Evolutionary History and Taxonomy of Red Algae

  • Hwan Su Yoon
  • Giuseppe C. Zuccarello
  • Debashish Bhattacharya
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 13)


The red algae (Rhodophyta) form a distinct photosynthetic eukaryotic lineage that consists of around 6,000 species including unicellular to large multicellular taxa (http://www.algaebase.org/). The red algae are unique among eukaryotes in lacking both flagella and centrioles during their entire life cycle (Gabrielson et al., 1990; Graham and Wilcox, 2000). Pit connections, pit plugs, and a triphasic life cycle that are mostly found in the Florideophyceae are also distinguishing characters of the red algae. The photosynthetic organelle (plastid) of red algae is bounded by two membranes and contains chlorophyll-a, phycocyanin, and phycoerythrin as photosynthetic pigments. These pigment complexes, organized in phycobilisomes, are located on the surface of unstacked thylakoid membranes to capture light energy. As a storage product, the red algae produce granulated floridean starch in the cytoplasm that is different from green algal starch. In addition to these unique features, the monophyly of red algae is strongly supported by nuclear, plastid, and mitochondrial gene trees (Freshwater et al., 1994; Ragan et al., 1994; Van de Peer and De Wachter, 1997; Burger et al., 1999; Yoon et al., 2002b, 2004).


  1. Albertano, P., Ciniglia, C., Pinto, G., and Pollio, A. (2000) The taxonomic position of Cyanidium, Cyanidioschyzon and Galdieria: an update. Hydrobiologia 433: 137–143.CrossRefGoogle Scholar
  2. Barghoorn, E.S. and Tyler, S.A. (1965) Microorganisms from the Gunflint Chert. Science 147: 563–577.PubMedCrossRefGoogle Scholar
  3. Bhattacharya, D. and Medlin, L. (1995) The phylogeny of plastids: a review based on comparisons of small-subunit ribosomal RNA coding regions. J. Phycol. 31: 489–498.CrossRefGoogle Scholar
  4. Bhattacharya, D., Yoon, H.S. and Hackett, J.D. (2004) Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays 26: 50–60.PubMedCrossRefGoogle Scholar
  5. Broadwater, S.T. and Scott, J.L. (1994) Ultrastructure of unicellular red algae, In: J. Seckbach (ed.) Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells. Kluwer, The Netherlands, pp. 215–230.Google Scholar
  6. Broom, J.E., Farr, T.J. and Nelson, W.A. (2004) Phylogeny of the Bangia flora of New Zealand suggests a southern origin for Porphyra and Bangia (Bangiales, Rhodophyta). Mol. Phylogenet. Evol. 31: 1197–1207.PubMedCrossRefGoogle Scholar
  7. Burger, G., Saint-Louis, D., Gray, M.W. and Lang, B.F. (1999) Complete sequence of the mitochondrial DNA of the red alga Porphyra purpurea. Cyanobacterial introns and shared ancestry of red and green algae. Plant Cell 11: 1675–1694.Google Scholar
  8. Butterfield, N.J. (2000) Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26: 386–404.CrossRefGoogle Scholar
  9. Butterfield, N.J. (2005) Probable Proterozoic Fungi. Paleobiology 31: 165–182.CrossRefGoogle Scholar
  10. Butterfield, N.J., Knoll, A.H. and Swett, K. (1988) Exceptional preservation of fossils in an Upper Proterozoic shale. Nature 334: 424–427.PubMedCrossRefGoogle Scholar
  11. Cavalier-Smith, T. (1998) A revised six-kingdom system of life. Biol. Rev. 73: 203–266.PubMedCrossRefGoogle Scholar
  12. Ciniglia, C., Yoon, H.S., Pollio, A., Pinto, G. and Bhattacharya, D. (2004) Hidden biodiversity of the extremophilic Cyanidiales red algae. Mol. Ecol. 13: 1827–1838.PubMedCrossRefGoogle Scholar
  13. Delwiche, C.F., Kuhsel, M. and Palmer, J.D. (1995) Phylogenetic analysis of tufA sequences indicates a cyanobacterial origin of all plastids. Mol. Phylogenet. Evol. 4: 110–128.PubMedCrossRefGoogle Scholar
  14. Dixon, P.S. (1973) Biology of the Rhodophyta. Oliver and Boyd, Edinburgh, Scotland.Google Scholar
  15. Douzery, E.J., Snell, E.A., Bapteste, E., Delsuc, F. and Philippe, H. (2004) The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils? Proc. Natl. Acad. Sci. USA 101: 15386–15391.PubMedCrossRefGoogle Scholar
  16. Freshwater, D.W., Fredericq, S., Butler, B.S., Hommersand, M.H. and Chase, M.W. (1994) A gene phylogeny of the red algae (Rhodophyta) based on plastid rbcL. Proc. Natl. Acad. Sci. USA 91: 7281–7285.PubMedCrossRefGoogle Scholar
  17. Gabrielson, P.W., Garbary, D.J. and Scagel, R.F. (1985) The nature of the ancestral red alga: inferences from a cladistic analysis. Biosystems 18: 335–346.PubMedCrossRefGoogle Scholar
  18. Gabrielson, P.W., Garbary, D.J., Sommerfeld, M.R., Townsend, R.A. and Tyler, P.L. (1990) Phylum Rhodophyta, In: L. Margulis, J.O. Corliss, M. Melkonian and D.J. Chapman (eds.) Handbook of Protoctista: The Structure, Cultivation, Habitats and Life Histories of the Eukayotic Microorganisms and Their Descendants Exclusive of Animals, Plants and Fungi. Jones & Bartlett, Boston, MA, pp. 914.Google Scholar
  19. Garbary, D.J. and Gabrielson, P.W. (1990) Taxonomy and evolution, In: K.M. Cole, and R.G. Sheath (eds.) Biology of the Red Algae. Cambridge University Press, New York, pp. 477–498.Google Scholar
  20. Graham, L.D. and Wilcox, L.W. (2000) Algae. Prentice-Hall, Upper Saddle River, NJ.Google Scholar
  21. Gross, W., Heilmann, I., Lenze, D. and Schnarrenberger, C. (2001) Biogeography of the Cyanidiaceae (Rhodophyta) based on 18S ribosomal RNA sequence data. Eur. J. Phycol. 36: 275–280.CrossRefGoogle Scholar
  22. Hackett, J.D., Yoon, H.S., Li, S., Reyes-Prieto, A., Rummele, S.E. and Bhattacharya, D. (2007a) Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of Rhizaria with chromalveolates. Mol. Biol. Evol. 24: 1702–1713.PubMedCrossRefGoogle Scholar
  23. Hackett, J.D., Yoon, H.S., Butterfield, N.J., Sanderson, M.J. and Bhattacharya, D. (2007b) Plastid endosymbiosis: origins and timing of events, In: P. Falkowski, and A. Knoll (eds.) Evolution of Aquatic Photoautotrophs. Academic Press, New York, pp. 109–132.Google Scholar
  24. Harper, J.T. and Saunders, G.W. (2002) A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta). Eur. J. Phycol. 37: 463–476.CrossRefGoogle Scholar
  25. Hawkes, M.W. (1988) Evidence of sexual reproduction in Smithora naiadum (Erythropeltidales, Rhodophyta) and its evolutionary significance. Brit. Phycol. J. 23: 327–336.CrossRefGoogle Scholar
  26. Huang, J. and Gogarten, J.P. (2007) Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol. 8: R99.PubMedCrossRefGoogle Scholar
  27. Huisman, J.M., Sherwood, A.R. and Abbott, I.A. (2003) Morphology, reproduction, and the 18S rRNA gene sequence of Pihiella liagoraciphila gen. et sp. nov. (Rhodophyta), the so-called ‘monosporangial discs’ associated with members of the Liagoraceae (Rhodophyta)and proposal of the Pihiellales ord. nov. J. Phycol. 39: 978–987.CrossRefGoogle Scholar
  28. Javaux, E.J., Knoll, A.H. and Walter, M.R. (2001) Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412: 66–69.PubMedCrossRefGoogle Scholar
  29. Karsten, U., West, J.A., Zuccarello, G.C., Engbrodt, R., Yokoyama, A., Hara, Y. and Brodie, J. (2003) Low molecular weigh carbohydrates of the Bangiophycidae (Rhodophyta). J. Phycol. 39: 584–589.CrossRefGoogle Scholar
  30. Li, S., Nosenko, T., Hackett, J.D. and Bhattacharya, D. (2006) Phylogenomic analysis identifies red algal genes of endosymbiotic origin in the chromalveolates. Mol. Biol. Evol. 23: 663–674.PubMedCrossRefGoogle Scholar
  31. Maggs, C.A. and Pueschel. C.M. (1989) Morphology and development of Ahnfeltia plicata (Rhodophyta): proposal of Ahnfeltiales ord. nov. J. Phycol. 25: 333–351.CrossRefGoogle Scholar
  32. Magne, F. (1960) Le Rhodochaete parvula Thuret (Bangioidée) et sa reproduction sexuée. Cahiers de Biologie Marine 1: 407–420.Google Scholar
  33. Magne, F. (1990) Reproduction sexuée chez Erythrotrichia carnea (Rhodophyceae, Erythropeltidales). Cryptogamie, Algol. 11:157–170.Google Scholar
  34. McFadden, G.I. (1999) Plastids and protein targeting. J. Eukaryot. Microbiol. 46: 339–346.PubMedCrossRefGoogle Scholar
  35. McFadden, G.I. and van Dooren, G.G. (2004) Evolution: red algal genome affirms a common origin of all plastids. Curr. Biol. 14: R514–516.PubMedCrossRefGoogle Scholar
  36. Merola, A., Castaldo, R., Gambardella, P., Musachio, R. and Taddei, R. (1981) Revision of Cyanidium caldarium: three species of acidophilic alage. Giorn. Bot. Ital. 115: 189–195.CrossRefGoogle Scholar
  37. Moreira, D., Le Guyader, H. and Phillippe, H. (2000) The origin of red algae and the evolution of chloroplasts. Nature 405: 69–72.PubMedCrossRefGoogle Scholar
  38. Moustafa, A., Reyes-Prieto, A. and Bhattacharya, D. (2008) Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions. PLoS ONE 3(5): e2205.PubMedCrossRefGoogle Scholar
  39. Müller, K.M., Oliveira, M.C., Sheath, R.G. and Bhattacharya, D. (2001) Ribosomal DNA phylogeny of the Bangiophycidae (Rhodophyta) and the origin of secondary plastids. Am. J. Bot. 88: 1390–1400.PubMedCrossRefGoogle Scholar
  40. Müller, K.M., Cannone, J.J. and Sheath, R.G. (2005) A molecular phylogenetic analysis of the Bangiales (Rhodophyta) and description of a new genus and species, Pseudobangia kaycoleia. Phycologia 44: 146–155.CrossRefGoogle Scholar
  41. Nelson, W.A. (2007) Bangiadulcis gen. nov.: a new genus for freshwater filamentous Bangiales (Rhodophyta). Taxon 56: 883–886.CrossRefGoogle Scholar
  42. Nelson, W.A., Broom J.E. and Farr T.J. (2003) Pyrophyllon and Chlidophyllon (Erythropeltidales, Rhodophyta): two new genera for obligate epiphytic species previously placed in Porphyra, and a discussion of the orders Erythropeltidales and Bangiales. Phycologia 42: 308–315.CrossRefGoogle Scholar
  43. Nelson, W.A., Farr, T.J. and Broom, J.E.S. (2005) Dione and Minerva, two new genera from New Zealand circumscribed for basal taxa in the Bangiales (Rhodophyta). Phycologia 44: 139–145.CrossRefGoogle Scholar
  44. Nosenko, T., Lidie, K.L., Van Dolah, F.M., Lindquist, E., Cheng, J.F. and Bhattacharya, D. (2006) Chimeric plastid proteome in the Florida “red tide” dinoflagellate Karenia brevis. Mol. Biol. Evol. 23: 2026–2038.PubMedCrossRefGoogle Scholar
  45. Nozaki, H., Matsuzaki, M., Takahara, M., Misumi, O., Kuroiwa, H., Hasegawa, M., Shin, I.T., Kohara, Y., Ogasawara, N. and Kuroiwa, T. (2003) The phylogenetic position of red algae revealed by multiple nuclear genes from mitochondria-containing eukaryotes and an alternative hypothesis on the origin of plastids. J. Mol. Evol. 56: 485–497.PubMedCrossRefGoogle Scholar
  46. Oliveira, M.C. and Bhattacharya, D. (2000) Phylogeny of the Bangiophycidae (Rhodophyta) and the secondary endosymbiotic origin of algal plastids. Am. J. Bot. 87: 482–492.PubMedCrossRefGoogle Scholar
  47. Ott, F.D. and Seckbach, J. (1994) New classification for the genus Cyanidium Geitler 1933, In: J. Seckbach (ed.) Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells. Kluwer, London, pp. 145–152.CrossRefGoogle Scholar
  48. Pinto, G., Albertano, P., Ciniglia, C., Cozzolino, S., Pollio, A., Yoon, H.S. and Bhattacharya, D. (2003) Comparative approaches to the taxonomy of the genus Galdieria Merola (Cyanidiales, Rhodophyta). Cryptogamie, Algol. 24: 13–32.Google Scholar
  49. Pinto, G., Ciniglia, C., Cascone, C. and Pollio, A. (2007) Species composition of Cyanidiales assemblages in Pisciarelli (Campi Flegrei, Italy) and description of Galdieria phlegrea sp. nov., In: J. Seckbach (ed.) Algae and Cyanobacteria in Extreme Environments. Springer, The Netherlands, pp. 387–397.CrossRefGoogle Scholar
  50. Porter, S.M. (2006) The Proterozoic fossil record of heterotrophic eukaryotes, In: S. Xiao, and A.J. Kaufman (eds.) Neoproterozoic Geobiology and Paleobiology. Springer, The Netherlands, pp. 1–21.CrossRefGoogle Scholar
  51. Pueschel, C.M. and Cole, K.M. (1982) Rhodophycean pit plugs: an ultrastructural survey with taxonomic implications. Am. J. Bot. 69: 703–720.CrossRefGoogle Scholar
  52. Ragan, M.A., Bird, C.J., Rice, E.L., Gutell, R.R., Murphy, C.A. and Singh, R.K. (1994) A molecular phylogeny of the marine red algae (Rhodophyta) based on the nuclear small-subunit rRNA gene. Proc. Natl. Acad. Sci. USA 91: 7276–7280.PubMedCrossRefGoogle Scholar
  53. Reumann, S., Inoue, K. and Keegstra, K. (2005) Evolution of the general protein import pathway of plastids (review). Mol. Membr. Biol. 22: 73–86.PubMedCrossRefGoogle Scholar
  54. Reyes-Prieto, A. and Bhattacharya, D. (2007) Phylogeny of nuclear-encoded plastid-targeted proteins supports an early divergence of glaucophytes within Plantae. Mol. Biol. Evol.24: 2358–2361.PubMedCrossRefGoogle Scholar
  55. Rintoul, T.L., Sheath, R.G. and Vis, M.L. (1999) Systematics and biogeography of the Compsopogonales (Rhodophyta) with emphasis on the freshwater families in North America. Phycologia 38: 517–527.CrossRefGoogle Scholar
  56. Rodriguez-Ezpeleta, N., Brinkmann, H., Burey, S.C., Roure, B., Burger, G., Loffelhardt, W., Bohnert, H.J., Philippe, H. and Lang, B.F. (2005) Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr. Biol. 15: 1325–1330.PubMedCrossRefGoogle Scholar
  57. Saunders, G.W. and Hommersand, M.H. (2004) Assessing red algal supraordinal diversity and taxonomy in the context of contemporary systematic data. Am. J. Bot. 91: 1494–1507.PubMedCrossRefGoogle Scholar
  58. Saunders, G.W. and Kraft, G.T. (1997) A molecular perspective on red algal evolution: focus on the Florideophycidae, In: D. Bhattacharya (ed.) Origins of Algae and Their Plastids. Springer-Verlag Wein, New York, pp. 115–138.Google Scholar
  59. Saunders, G.W., Chiovitti, A. and Kraft, G.T. (2004) Small-subunit rRNA gene sequences from representatives of selected families of the Gigartinales and Rhodymeniales (Rhodophyta). 3. Recognizing the Gigartinales sensu stricto. Can. J. Bot. 82: 43–74.CrossRefGoogle Scholar
  60. Scott, J.L., Broadwater, S.T., Saunders, B.D., Thomas, J.P. and Gabrielson, P.W. (1992) Ultrastucture of vegetative organization and cell division in the unicellular red alga Dixoniella grisea gen. nov. (Rhodophyta) and a consideration of the genus Rhodella. J. Phycol. 28: 649–660.CrossRefGoogle Scholar
  61. Sentsova, O.Y. (1991) Diversity of acido-theromphilic unicellular algae of the genus Galdieria (Rhodophyta, Cyanidiophyceae). Botanicheskii Zhurnal 76: 69–79.Google Scholar
  62. Stiller, J.W. and Harrell, L. (2005) The largest subunit of RNA polymerase II from the Glaucocystophyta: functional constraint and short-branch exclusion in deep eukaryotic phylogeny. BMC Evol. Biol. 5: 71.PubMedCrossRefGoogle Scholar
  63. Stiller, J.W., Riley, J. and Hall, B.D. (2001) Are red algae plants? A critical evaluation of three key molecular data sets. J. Mol. Evol. 52: 527–539.PubMedGoogle Scholar
  64. Tappan, H. (1976) Possible eukaryotic algae (Bangiophycidae) among early Proterozoic microfossils. Bull. Geol. Soc. Am. 87: 633–639.CrossRefGoogle Scholar
  65. Van de Peer, Y. and De Wachter, R. (1997) Evolutionary relationships among the eukaryotic crown taxa taking into account site-to-site rate variation in 18S rRNA. J. Mol. Evol. 45: 619–630.PubMedCrossRefGoogle Scholar
  66. Weber, A.P., Linka, M. and Bhattacharya, D. (2006) Single, ancient origin of a plastid metabolite translocator family in Plantae from an endomembrane-derived ancestor. Eukaryot. Cell 5: 609–612.PubMedCrossRefGoogle Scholar
  67. West, J.A., Zuccarello, G.C., Scott, J., Pickett-Heaps, J. and Kim, G.-H. (2005) Observations on Purpureofilum apyrenoidigerum gen. et sp. nov. from Australia and Bangiopsis subsimplex from India (Stylonematales, Bangiophyceae, Rhodophyta). Phycol. Res. 53: 49–66.CrossRefGoogle Scholar
  68. West, J.A., Zuccarello, G.C., Scott, J.L., West, K.A. and Karsten, U. (2007) Rhodaphanes brevistipitata gen. et sp. nov., a new member of the Stylonematophyceae (Rhodophyta). Phycologia 46: 440–449.CrossRefGoogle Scholar
  69. Xiao, S., Zhang, Y. and Knoll, A.H. (1998) Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature 391: 553–558.CrossRefGoogle Scholar
  70. Xiao, S., Knoll, A.H., Yuan, X. and Pueschel, C.M. (2004) Phosphatized multicellular algae in the Neoproterozoic Doushantuo Formation, China, and the early evolution of florideophyte red algae. Am. J. Bot. 91: 214–227.PubMedCrossRefGoogle Scholar
  71. Yoon, H.S., Hackett, J.D. and Bhattacharya, D. (2002a) A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc. Natl. Acad. Sci. USA 99: 11724–11729.PubMedCrossRefGoogle Scholar
  72. Yoon, H.S., Hackett, J.D., Pinto, G. and Bhattacharya, D. (2002b) The single, ancient origin of chromist plastids. Proc. Natl. Acad. Sci. USA 99: 15507–15512.PubMedCrossRefGoogle Scholar
  73. Yoon, H.S., Hackett, J.D., Ciniglia, C., Pinto, G. and Bhattacharya, D. (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 21: 809–818.PubMedCrossRefGoogle Scholar
  74. Yoon, H.S., Hackett, J.D., Van Dolah, F.M., Nosenko, T., Lidie, K.L. and Bhattacharya, D. (2005) Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Mol. Biol. Evol. 22: 1299–1308.PubMedCrossRefGoogle Scholar
  75. Yoon, H.S., Müller, K.M., Sheath, R.G., Ott, F.D. and Bhattacharya, D. (2006) Defining the major lineages of red algae (Rhodophyta). J. Phycol. 42: 482–492.CrossRefGoogle Scholar
  76. Zuccarello, G., West, J., Bitans, A. and Kraft, G. (2000) Molecular phylogeny of Rhodochaete parvula (Bangiophycidae, Rhodophyta). Phycologia 39: 75–81.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Hwan Su Yoon
    • 1
  • Giuseppe C. Zuccarello
    • 2
  • Debashish Bhattacharya
    • 3
  1. 1.Bigelow Laboratory for Ocean SciencesWest Boothbay HarborUSA
  2. 2.School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand
  3. 3.Department of Ecology, Evolution and Natural ResourcesRutgers UniversityNewarkUSA

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