Chlorophyll c Pigments: Current Status

  • Manuel Zapata
  • José L Garrido
  • Shirley W. Jeffrey
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 25)


Chlorophyll (Chl) c pigments are found in nine Divisions of aquatic chromophyte algae, co-occurring with Chl a and carotenoids in chloroplast thylakoids, and in two Divisions of photosynthetic prokaryotes. Chls c differ from Chls a, b and d in being Mg-phytoporphyrins rather than Mg-chlorins. In addition to Chls c 1, c 2 and c 3, many new Chl c-like pigments have recently been isolated and characterized in parallel with advances in separation techniques and spectroscopic methods. Since 1990, the number of known Chls c increased from seven (Chls c 1, c 2, c 3, Chl cCS-170, a Chl c 2-like pigment from Pavlova gyrans, [DV]-PChlide (i.e. MgDVP) and a nonpolar Chl c-like pigment) to eleven compounds. Novel Chls c include [MV]-Chl c 3 from the haptophyte Emiliania huxleyi, a Chl c 1-like pigment from the dinoflagellate Kryptoperidinium foliaceum and two Chl c 2 pigments esterified with monogalactosyl diacylglycerides (MGDG) which have been identified as Chl c 2-MGDG (18:4/14:0) from E. huxleyi and Chl c 2-MGDG (14:0/14:0) from Chrysochromulina polylepis, respectively. In addition, one nonpolar Chl c 1-like pigment has been isolated from Prymnesium parvum. Chl c 2 is the major Chl c pigment found in all Divisions of chromophyte algae, either alone or with significant quantities of Chls c 1 and/or c 3. Chl c diversity is highest in the Haptophyta.


Phytoplankton Pigment Emiliania Huxleyi Rhodomonas Salina Prochlorococcus Marinus HPLC Pigment 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Andersen RA and Mulkey TJ (1983) The occurrence of chlorophylls c 1 and c 2 in the Chrysophyceae. J Phycol 19: 289–294CrossRefGoogle Scholar
  2. Anderson JM and Barrett J (1986) Light-harvesting pigment protein complexes of algae. In: Staehelin LA and Arntzen CAJ (eds) Photosynthesis III. Photosynthetic Membranes and Light Harvesting Systems, pp 269–285, Springer-Verlag, BerlinGoogle Scholar
  3. Beale SI (1984) Biosynthesis of photosynthetic pigments. In: Baker NR and Barber J (eds) Chloroplast Biogenesis, pp 135–205. Elsevier, AmsterdamGoogle Scholar
  4. Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60: 43–73CrossRefGoogle Scholar
  5. Bidigare RR, Kennicutt MC, Ondrusek ME, Keller MD and Guillard RRL (1990) Novel chlorophyll-related compounds in marine phytoplankton: Distributions and geochemical implications. Energy Fuels 4: 653–657CrossRefGoogle Scholar
  6. Bogorad L (1976) Chlorophyll biosynthesis. In: Goodwin TW (ed) Chemistry and Biochemistry of Plant Pigments, pp 64–148. Academic Press Inc, LondonGoogle Scholar
  7. Budzikiewicz H and Taraz K (1971) Chlorophyll c. Tetrahedron 27: 1447–1460CrossRefGoogle Scholar
  8. Caron L, Douady D, De Martino A and Quinet M (2001) Light harvesting in brown algae. Cah Biol Mar 42: 109–124Google Scholar
  9. De Martino A, Douady D, Rousseau B, Duval JC and Caron L (1997) Characterization of two light-harvesting subunits isolated from the brown alga Pelvetia canaliculata: Heterogeneity of xanthophyll distribution. Photochem Photobiol 66: 190–197Google Scholar
  10. Delwiche CF (1999) Tracing the thread of plastid diversity through the tapestry of life. Amer Nat 154: S164–S177CrossRefGoogle Scholar
  11. Dougherty RC, Strain HH, Svec WA, Uphaus RA and Katz JJ (1966) The structure, properties and distribution of chlorophyll c. J Amer Chem Soc 88: 5037–5038CrossRefGoogle Scholar
  12. Dougherty RC, Strain HH, Svec WA, Uphaus RA and Katz JJ (1970) The structure, properties and distribution of chlorophyll c. J Amer Chem Soc 92: 2826–2833CrossRefGoogle Scholar
  13. Durnford DG, Deane JA, Tan S, McFadden GI, Gantt E and Green BR (1999) A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J Mol Evol 48: 59–68PubMedCrossRefGoogle Scholar
  14. Fawley MW (1988) Separation of chlorophylls c 1 and c 2 from pigment extracts of Pavlova gyrans by reversed-phase high performance liquid chromatography. Plant Physiol 86: 76–78PubMedGoogle Scholar
  15. Fawley MW (1989a) A new form of chlorophyll c involved in light-harvesting. Plant Physiol 91: 727–732CrossRefGoogle Scholar
  16. Fawley MW (1989b) Detection of chlorophylls c 1, c 2 and c 3 in pigment extracts of Prymnesium parvum (Prymnesiophyceae). J Phycol 25: 601–604CrossRefGoogle Scholar
  17. Fookes CJR and Jeffrey SW (1989) The structure of chlorophyll c 3, a novel marine photosynthetic pigment. J Chem Soc Chem Commun 23: 1827–1828CrossRefGoogle Scholar
  18. Gantt E, Cunningham FX, Grabowski B and Tan S (1998) Relatedness of carotene-chlorophyll antenna complexes in algae and plants. In Garab G (ed) Photosynthesis: Mechanisms and Effects, Vol I, pp 239–247. Kluwer Academic Publishers, DordrechtGoogle Scholar
  19. Garrido JL and Zapata M (1993) High performance liquid chromatographic separation of polar and non-polar chlorophyll pigments from algae using a wide pore polymeric octadecylsilica column. J High Resolut Chromatogr 16: 229–233CrossRefGoogle Scholar
  20. Garrido JL and Zapata M (1997) Reversed-phase high-performance liquid chromatographic separation of mono- and divinyl chlorophyll forms using pyridine-containing mobile phases and a polymeric octadecylsilica column. Chromato graphia 44: 43–49CrossRefGoogle Scholar
  21. Garrido JL and 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: 70–78CrossRefGoogle Scholar
  22. Garrido JL, Zapata M and Muñiz S (1995) Spectral characterization of new chlorophyll c pigments isolated from Emiliania huxleyi (Prymnesiophyceae) by high-performance liquid chromatography. J Phycol 31: 761–768CrossRefGoogle Scholar
  23. Garrido JL, Otero J, Maestro MA and Zapata M (2000) The main nonpolar chlorophyll c from Emiliania huxleyi (Prymnesiophyceae) is a chlorophyll c 2-monogalactosyl diacylglyceride ester: a mass spectrometry study. J Phycol 36: 497–505CrossRefGoogle Scholar
  24. Gieskes WWC and 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: 45–52CrossRefGoogle Scholar
  25. Goericke R and Repeta DJ (1993) Chlorophylls a and b and divinyl chlorophylls a and b in the open subtropical North Atlantic Ocean. Mar Ecol Prog Ser 101: 307–313Google Scholar
  26. Goericke R, Olson RJ and Shalapyonok A (2000) A novel niche for Prochlorococcus sp. in suboxic environments in the Arabian Sea and the Eastern Tropical North Pacific. Deep-Sea Res I 47: 1183–1205CrossRefGoogle Scholar
  27. Granick S (1949) The pheoporphyrin nature of chlorophyll c. J Biol Chem 179: 505PubMedGoogle Scholar
  28. Green BR and Durnford DG (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 47: 685–714PubMedCrossRefGoogle Scholar
  29. Grossman AR, Bhaya D, Apt KE and Kehoe DM (1995) Lightharvesting complexes in oxygenic photosynthesis: Diversity, control and evolution. Annu Rev Genetics 29: 231–288CrossRefGoogle Scholar
  30. Guillou L, Chrétiennot-Dinet M-J, Medlin LK, Claustre H, Loiseaux-de Goër S and Vaulot D (1999) Bolidomonas: A new genus with two species belonging to a new algal class, the Bolidophyceae (Heterokonta) J Phycol 35: 368–381CrossRefGoogle Scholar
  31. Helfrich M, Ross A, King GC, Turner AG and Larkum AWD (1999) Identification of [8-vinyl]-protochlorophyllide a in phototrophic prokaryotes and algae: Chemical and spectroscopic properties. Biochim Biophys Acta 1410: 262–272PubMedCrossRefGoogle Scholar
  32. Hoober JK and Eggink LL (2001) A potential role of chlorophylls b and c in assembly of light-harvesting complexes. FEBS Lett 489: 1–3PubMedCrossRefGoogle Scholar
  33. Jeffrey SW (1969) Properties of two spectrally different components in chlorophyll c preparations. Biochim Biophys Acta 177: 456–467PubMedGoogle Scholar
  34. Jeffrey SW (1972) Preparation and some properties of crystalline chlorophyll c 1 and c 2 from marine algae. Biochim Biophys Acta 279: 15–33PubMedGoogle Scholar
  35. Jeffrey SW (1976) The occurrence of chlorophyll c 1 and c 2 in algae. J Phycol 12: 349–354CrossRefGoogle Scholar
  36. Jeffrey SW (1989) Chlorophyll c pigments and their distribution in the chromophyte algae. In: Green JC, Leadbeater BSC and Diver WL (eds) The Chromophyte Algae: Problems and Perspectives, pp 13–36. Clarendon Press, OxfordGoogle Scholar
  37. Jeffrey SW (1997a) Structural relationships between algal chlorophylls. In: Jeffrey SW, Mantoura RFC and Wright SW (eds) Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods, pp 566–571. UNESCO Publishing, ParisGoogle Scholar
  38. Jeffrey SW (1997b) Chlorophyll and carotenoid extinction coefficients. In: Jeffrey SW, Mantoura RFC and Wright SW (eds) Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods, pp 595–596. UNESCO Publishing, ParisGoogle Scholar
  39. Jeffrey SW and Anderson JM (2000) Emiliania huxleyi (Haptophyta) holds promising insights for photosynthesis. J Phycol 36: 449–452CrossRefGoogle Scholar
  40. Jeffrey SW and Mantoura RFC (1997) Development of pigment methods for oceanography: SCOR-supported Working Groups and objectives. In: Jeffrey SW, Mantoura RFC and Wright SW (eds) Phytoplankton pigments in oceanography: Guidelines to modern methods, pp 19–36. UNESCO Publishing, ParisGoogle Scholar
  41. Jeffrey SW and Vesk M (1997) Introduction to marine phytoplankton and their pigment signatures. In: Jeffrey SW, Mantoura RFC and Wright SW (eds) Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods, pp 37–84. UNESCO Publishing, ParisGoogle Scholar
  42. Jeffrey SW and Wright SW (1987) A new spectrally distinct component in preparations of chlorophyll c from the microalga Emiliania huxleyi (Prymnesiophyceae). Biochim Biophys Acta 894: 180–188CrossRefGoogle Scholar
  43. Jeffrey SW and Wright SW (1994) Photosynthetic pigments in the Haptophyta. In: Green JC and Leadbeater BSC (eds) The Haptophyte Algae, pp 111–132. Clarendon Press, OxfordGoogle Scholar
  44. Jeffrey SW, Sielicki M and Haxo FT (1975) Chloroplast pigment patterns in dinoflagellates. J Phycol 11: 374–384CrossRefGoogle Scholar
  45. Jeffrey SW and Wright SW (2006) Photosynthetic pigments in marine microalgae: Insights from cultures and the sea. In: Subba Rao DV (ed) Algal Cultures, Analogues of Blooms and Applications. Science Publishers, Enfield, in pressGoogle Scholar
  46. Jeffrey SW, Mantoura RFC and Bjørnland T (1997) Data for the identification of 47 key phytoplankton pigments. In: Jeffrey SW, Mantoura RFC and Wright SW (eds) Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods, pp 449–559. UNESCO Publishing, ParisGoogle Scholar
  47. Jeffrey SW, Wright SW and Zapata M (1999) Recent advances in HPLC pigment analysis of phytoplankton. Mar Freshwater Res 50: 879–896CrossRefGoogle Scholar
  48. Johnsen G and Sakshaug E (1993) Bio-optical characteristics and photoadaptive responses in the toxic and bloom-forming dinoflagellates Gyrodinium aureolum, Gymnodinium galatheanum, and two strains of Prorocentrum minimum. J Phycol 29: 627–642CrossRefGoogle Scholar
  49. Larkum AWD, Scaramuzzi C, Cox GC, Hiller RG and Turner AG (1994) Light-harvesting chlorophyll c-like pigment in Prochloron. Proc Natl Acad Sci USA 91: 679–683PubMedCrossRefGoogle Scholar
  50. Litaker RW, Tester PA, Duke CS, Kenney BE, Pinckney JL and Ramus J (2002). Seasonal niche strategy of the bloom-forming dinoflagellate Heterocapsa triquetra. Mar Ecol Prog Ser: 232: 45–62.Google Scholar
  51. Mantoura RFC and Llewellyn CA (1983) The rapid determination of algal chlorophyll and carotenoid pigments and their breakdown products in natural waters by reverse-phase highperformance liquid chromatography. Anal Chim Acta 151: 297–314CrossRefGoogle Scholar
  52. Miyashita H, Adachi K, Kurano N, Ikemoto H, Chihara M and Miyachi S (1997) Pigment composition of a novel photosynthetic prokaryote containing chlorophyll d as the major chlorophyll. Plant Cell Physiol 38: 274–281Google Scholar
  53. Nelson JR and Wakeham SG (1989) A phytol-substituted chlorophyll c from Emiliania huxleyi (Prymnesiophyceae). J Phycol 25: 761–766CrossRefGoogle Scholar
  54. Oster U, Janaka R, Janake A and Rüdiger W (2000) Cloning and expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliania. Plant J 21: 306–310CrossRefGoogle Scholar
  55. Porra RJ (1997) Recent progress in porphyrin and chlorophyll biosynthesis. Photochem Photobiol. 65: 492–516Google Scholar
  56. Porra RJ, Schäfer W, Cmiel E, Katheder I and Scheer H (1994) The derivation of the formyl group oxygen of chlorophyll b in higher plants from molecular oxygen: achievement of high enrichment of the 7-formyl group oxygen from 18O2 in greening maize leaves. Eur J Biochem 219: 671–679PubMedCrossRefGoogle Scholar
  57. Porra RJ, Pfündel EE and Engel N (1997) Metabolism and function of photosynthetic pigments. In: Jeffrey SW, Mantoura RFC and Wright SW (eds) Phytoplankton pigments in oceanography: Guidelines to modern methods, pp 85–126. UNESCO Publishing, ParisGoogle Scholar
  58. Rebeiz CA, Wu SM, Kuhadja M, Daniell H and Perkins EJ (1983) Chlorophyll a biosynthetic routes and chlorophyll a chemical heterogeneity in plants. Mol Cell Biochem 57: 97–125PubMedCrossRefGoogle Scholar
  59. Rhiel E, Lange W and Mörschel E (1993) The unusual light harvesting complex of Mantoniella squamata: Supramolecular composition and assembly. Biochim Biophys Acta 1143: 163–172PubMedCrossRefGoogle Scholar
  60. Ricketts TR (1966) Magnesium 2,4-divinyl pheoporphyrin a5 monomethyl ester, a protochlorophyll-like pigment present in some unicellular flagellates. Phytochem 5: 223–229CrossRefGoogle Scholar
  61. Scheer H (1991) Chemistry of chlorophylls. In: Scheer H (ed) Chlorophylls, pp 3–30. CRC Press, Boca RatonGoogle Scholar
  62. Shioi Y and Beale SI (1987) Polyethylene-based high-per formance liquid chromatography of chloroplast pigments: reso lution of mono- and divinyl chlorophyllides and other pigment mixtures. Anal Biochem 162: 493–499PubMedCrossRefGoogle Scholar
  63. Stauber JL and Jeffrey SW (1988) Photosynthetic pigments in fifty-one species of marine diatoms. J Phycol 24: 158–172Google Scholar
  64. Strain HH, Cope BT, McDonald GN, Svec WA and Katz JJ (1971) Chlorophylls c 1 and c 2. Phytochem 10: 1109–1114CrossRefGoogle Scholar
  65. Tengs T, Dahlberg OJ, Shalchian-Tabrizi K, Klaveness D, Rudi K, Delwiche CF and Jakobsen KS (2000) Phylogenetic analyses indicate that the 19′ hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Mol Biol Evol 17: 718–729PubMedGoogle Scholar
  66. Van Lenning K, Latasa M, Estrada M, Saez AG, Medlin L, Probert I, Veron B and Young B (2003) Pigment signatures and phylogenetic relationships of the Pavlovophyceae (Haptophyta). J Phycol 39: 379–389Google Scholar
  67. Vesk M and Jeffrey SW (1987) Ultrastructure and pigments of two strains of the picoplanktonic alga Pelagococcus subviridis (Chrysophyceae). J Phycol 23: 322–336Google Scholar
  68. Wasley JWF, Scott WT and Holt AS (1970) Chlorophyllides c. Can J Biochem 48: 376–383PubMedCrossRefGoogle Scholar
  69. Wilhelm C (1987) Purification and identification of chlorophyll c 1 from the green alga Mantoniella squamata. Biochim Biophys Acta 892: 23–29CrossRefGoogle Scholar
  70. Wilhelm C and Wiedemann I (1991) Evidence of protein bound chlorophyll c 3 in a light-harvesting protein isolated from the .agellate alga Prymnesium parvum (Prymnesiophyceae). Photosynthetica 25: 249–255Google Scholar
  71. Wright SW and Van den Enden RL (2000) Phytoplankton community structure and stocks in the East Australian marginal ice zone (BROKE survey, January-March 1996) determined by CHEMTAX analysis of HPLC pigment signatures. Deep-Sea Res II 47: 2363–2400CrossRefGoogle Scholar
  72. Wright SW, Jeffrey SW, Mantoura RFC, Llewellyn CA, Bjørnland T, Repeta D and Welschmeyer N (1991) Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Mar Ecol Prog Ser 77: 183–96Google Scholar
  73. Zapata M and Garrido JL (1997) Occurrence of phytylated chlorophyll c in Isochrysis galbana and Isochrysis sp. (clone T-ISO) (Prymnesiophyceae). J Phycol 33: 209–214CrossRefGoogle Scholar
  74. Zapata M, Ayala AM, Franco JM and Garrido JL (1987) Separation of chlorophylls and their degradation products in marine phytoplankton by reversed-phase high-performance liquid chromatography. Chromatographia 23: 26–30CrossRefGoogle Scholar
  75. Zapata M, Freire J and Garrido JL (1998) Pigment composition of several harmful algae as determined by HPLC using pyridine-containing mobile phases and a polymeric octadecylsilica column. In: Reguera B, Blanco J, Fernández ML and Wyatt T (eds) Harmful Algae, pp 304–307. Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, Santiago de CompostelaGoogle Scholar
  76. Zapata M, Rodríguez F and Garrido JL (2000) Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridinecontaining mobile phases. Mar Ecol Prog Ser 195: 29–45Google Scholar
  77. Zapata M, Edvardsen B, Rodríguez F, Maestro MA and Garrido JL (2001) Chlorophyll c 2 monogalactosyldiacylglyceride ester (chl c 2-MGDG). A novel marker pigment for Chrysochromulina species (Haptophyta). Mar Ecol Prog Ser 219: 85–98Google Scholar
  78. Zapata M, Jeffrey SW, Wright SW, Rodriguez F, Garrido JL and Clementson L (2004) Photosynthetic pigments in 37 species (65 strains) of Haptophyta: Implications for oceanography and chemotaxonomy. Mar Ecol Prog Ser 270: 83–10Google Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Manuel Zapata
    • 1
  • José L Garrido
    • 2
  • Shirley W. Jeffrey
    • 3
  1. 1.Centro de Investigacións Mariñas, Consellería de Pesca, Xunta de GaliciaSpain
  2. 2.Instituto de Investigacións Mariñas de Vigo (CSIC)VigoSpain
  3. 3.CSIRO Division of Marine ResearchAustralia

Personalised recommendations