mar Biol Ecol 11: 137–155

    Article  Google Scholar 

  • Keller MD, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. J Phycol 23: 33–638

    Google Scholar 

  • Kirk JTO (1994) Light and photosynthesis in aquatic ecosystems. 2nd ed., Cambridge University Press, Cambridge, 401 pp

    Book  Google Scholar 

  • Latasa M, Van Lenning K, Garrido JL, Scharek R, Estrada M, Rodríguez F, Zapata M (2001) Losses of chlorophylls and carotenoids in aqueous acetone and methanol extracts prepared for RPHPLC analysis of pigments. Chromatographia 53: 85–391

    Article  Google Scholar 

  • Letelier RM, Bidigare RR, Hebel DV, Ondrusek M, Winn CD, Karl DM (1993) Temporal variability of phytoplankton community structure based on pigment analysis. Limnol Oceanogr 38: 1420–1437

    Article  Google Scholar 

  • Liu WL, Marsh TL, Cheng H, Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16rRNA. Appl Environ Microbial 63:4516–4522

    Google Scholar 

  • Loftus ME, Carpenter JH (1971) A fluorimetric method for determining chlorophylls a, b and c. J Mar Res 29: 319–338

    Google Scholar 

  • Lohr M, Wilhelm C (1999) Algae displaying the diadinoxanthin cycle also possess the violaxanthin cycle. Proc. Natl Acad Sci 96: 8784–8789

    Article  Google Scholar 

  • Long SP, Humphries S (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol, Plant Mol Biol 45: 633–662

    Google Scholar 

  • López-García P, Rodriguez-Valera F, Pedros-Alio C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409: 603–607

    Article  Google Scholar 

  • Lorenzen CJ (1967) Determination of chlorophyll and phaeopigments: spectrophotometric equations. Limnol Oceanogr 12: 343–346

    Article  Google Scholar 

  • Mackey MD, Mackey DJ, Higgins HW, Wright SW (1996) CHEMTAX — a program for estimating class abundance from chemical markers: application to HPLC measurements of phytoplankton. Mar Ecol Prog Ser 144: 265–283

    Article  Google Scholar 

  • Mantoura RFC, Jeffrey SW, Llewellyn CA, Claustre H, Morales CE (1997) Comparison between spectrophotometric, fluorometric and HPLC methods for chlorophyll analysis. In: Jeffrey SW, Mantoura RFC, Wright SW (eds) Phytoplankton pigments in oceanography: guidelines to modern methods. UNESCO Publishing Paris, pp 361–380

    Google Scholar 

  • Marsh TL (1999) Terminal restriction fragment length polymorphism (T-RFLP): an emerging method for characterizing diversity among homologous population products. Curr Opin Microbiol 2: 323–327

    Article  Google Scholar 

  • Medlin LK, Kooistra WHCF, Potter D, Saunders JB, Andersen RA (1997) Plant systematics and evolution. Supplementum 11: 187–219

    Google Scholar 

  • Moeseneder MM, Arrieta JM, Muyzer G, Winter C, Herndl GJ (1999) Optimisation of terminal-restriction fragment length polymorphism analysis for complex marine bacte-rioplankton communities and comparison with denaturating gradient gel electrophoresis. Appl Environ Microbiol 65: 3518–3525

    Google Scholar 

  • Moon-Van der Staay SY, De Wächter R, Vaulot D (2001) Oceanic 18S rDNA sequences from picoplankton reveal unexpected eukaryotic diversity. Nature 409: 607–610

    Article  Google Scholar 

  • Murphy LS, Haugen EM (1985) The distribution and abundance of phototrophic ultra-plankton in the North Atlantic. Limnol Oceanogr 30: 47–59

    Article  Google Scholar 

  • Muyzer G (1999) DGGE/TGGE a method for identifying genes from natural communities. Curr Opin Microbiol 2: 317–322

    Article  Google Scholar 

  • Muyzer G, Brinkhoff T, Niibel U, Santegoeds C, Schäfer H, Wawer C (1997) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: Akkermans DL, Van Elsas JD, de Bruijn FJ (eds) Molecular Microbial Ecology Manual Volume 3.4.4. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 1–27

    Google Scholar 

  • Nelson JR, Wakeham SG (1989) A phytol-substituted chlorophyll c from Emiliania huxleyi (Prymnesiophyceae). J Phycol 25: 761–66

    Article  Google Scholar 

  • Norgård S, Svec WA, Liaaen-Jensen S, Jensen A, Guillard RRL (1974) Algal carotenoids and chemotaxonomy. Biochem Syst Ecol 2: 7–9

    Article  Google Scholar 

  • Porra RJ, Pfündel EE, Engel N (1997) Metabolism and function of photosynthetic pigments. In: Jeffrey SW, Mantoura RFC, Wright SW (eds.) Phytoplankton pigments in oceanography – guidelines to modern methods. UNESCO Publishing, Paris, pp 85–126

    Google Scholar 

  • Richards FA, Thomson TG (1952) The estimation and characterization of plankton populations by pigment analysis II, A spectrophotometric method for the estimation of plankton pigments. J Mar Res 11: 156–172

    Google Scholar 

  • Ricketts TR (1966) Magnesium 2,4-divinyl pheoporphyrin a 5 monomethyl ester, a proto-chlorophyll-like pigment present in some unicellular flagellates. Phytochem 5: 223–229

    Article  Google Scholar 

  • Rodriguez F (2001) Aplicación del análisis de pigmentos por cromatografía líquida de alta eficácia (HPLC) ai estúdio de Ia composición y distribución dei fitoplancton marino. Ph.D. Thesis, University of Vigo, Spain, 264 pp

    Google Scholar 

  • Sáez AG, Probert I, Geisen M, Quinn P, Young JR, Medlin LK (2003) Pseudo-cryptic spe-ciation in coccolithophores. PN AS 100: 7163–7168

    Google Scholar 

  • Suzuki M, Rappé MS, Giovannoni S J (1998) Kinetic bias in estimates of coastal picoplankton community structure obtained by measurements of small-subunit rRNA gene PCR amplicon length heterogeneity. Appl Environ Microbiol 64: 4522–4529

    Google Scholar 

  • Van Lenning K (2000) Variability in biomass and structure of phytoplankton populations in the Canary Islands waters, as determined by HPLC analyses of pigments. Ph.D. Thesis, University of Las Palmas de Gran Canária, Spain, 271 pp

    Google Scholar 

  • Van Lenning K, Latasa M, Estrada M, Saez A, Medlin L, Probert I, Véron B, Young J (2003) Pigment signatures and phylogenetic relationships of the Pavlovophyceae (Haptophyta). J Phycol 39: 379–389

    Article  Google Scholar 

  • Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and phaeopigments. Limnol Oceanogr 39: 1985–1992

    Article  Google Scholar 

  • Zapata M, Freire J, Garrido JL (1998) Pigment composition of several harmful algae as determined by HPLC using pyridine-containing mobile phases and a polymeric octa-decylsilica column. In: Reguera B, Blanco J, Fernandez ML, Wyatt T (eds) Harmful Algae. Xunta de Galicia and Intergovernmental Océanographie Commission of UNESCO, Santigago de Compostela, pp 304–307

    Google Scholar 

  • Zapata M, Rodriguez F, Fraga S (2000a) Pigment patterns of toxic and non-toxic Pseudo-nitzschia species (Bacillariophyceae). Harmful Algal Blooms, Ninth Conference, Tasmania

    Google Scholar 

  • Zapata M, Rodriguez F, Garrido JL (2000b) Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed-phase C8 column and pyridine-containing mobile phases. Mar Ecol Prog Ser 195: 29–45

    Article  Google Scholar 

  • Zapata M, Edvardsen B, Rodriguez F, Maestro MA, Garrido JL (2001) Chlorophyll c2 monogalactosyldiacylglyceride ester (chl c2-MGDG) A novel marker pigment for Chrysochromulina species (Haptophyta). Mar Ecol Prog Ser 219: 85–98

    Article  Google Scholar 

  • Zapata M, Garrido JL, Jeffrey SW (in press). Chlorophyll c Pigments: Current Status. In: Grimm B, Porra RJ, Rüdiger W, Scheer H (eds) Chlorophylls and Bacteriochloro-phylls: Biochemistry, Biophysics and Biological Functions. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut de Ciencias del Mar CMIMA-CSIC, Pg. Maritim de la Barceloneta, 37-49, E-08003, Barcelona, Spain

    Kees Van Lenning, Mikel Latasa & Marta Estrada

  2. Laboratory of Marine Biology and Biotechnology, University of Caen, F-14032, Caen, France

    Ian Probert

  3. Palaeontology Department, The Natural History Museum, Cromwell Road, London, SW7 5BD, England

    Jeremy R. Young

Authors
  1. Kees Van Lenning
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ian Probert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mikel Latasa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marta Estrada
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jeremy R. Young
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Geological Institute, ETH-Zentrum, 8092, Zürich, Switzerland

    Hans R. Thierstein

  2. Department of Palaeontology, The Natural History Museum, Cromwell Road, SW7 5BD, London, UK

    Jeremy R. Young

Rights and permissions

Reprints and permissions

Copyright information

© 2004 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Lenning, K.V., Probert, I., Latasa, M., Estrada, M., Young, J.R. (2004). Pigment diversity of coccolithophores in relation to taxonomy, phylogeny and ecological preferences. In: Thierstein, H.R., Young, J.R. (eds) Coccolithophores. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-06278-4_3

Download citation

  • DOI: https://doi.org/10.1007/978-3-662-06278-4_3

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-06016-8

  • Online ISBN: 978-3-662-06278-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation