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Evolutionary History and Taxonomy of Red Algae

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Red Algae in the Genomic Age

Abstract

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).

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References

  • Albertano, P., Ciniglia, C., Pinto, G., and Pollio, A. (2000) The taxonomic position of Cyanidium, Cyanidioschyzon and Galdieria: an update. Hydrobiologia 433: 137–143.

    Article  Google Scholar 

  • Barghoorn, E.S. and Tyler, S.A. (1965) Microorganisms from the Gunflint Chert. Science 147: 563–577.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Bhattacharya, D., Yoon, H.S. and Hackett, J.D. (2004) Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays 26: 50–60.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Butterfield, N.J. (2005) Probable Proterozoic Fungi. Paleobiology 31: 165–182.

    Article  Google Scholar 

  • Butterfield, N.J., Knoll, A.H. and Swett, K. (1988) Exceptional preservation of fossils in an Upper Proterozoic shale. Nature 334: 424–427.

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith, T. (1998) A revised six-kingdom system of life. Biol. Rev. 73: 203–266.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Dixon, P.S. (1973) Biology of the Rhodophyta. Oliver and Boyd, Edinburgh, Scotland.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • Graham, L.D. and Wilcox, L.W. (2000) Algae. Prentice-Hall, Upper Saddle River, NJ.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • Hawkes, M.W. (1988) Evidence of sexual reproduction in Smithora naiadum (Erythropeltidales, Rhodophyta) and its evolutionary significance. Brit. Phycol. J. 23: 327–336.

    Article  Google Scholar 

  • Huang, J. and Gogarten, J.P. (2007) Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol. 8: R99.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Javaux, E.J., Knoll, A.H. and Walter, M.R. (2001) Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412: 66–69.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Magne, F. (1960) Le Rhodochaete parvula Thuret (Bangioidée) et sa reproduction sexuée. Cahiers de Biologie Marine 1: 407–420.

    Google Scholar 

  • Magne, F. (1990) Reproduction sexuée chez Erythrotrichia carnea (Rhodophyceae, Erythropeltidales). Cryptogamie, Algol. 11:157–170.

    Google Scholar 

  • McFadden, G.I. (1999) Plastids and protein targeting. J. Eukaryot. Microbiol. 46: 339–346.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Moreira, D., Le Guyader, H. and Phillippe, H. (2000) The origin of red algae and the evolution of chloroplasts. Nature 405: 69–72.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Nelson, W.A. (2007) Bangiadulcis gen. nov.: a new genus for freshwater filamentous Bangiales (Rhodophyta). Taxon 56: 883–886.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Pueschel, C.M. and Cole, K.M. (1982) Rhodophycean pit plugs: an ultrastructural survey with taxonomic implications. Am. J. Bot. 69: 703–720.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Reumann, S., Inoue, K. and Keegstra, K. (2005) Evolution of the general protein import pathway of plastids (review). Mol. Membr. Biol. 22: 73–86.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Sentsova, O.Y. (1991) Diversity of acido-theromphilic unicellular algae of the genus Galdieria (Rhodophyta, Cyanidiophyceae). Botanicheskii Zhurnal 76: 69–79.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Tappan, H. (1976) Possible eukaryotic algae (Bangiophycidae) among early Proterozoic microfossils. Bull. Geol. Soc. Am. 87: 633–639.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Zuccarello, G., West, J., Bitans, A. and Kraft, G. (2000) Molecular phylogeny of Rhodochaete parvula (Bangiophycidae, Rhodophyta). Phycologia 39: 75–81.

    Article  Google Scholar 

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Acknowledgments

The authors thank Dr. N. J. Butterfield for kindly providing the Bangiomorpha fossil images. This project was partially supported from the National Science Foundation Assembling the Tree of Life program to HSY and DB (DEB-0937975).

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Yoon, H.S., Zuccarello, G.C., Bhattacharya, D. (2010). Evolutionary History and Taxonomy of Red Algae. In: Seckbach, J., Chapman, D. (eds) Red Algae in the Genomic Age. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 13. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3795-4_2

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