Antenna Systems of Red Algae: Phycobilisomes with Photosystem ll and Chlorophyll Complexes with Photosystem I

  • Elisabeth Gantt
  • Beatrice Grabowski
  • Francis X. CunninghamJr.
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 13)


Red algae have two types of light-harvesting antennas: the phycobilisome which is directly connected to the reaction centers of Photosystem II, and a LHC I complex connected to the reaction centers of PS I. The structure of red algal phycobilisomes is much like those of cyanobacteria, with a central allophycocyanin core surrounded by phycocyanin and with phycoerythrin on the periphery. In many reds the phycobilisome size is larger due mainly to a greater phycoerythrin content. The presence of LHC I may be regarded as a considerable advance in extending the light absorbing capacity in photosynthetic eukaryotes; an exception exists in the glaucocystophytes where LHC complexes have not yet been found. Chlorophyll a is the only type of chlorophyll present, while the presence of chlorophyll d is still in doubt. Zeaxanthin, and sometimes lutein, is the predominant carotenoid. Though zeaxanthin does not appear to function as an antenna pigment, in vitro reconstitution studies show its necessity for LHC stability and chlorophyll insertion. Phylogenetic relatedness of rhodophyte LHCs with those of higher plants, chromophytes, and dinophytes is evident in the high conservation of critical residues in three intrinsic membrane regions and in the successful reconstitution of red algal LHC polypeptides with pigments of other groups. Convincing evidence for excitation energy transfer between PS I and PS II is lacking. Photoacclimation to high light intensity is manifested by a per cell reduction of thylakoid area and chlorophyll, a decrease in the phycoerythrin content per phycobilisome, and a decline in LHC I polypeptides. In cells acclimated to light absorbed primarily by chlorophyll (red) the RC 1 content decreases and the RC 2 increases, in contrast to the opposite response with phycobilisome-absorbing green light. Complementary chromatic adaptation to red or green light, i.e. changes in phycobilisome pigments as in certain cyanobacteria, does not occur in reds.


Porphyridium Cruentum Pigment Binding Linker Polypeptide Cyanidium Caldarium Complementary Chromatic Adaptation 
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.









linker polypeptide for phycobilisome core-thylakoid association


light-harvesting complex

LhcaRl, LhcaR2

genes encoding LHC I polypeptides of red algae


light-harvesting complex of PS I




absorbance change used to assay PS I activity


phycocyanin (Cyanophycean: C-PC, Rhodophycean: R- PC)


phycoerythrin (Bangiophycean: large (B-PE) or small (b-PE) mol. wt., Rhodophycean: large (R-PE) or small (r-PE) mol. wt.)


Photosystem I


Photosystem II


primary acceptor of PS II

RC 1

reaction center of PS I

RC 2

reaction center of PS II




Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aizawa K, Tan S and Gantt E (1997) Rapid separation and analysis of chlorophyll-proteins from the red alg & Porphyridium cruentum. Proceedings of the First Annual Meeting Japanese Soc Marine Biotechnol 1: 69AGoogle Scholar
  2. Algarra P, Thomas J-C and Mousseau A (1990) Phycobilisome heterogeneity in the red alga Porphyra umbilicalis. Plant Physiol 92: 570–576PubMedCrossRefGoogle Scholar
  3. Apt KE, Hoffman NE and Grossman AR (1993) The gamma subunit of R-phycoerythrin and its possible mode of transport into the plastid of red algae. J Biol Chem 268: 16208–16215PubMedGoogle Scholar
  4. Apt KE, Collier JL and Grossman AR (1995) Evolution of the phycobiliproteins. J Mol Biol 248: 79–96PubMedCrossRefGoogle Scholar
  5. Bassi R, Croce R, Cugini D and Sandona D (1999) Mutational analysis of a higher plant antenna protein provides identification of chromophores bound into multiple sites. Proc Natl Acad Sci USA 96: 10056–10061PubMedCrossRefGoogle Scholar
  6. Bernard C, Etienne A-L and Thomas J-C (1996) Synthesis and binding of phycoerythrin and its associated linkers to the phycobilisome in Rhodella violacea ( Rhodophyta ): Compared effects of high light and translation inhibitors. J Phycol 32: 265–271Google Scholar
  7. Biggins J, Campbell CL and Bruce D (1984) Mechanism of the light state transition in photosynthesis II. Analysis of phosphorylated polypeptides in the red alga Porphyridium cruentum. Biochim Biophys Acta 767: 138–144.CrossRefGoogle Scholar
  8. Bruce D, Hanzlick CA, Hancock LE, Biggins J and Knox RS (1986) Energy distribution in the photochemical apparatus of Porphyridium cruentum: Picosecond fluorescence spectroscopy of cells in state 1 and state 2 at 77 K. Photosynth Res 10: 283–290CrossRefGoogle Scholar
  9. Bryant DA (1991) Cyanobacterial phycobilisomes: Progress toward complete structural and functional analysis via molecular genetics. In: Bogorad L and Vasil IL (eds) Cell Cultures and Somatic Cell Genetics of Plants, Vol 7B: The Photosynthetic Apparatus: Molecular Biology and Operation, pp 257–300. Academic Press, San DiegoCrossRefGoogle Scholar
  10. Cavalier-Smith T (1993) Kingdom protozoa and its 18 phyla. Microbiol Rev 57: 953–994PubMedGoogle Scholar
  11. Cunningham FX, Jr, Dennenberg RJ, Mustardy L, Jursinic PA and Gantt E (1989) Stoichiometry of Photosystem I, Photosystem II, and phycobilisomes in the red alga Porphyridium cruentum as a function of growth irradiance. Plant Physiol 91: 1179–1187PubMedCrossRefGoogle Scholar
  12. Cunningham FX, Jr, Dennenberg RJ, Jursinic PA and Gantt E (1990) Growth under red light enhances Photosystem II relative to Photosystem I and phycobilisomes in the red alga Porphyridium cruentum. Plant Physiol 93: 888–895PubMedCrossRefGoogle Scholar
  13. Delphin E, Duval J-C, Etienne A-L and Kirilovsky D (1996) State transitions or A-pH dependent quenching of Photosystem II fluorescence in red algae. Biochemistry 35: 9435–9445PubMedCrossRefGoogle Scholar
  14. Delphin E, Duval J-C, Etienne A-L and Kirilovsky D (1998) ApH-dependent Photosystem II fluorescence quenching induced by saturating, multiturnover pulses in red algae. Plant Physiol 118: 103–113PubMedCrossRefGoogle Scholar
  15. Delphin E, Duval J-C and Kirilovsky D (1995) Comparison of state 1-state 2 transitions in the green alga Chlamydomonas reinhardtii and in the red alga Rhodella violacea: Effect of kinase and phosphatase inhibitors. Biochim Biophys Acta 1232: 91–95Google Scholar
  16. Delwiche C, Kuhsel M and Palmer JD (1995) Phylogenetic analysis of tufk sequences indicates a cyanobacterial origin of all plastids. Mol Phylogeny and Evol 4: 110–128CrossRefGoogle Scholar
  17. 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 forplastid evolution. J Molec Evolution 48: 59–68.CrossRefGoogle Scholar
  18. Enami I, Murayama H, Ohta H, Kamo M, Nakazato K, Sehn J-R (1995) Isolation and characterization of a Photosystem II complex from the red alga Cyanidium caldarium: Association of cytochrome c-550 and a 12 kDa protein with the complex. Biochim Biophys Acta. 1232: 208–216.PubMedCrossRefGoogle Scholar
  19. Ficner R, Huber R (1993) Refined crystal structure of phycoerythrin from Porphyridium cruentum at 0.23 nm resolution and localization of the a-subunit. Eur J Biochem 218: 103–106PubMedCrossRefGoogle Scholar
  20. Gantt E (1980) Structure and function of phycobilisomes: Light harvesting pigment complexes in red and blue-green algae. Intl Rev Cytol 66: 45–80CrossRefGoogle Scholar
  21. Gantt E (1986) Phycobilisomes. In: Staehelin LA and Arntzen CJ (eds) Encyclopedia of Plant Physiology. Photosynthetic Membranes and Light-Harvesting Systems: Photosystem III, 19: 260–268.Google Scholar
  22. Springer-Verlag, Berlin Gantt E (1990) Pigmentation and photoacclimation. In Cole KM and Sheath RG (eds) Biology of the Red Algae, pp 203–219. Cambridge University Press, CambridgeGoogle Scholar
  23. Gantt E (1996) Pigment protein complexes and the concept of the photosynthetic unit: Chlorophyll complexes and phycobilisomes. Photosynth Res 48: 47–53.CrossRefGoogle Scholar
  24. Glazer AN (1985) Light harvesting by phycobilisomes. Annu Rev Biophys Chem 14: 47–77CrossRefGoogle Scholar
  25. Glazer AN (1989) Light guides. Directional energy transfer in a photosynthetic antenna. J Biol Chem 264: 1–4PubMedGoogle Scholar
  26. Glazer AN, Chan CF and JA West (1997) An unusual phycocyanobilin-containing phycoerythrin of several bluish-colored, acrochaetoid, freshwater red algal species. J Phycol 33: 617–624CrossRefGoogle Scholar
  27. Grabowski B, Tan S, Cunningham FX, Jr and Gantt, E (2000) Characterization of the Porphyridium cruentum Chi a-binding LHC by in vitro reconstitution: LHCaRl binds 8 Chi a molecules and proportionately more carotenoids than CAB proteins. Photosynth Res 63: 85–96PubMedCrossRefGoogle Scholar
  28. Grabowski B, Cunningham FX, Jr and Gantt, E (2001) Chlorophyll and carotenoid binding in a simple red algal LHC crosses phylogenetic lines. Proc Natl Acad Sci USA. 98: 2911–2916PubMedCrossRefGoogle Scholar
  29. Green BR (2001) Was ‘molecular opportunism’ a factor in the evolution of different photosynthetic light-harvesting systems? Proc Natl Acad Sci USA. 98: 2119–2121PubMedCrossRefGoogle Scholar
  30. Green BR and Durnford (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Ann Rev Plant Physiol Plant Molec Biol 47: 685–714CrossRefGoogle Scholar
  31. Green BR and Kiihlbrandt W (1995) Sequence conservation of light-harvesting and stress-response proteins in relation to the 3-dimensional molecular-structure of LHCII. Photosynth Res 44: 139–148CrossRefGoogle Scholar
  32. Grossman AR, Bhaya D, Apt KE and Kehoe DM (1995) Light-harvesting complexes in oxygenic photosynthesis: Diversity, control, and evolution. Annu Rev Genet 29: 231–88Google Scholar
  33. Hanelt D, Huppertz K and Nultsch W (1992) Photoinhibition of photosynthesis and its recovery in red algae. Bot Acta 105: 278–284Google Scholar
  34. Jeffrey SW, Mantoura RFC and Wright SW (eds) (1997) Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods, UNESCO, ParisGoogle Scholar
  35. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W and Krauss N (2001) Three-dimensional structure of cyanobacterial Photosystem I at 2.5 A resolution. Nature 411: 909–917PubMedCrossRefGoogle Scholar
  36. Kiihlbrandt W, Wang DN and Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614–621CrossRefGoogle Scholar
  37. Koike H, Shibata M, Yasutomi K, Kashino Y and K Satoh (2001) Identification of Photosystem I components from a glauco-cystophyte, Cyanophoraparadoxal the PsaD protein has anNterminal stretch homologous to higher plants. Photosynth Res 65: 207–217CrossRefGoogle Scholar
  38. Lee YK and Vonshak A (1988) The kinetics of photoinhibition and its recovery in the red alga Porphyridium cruentum. Arch Microbiol 150: 529–533CrossRefGoogle Scholar
  39. Levy I and Gantt E (1988) Light acclimation of Porphyridium purpureum (Rhodophyta): Growth, photosynthesis, and phycobilisomes. J Phycol 24: 452–458Google Scholar
  40. Ley AC (1984) Effective absorption cross-sections in Porphyridium cruentum. Implications for energy transfer between phycobilisomes and Photosystem II reaction centers. Plant Physiol 74: 451–454PubMedCrossRefGoogle Scholar
  41. Loffelhardt W, Bohnert HJ and Bryant Da (1997) The cyanelles of Cyanophoraparadoxa. Critical Rev Plant Sci 16: 393–413CrossRefGoogle Scholar
  42. Liining K (1993) Environmental and internal control of seasonal growth in seaweeds. Hydrobiologia 260 /262: 1–14CrossRefGoogle Scholar
  43. MacColl R and Guard-Friar D (1987) Phycobiliproteins. CRC Press, Boca Raton Manning WM and Strain HH (1943) Chlorophyll d, a green pigment of red algae. J Biol Chem 151: 1–19Google Scholar
  44. Marquardt J (1998) Effects of carotenoid depletion on the photosynthetic apparatus of Galdieria sulphuraria (Rhodophyta) strain that retains its photosynthetic apparatus in the dark. J Plant Physiol 152: 372–380CrossRefGoogle Scholar
  45. Marquardt J and Rhiel E (1997) The membrane-intrinsic light-harvesting complex of the red alga Galdieria sulphuraria (formerly Cyanidium caldarium): Biochemical and immunochemical characterization. Biochim et Biophys Acta 1320: 153–164.CrossRefGoogle Scholar
  46. Marquardt J, Wans S, Rhiel E, Randolf A and Krumbein WE (2000) Intron-exon structure and gene copy number of a gene encoding for a membrane intrinsic light-harvesting polypeptide of the red alga Galdieria sulphuraria. Gene 255: 257–265PubMedCrossRefGoogle Scholar
  47. Marquardt J, Lutz B, Wans S, Rhiel E and Krumbein WE (2001) The gene family coding for the light-harvesting poypetides of Photosystem I of the red alga Galdieria sulfuraria. Photosynth Res 68: 121–130PubMedCrossRefGoogle Scholar
  48. Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M and Miyachi S (1996) Chi d as a major pigment. Nature 383: 402CrossRefGoogle Scholar
  49. Miyashita H, Adachi K, Kurano N, Ikemoto H, Chihara M and Miyachi S (1997) Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as the major chlorophyll. Plant Cell Physiol 38: 274–281CrossRefGoogle Scholar
  50. Moreira D, Le Guyader H and Philippe H (2000) The origin of red algae and the evolution of chloroplasts. Nature 405: 69–72PubMedCrossRefGoogle Scholar
  51. Morschel E and Miihlethaler K (1983) On the linkage of exoplasmic freeze-fracture particles to phycobilisomes. Planta 158: 451–457CrossRefGoogle Scholar
  52. Mullineaux CW, Tobin MJ and Jones GR (1998) Mobility of photosynthetic complexes in thylakoid membranes. Nature 390: 421–424CrossRefGoogle Scholar
  53. Mustardy L, Cunningham FX Jr and Gantt E (1992) Photosynthetic membrane topography: Quantitative in situ localization of Photosystem I and II. Proc Natl Acad Sci USA 89: 10021–10025Google Scholar
  54. Necchi O Jr and Zucchi MR (2001) Photosynthetic performance of freshwater Rhodophyta in response to temperature, irradiance, pH and diurnal rhythm. Phycolog Res 49: 305–318CrossRefGoogle Scholar
  55. Passaquet C and Lichtle C (1995) Molecular study of a light-harvesting apoprotein of Giraudyopsis stellifer (Chryoso-phyeceae). Plant Molec. Biol. 29: 135–148Google Scholar
  56. Pursiheimo S, Rintamaki E, Baena-Gonzales E and Aro E-M (1998) Thylakoid protein phosphorylation in evolutionally divergent species with oxygenic photosynthesis. FEBS Lett 423: 178–182PubMedCrossRefGoogle Scholar
  57. Ritter S, Hiller RG, Wrench PM, Welte W, Diederichs K (1999) Crystal structure of a phycourobilin-containing phycoerythrin at 1.90-A resolution. J Struct Biol 126: 86–97PubMedCrossRefGoogle Scholar
  58. Ritz M, Licthle C, Spilar A, Joder A, Thomas J-C and Etienne AL (1998) Characterization of phycocyanin-deficient phycobilisomes from a pigment mutant of Porphyridium sp. ( Rhodophyta ). J Phycol 34: 835–843Google Scholar
  59. Ritz M, Thomas J-C, Spilar A and Etienne A-L (2000) Kinetics of photoacclimation in response to a shift to high light of the red alga Rhodella violacea adapted to low irradiance. Plant Physiol 123: 1415–1425PubMedCrossRefGoogle Scholar
  60. Rogl H and Kuhlbrandt W (1999) Mutant trimers of light-harvesting complex II exhibit altered pigment content and spectroscopic features. Biochemistry 38: 16214–16222.PubMedCrossRefGoogle Scholar
  61. Sandona D, Croce R, Pagano A, Crimi M and Bassi R (1998) Higher plant light harvesting proteins. Structure and function as revealed by mutation analysis of either protein or chromophore moieties. Biochim. Biophys. Acta 1365: 207–214Google Scholar
  62. Sheath RG and Hambrook JA (1990) Freshwater ecology. In: Cole KM and Sheath RG (eds) Biology of the Red Algae, pp 423–453. Cambridge University Press, CambridgeGoogle Scholar
  63. Sidler W A (1994) Phycobilisome and phycobiliprotein structures. In: Bryant DA (ed) The Molecular Biology of the Cyano-bacteria, pp 139–246. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  64. Stransky H and Hager A (1970) Das Carotenoidmuster und die Verbreitung des lichtinduzuierten Xanthophyllcyclus in verschiendened Algenklassen IV. Cyanophyceae und Rhodo-phyceae. Arch Microbiol 72: 84–96Google Scholar
  65. Talarico L and Maranza G (2000) Light adaptive responses in red macroalgae: An overview. J Photochem Photobiol B: Biology 56: 1–11PubMedCrossRefGoogle Scholar
  66. Tan S, Wolfe GR, Cunningham FX Jr and Gantt E (1995) Decrease of polypeptides in the PS I antenna complex with increasing growth irradiance in the red alga Porphyridium cruentum. Photosynth Res 45: 1–10CrossRefGoogle Scholar
  67. Tan S, Cunningham FX, Jr and Gantt E (1997a) LHCaRl of the red alga Porphyridium cruentum encodes a polypeptide of the LHCI complex with seven potential chlorophyll a-binding residues that are conserved in most LHCs. Plant Molec Biol 33: 157–167Google Scholar
  68. Tan S, Ducret A, Aebersold R and Gantt E (1997b) Red algal LHCI genes have similarities with both Chi a/b-and a/c-binding proteins: A 21 kDa polypeptide encoded by LhcaR2 is one of the six LHCI polypeptides. Photosynth Res 53: 129–140CrossRefGoogle Scholar
  69. Thomas J-C and Passaquet C (1999) Characterization of a phycoerythrin without a-subunits from a unicellular red alga. J Biol Chem 274: 2472–2482PubMedCrossRefGoogle Scholar
  70. Wolfe GR, Cunningham FX Jr, Durnford D, Green BR and Gantt E (1994a) Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation. Nature 367: 566–568CrossRefGoogle Scholar
  71. Wolfe GR, Cunningham FX Jr, Grabowski B and Gantt E (1994b) Isolation and characterization of Photosystem I and II from the red alga Porphyridium cruentum. Biochim Biophys Acta 1188: 357–366CrossRefGoogle Scholar
  72. Zhang J-M, Zheng X-G, Zhang J-P, Zhao F-l, Xie J, Wang H-Z, Zhao J-Q, Jiang L-Y (1998) Studies of the energy transfer among allophycocyanin from phycobilisomes of Polysiphonia urceolata by time-resolved fluorescence isotropic and anisotropic spectroscopy. Photochem Photobiol 68: 777–784CrossRefGoogle Scholar
  73. Zucchi MR and Necchi O Jr (2001) Effects of temperature, irradiance and photoperiod on growth and pigment content in some freshwater red algae in culture. Phycolog Res 49: 103–114CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2003

Authors and Affiliations

  • Elisabeth Gantt
    • 1
  • Beatrice Grabowski
    • 1
  • Francis X. CunninghamJr.
    • 1
  1. 1.Department of Cell Biology and Molecular Genetics, Microbiology BuildingUniversity of MarylandCollege ParkUSA

Personalised recommendations