Skip to main content
Log in

The first eukaryotic cells — Acid hot-spring algae

Evolutionary paths from prokaryotes to unicellular red algae via Cyanidium caldarium (PreRhodophyta) succession

  • Section 10. Origin And Structure Of The Cell: Biological Aspects
  • Published:
Journal of Biological Physics Aims and scope Submit manuscript

Abstract

The Cyanidiophyceae members (PreRhodophyta) may serve as a transitional algal group bridging the cyanobacteria and the unicellular Rhodophyta. This thermoacidic algal group is composed of three genera containing several species. We suggested placing these algae in progressively evolutionary steps: (Cyanidioschyzon → Cyanidium → Galdieria). This evolutional ladder is based upon various areas of research like biochemistry, amount of nuclear genome and shape of chloroplast nucleoid, ultrastructure and ecological aspects. The first alga —Cyanidioschyzon — is the cornerstone of this succession; it shows mixed features between cyanobacterium and archaebacteria(Thermoplasma-like cell). It demonstrates simple eukaryotic cellular features and has the smallest amount of nuclear and chloroplast DNA. The intermediate alga in this line,Cyanidium, is also a simple cell, but shows more progressive characterizations than theCyanidioschyzon. The third taxon,Galdieria, is already very close to the unicellular rhodophytes (red algae) and indicates typical advanced eukaryotic characterization. We propose thatCyanidioschyzon (considered to be the simplest eukaryote) may have evolved from an association betweenThermoplasma-like archaebacterium and a thermophilic cyanobacterium. Autogenous (non-symbiotic) compartmental steps may have taken place fromCyanidioschyzon toCyanidium and then toGaldieria, and from this alga (group) towards the other unicellular red algae.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allsopp, A. (1969) Phylogenetic relationships of the procaryota and the origin of the eucaryotic cell.New Phytol. 68, 591–612.

    Google Scholar 

  • Avers, C.J. (1989)Process & Pattern in Evolution, Oxford U. Press, UK.

    Google Scholar 

  • Birky, C.W. (1982) Endosymbiosis vs. Autogeny.Science 215, 495–497.

    Google Scholar 

  • Broda, E. (1975)The Evolution of the Bioenergetic Processes. Pergamon Press, UK. (see pp 116–133.)

    Google Scholar 

  • Chapman, D.J. (1992) Origin and divergence of protists, in J.E. Schopf and C. Klein (eds.),The Proterozoic Biosphere: a Multidisciplinary study, Cambridge University Press, Cambridge, NY. pp. 477–483.

    Google Scholar 

  • Chela-Flores, J. (1995) Some physical problems in Biology: Aspects of the origin and structure of the first cell, in J. Chela-Flores and C. Ponnamperuma (eds.)Proceedings of the conference on the structure and model of the first cell, Kluwer Academic Publishers, Dordrecht, in-press.

    Google Scholar 

  • Cohen, S.S. (1970) Are/were mitochondria and chloroplasts microorganisms?,Amer. Sci. 58, 281–289.

    Google Scholar 

  • Copeland, J.J. (1936) Yellowstone thermal myxophyceae,Ann. N.Y.Ac.Sc. 36, 1–232.

    Google Scholar 

  • Day, W. (1979)Genesis on Planet Earth, The House of Talos Publishers, Michigan, USA.

    Google Scholar 

  • De Luca, P., Taddei, R. and Varano, L. (1978)‘Cyanidioschyzon’: a new alga of thermal acidic environments,Webbia 33, 37–44.

    Google Scholar 

  • Ebringer, L. and Krajcovic, J. (1994)Cell Origin and Evolution, Veda Publishing House, Bratislava, Czechoslovak Society for Microbiology.

  • Fredrick, J.F. (1993) Biosynthesis of branched glucans and the origin of protist, in S. Sato, M. Ishida and H. Ishikawa (eds.),Endocytobiology V, Tübingen University Press, pp. 475–479.

  • Fredrick, J.F. and Seckbach, J. (1983) Intraspecies evolution of enzymic mechanisms associated with the synthesis of α-1,4 storage glucans in two thermophilic-acidophilic algae ofCyanidium type,Phytochem. 22(5), 1155–1157.

    Google Scholar 

  • Fredrick, J.F. and Seckbach, J. (1986) Storage glucan and glucosyltransferase isozymes ofCyanidioschyzon merolae: A primitive eukaryote,Phytochem. 25(2), 363–365.

    Google Scholar 

  • Fukuda, I., Nagashima, H. and Seckbach, J. (1990) DNA content and the evolution of information in the nucleus and nucleoids of the lowest eukaryote, in P. Nardon, V. Gianinazzi-Pearson, A.M. Grenier, L. Margulis and D.C. Smith (eds.),Endocytobiology IV, INSA, Paris, pp. 585–588.

    Google Scholar 

  • Gray, M.W. (1991) Origin and evolution of plastid genomes and genes, in L. Bogorad and I.K. Vasil (eds.),Molecular Biology of Plastids, Academic Press, Inc. San Diego, pp. 303–330.

    Google Scholar 

  • Han, T.-M. and Runnegar, B. (1992) Megascopic eukaryotic algae from the 2.1-billion-year-old Negaunee iron-formation, Michigan,Science 257, 232–235.

    Google Scholar 

  • Hashimoto, T., Adachi, J. and Hasegawa, M. (1992) Phylogenetic place ofGiardia lamblia a protozoan that lacks mitochondria,Endocytobiology & Cell Res. 9, 59–69.

    Google Scholar 

  • Hixon, W.G. and Searcy, D.G. (1993) Cytoskeleton in the archaebacteriumThermoplasma acidophilum? Viscosity increase in soluble extracts,Biosystems 29(2–3, 151–160.

    Google Scholar 

  • Hoffman, L. (1994)Cyanidium-like algae from caves, in J. Seckbach (ed.),Evolutionary Pathways and Enigmantic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells, Kluwer Academic Publishers, Dordrecht, pp. 175–182.

    Google Scholar 

  • Hoffmann, L. and Mayele, B. (1993) Ultrastructure of the plasmalemma of the caveCyanidium (Rhodophyta),Phycologia 32(4, 307–309.

    Google Scholar 

  • Hori, H. and Osawa, S. (1987) Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences,Mol. Biol. Evol. 4(5), 445–472.

    Google Scholar 

  • Hori, H., Satow, Y., Inoue, I. and Chihara, M. (1990) Origins of organelles and algae evolution deduced from 5S ribosomal RNA sequences, in P. Nardon, V. Gianinazzi-Pearson, A.M. Grenier, L. Margulis and D.C. Smith (eds.),Endocytobiology IV, INSA, Paris, pp. 557–559.

    Google Scholar 

  • Jensen, T.E. (1989) Thylakoids in aged cyanobacterial cells suggest origin of eukaryotic nuclear membranes,Cytobios 60, 47–61.

    Google Scholar 

  • Jensen, T.E. (1991) Autogenous bacterial origin of the eukaryotic cellEndocytobios & Cell Res. 8, 1–16.

    Google Scholar 

  • Jensen, T.E. (1994) Alternative pathway (cyanobacteria to Eukaryota), in J. Seckbach (ed.),Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells, Kluwer Academic Publishers, Dordrecht, pp. 53–66.

    Google Scholar 

  • Keyhani, E. (1983) The locked cell hypothesis. Origin of intracellular organelles, in H.E.A. Schenk and W. Schwemmler (eds.),Endocytobiology II, W. deGruyter & Co. Berlin. New York, pp. 129–145.

    Google Scholar 

  • Klein, R.M. and cronquist, A. (1967) A consideration of the evolutionary and taxonomic significance of some biochemical, micromorphological, and physiological characters in the Thallophytes,The Quart. Rev. of Biology. 42(2, 105–296.

    Google Scholar 

  • Kostrzewa, M., Valentin, K., Maid, U., Radetzky, R. and Zetsche, K. (1990), Structure of the Rubisco operon from the multicellular red algaAntithamnion spec.Curr. Genet. 18, 465–469.

    Google Scholar 

  • Kuroiwa, T. (1989) The nuclei of cellular organelles and the formation of daughter organelles by “plastid — dividing ring”,Bot. Mag. Tokyo 102, 291–329.

    Google Scholar 

  • Kuroiwa T., Nagashima, H. and Fukuda, I. (1989) Chloroplast division without DNA synthesis during the life cycle of unicellular algaCyanidium caldarium M-8 revealed by quantitative fluorescence microscope,Protoplasma 149, 120–129.

    Google Scholar 

  • Kuroiwa, T., Suzuki, K. and Kuroiwa, H. (1993) Mitochondrial division by an electron-dense ring inCyanidioschyzon merolae, Protoplasma 175, 173–177.

    Google Scholar 

  • Kuroiwa, T., Kawazu, T., Takahashi, H., Suzuki, K., Ohta, N. and Kuroiwa H. (1994a) Comparison of ultrastructures between the ultra-small eukaryoteCyanidioschyzon merolae andCyanidium caldarium, Cytologia 59, 149–158.

    Google Scholar 

  • Kuroiwa, T., Kuroiwa, H., Mita, T. and Ohta, N. (1994b)Cyanidium caldarium as a model for studying division of chloroplasts, in J. Seckbach (ed.),Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells, Kluwer Academic Publishers, Dordrecht, pp. 239–253.

    Google Scholar 

  • Lafrai, M.A. and Betz, A. (1985) Anaerobic fermentation inCyanidium caldarium, Planta 163, 38–42.

    Google Scholar 

  • Loiseaux-de Goër, L. S. (1994) Plastid lineages, in D.J. Chapman and F. Round (eds.),Recent Progress in Phycological Research (in press).

  • Lüttke, A. (1991) On the origin of chloroplasts and rhodoplast: protein sequence composition,Endocytobiosis & Cell Res. 8, 75–82.

    Google Scholar 

  • Maleszka, R. (1993) Electrophoretic analysis of the nuclear and organellar genomes in the ultra-small algaCyanidioschyzon merolae, Curr. Genet. 24(6, 548–450.

    Google Scholar 

  • Margulis, L. (1981)Symbiosis in Cell Evolution (Life and its environment on the early Earth). W.h. Freeman Company, San Francisco.

    Google Scholar 

  • Merola, A., Castaldo, R., De Luca, P., Gambardella, R., Musacchio, A. and Taddei, R. (1981) Revision ofCyanidium caldarium. Three species of acidophilic algae,Giorn. Bot. Ital. 115(4–5), 189–195.

    Google Scholar 

  • Nagashima, H., Kikuko, U., Fukuda, I. and Seckbach, J. (1993) Several new strains of thermal algaCyanidioschyzon as the most primitive eukaryotes, in S. Sato, M. Ishida and H. Ishikawa (eds.), Endocytobiology V, Tübingen University Press, pp. 279–285.

  • Nakamura, H. (1993) Metabolic and membranous differentiation leading non-symbiotic origin of eukaryotic cell, in S. Sato, M. Ishida and H. Ishikawa (eds.),Endocytobiology V, Tübingen University Press, pp. 335–342.

  • Nakamura, H. (1994) Origin of eukaryota from cyanobacterium: Membrane evolution theory, in J. Seckbach (ed.),Evolutionary Pathways and Engimatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells, Kluwer Academic Publishers, Dordrecht, pp. 3–18.

    Google Scholar 

  • Nakamura, H. and Hase, A. (1990–1991) Cellular differentation in the process of generation of the eukaryotic cell.Origin of Life 20, 499–514.

    Google Scholar 

  • Ohta, N., Nagashima, H. and Kuroiwa, T. (1992) Isolation of the chloroplast DNA and the sequence of trnK gene ofCyanidium caldarium strain RK-1,Plant & Cell Physiol. 33(5, 657–661.

    Google Scholar 

  • Ohta, N., Suzuki, K., Kawano, S. and Kuroiwa, T. (1993) Direct evidence of mitochondrial nuclear division in the ultra-micro algaCyanidioschyzon merolae, Cytologia 58, 471–476.

    Google Scholar 

  • Ott, F.D and Seckbach, J. (1994a) A review on the taxonomic position of the algal genusCyanidium Geitler 1933 and its ecological cohortsGaldieria Merola in Merola et al. 1981 andCyanidioschyzon DeLuca, Taddei and Varano 1978, in J. Seckbach (ed.),Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells, Kluwer Academic Publishers, Dordrecht, pp. 113 - 132.

    Google Scholar 

  • Ott, F.D and Seckbach, J. (1994b) New classification for the genusCyanidium Geitler 1933, in J. Seckbach (ed.),Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells, Kluwer Academic Publishers, Dordrecht, pp. 145 -152.

    Google Scholar 

  • Raff, R.A. and Mahler, H.R. (1972) The non symbiotic origin of mitochondria,Science 177, 575–582.

    Google Scholar 

  • Raff, R.A. and Mahler, H.R. (1975) The symbiont that never was: An inquiry into the evolutionary origin of the mitochondrion.Symp. Soc. Exp. Biol. 29, 41–92.

    Google Scholar 

  • Riding, R. (1992) The algal breath of life,Nature 359, 13–14.

    Google Scholar 

  • Richter, O.M. and Schafer, G. (1992) Purification and enzymic characterization of the cytoplasmic pyrophosphatase from the thermoacidophilic archaebacteriumThermoplasma acidophilum, Eur. J. Biochem. 209(1, 343–349.

    Google Scholar 

  • Schenk, H.E.A. (1993) Some thoughts towards a discussion of terms and definitions in endocytobiology, in S. Sato, M. Ishida and H. Ishikawa (eds.),Endocytobiology V, Tübingen University Press, pp. 547–556.

  • Schenk, H.E.A. (1994) Glaucocystophyta model for symbiogeneous evolution of new eukaryotic species, in J. Seckbach (ed.),Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells, Kluwer Academic Publishers, Dordrecht, pp. 19–52.

    Google Scholar 

  • Schopf, W.J. (1992) in J.W. Schopf (ed.),Major events in the history of life, Jones and Bartlett Publishers International, Boston and London.

    Google Scholar 

  • Searcy, D.G., Stein, D.B. and Green, G.R. (1978) Phylogenetic affinities between eukaryotic cells and a thermophilic mycoplasma,BioSystems 10, 19–28.

    Google Scholar 

  • Seckbach, J. (1987) Evolution of eukaryotic cells via bridge algae: The Cyanidia connection (Endocytobiology III),Ann. N.Y.Ac.Sc. 503, 424–437.

    Google Scholar 

  • Seckbach, J. (1991) Systematic problems withCyanidium caldarium andGaldieria sulphuraria and their implications for molecular biology studies.J. Phycol. 27, 794–796.

    Google Scholar 

  • Seckbach, J. (1992) The Cyanidiophyceae and the “anomalous symbiosis” ofCyanidium caldarium, in W. Reisser (ed.),Algae and Symbioses: Plants, Animals, Fungi, Viruses, Interactions Explored, Biopress Lmt. Bristol, England, pp. 399–426.

    Google Scholar 

  • Seckbach, J. (1994) The natural history ofCyanidium (Geitler 1933): Past and present perspectives, in J. Seckbach (ed.),Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells, Kluwer Academic Publishers, Dordrecht, pp. 99 - 112.

    Google Scholar 

  • Seckbach, J., Baker F.A. and Shugarman P.M. (1970) Algae thrive under pure CO2.Nature 227, 744–745.

    Google Scholar 

  • Seckbach, J., Hammerman, I.S. and Hanania, J. (1981) Ultrastructural studies ofCyanidium caldarium: Contribution to phylogenesis.Ann. N.Y.Ac.Sc. 361, 409–425.

    Google Scholar 

  • Seckbach, J., Fredrick J.F. and Garbary D.J. (1983) Auto-or exogeneous origin of transitional algae: An appraisal, in H.E.A. Schenk and W. Schwemmler (eds.),Endocytobiology II, W. deGruyter & Co. Berlin. New York. pp. 947–962.

    Google Scholar 

  • Seckbach, J., González, E., Wainwright, I.M. and Gross, W. (1992) Peroxisomal function in the Cyanidiophyceae (Rhodophyta): a discussion of phylogenetic relationships and the evolution of microbodies (peroxisomes).Nova Hedwigia 55(1–2), 99–109.

    Google Scholar 

  • Seckbach, J., Ikan, R. Nagashima, H. and Fukuda, I. (1993a) New phylogentic status for acid hot spring algae, in S. Sato, M. Ishida and H. Ishikawa (eds.),Endocytobiology V, Tübingen University Press, pp. 241–254.

  • Seckbach, J., Ikan, R. Ringelberg, D. and White, D. (1993b) Sterols and phylogeny of the acidophilic hot springs algaeCyanidium caldarium andGaldieria sulphuraria, Phytochem. 34(5), 1345–1349.

    Google Scholar 

  • Seckbach, J. and Ott, F.D. (1994) Systematic position and phylogenetic status ofCyanidium Geitler 1933, in J. Seckbach (ed.),Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells, Kluwer Academic Publishers, Dordrecht, pp. 133 -143.

    Google Scholar 

  • Sogin, M.L. (1991) Early evolution and the origin of eukaryotes,Current Opinion in Genetics and Development 1, 457–463.

    Google Scholar 

  • Sogin, M.L., Gunderson, J.H., Elwood, H.J., Alonso, R.A. and Peattie, D.A. (1989) Phylogenetic meanings of the kingdom concept: an unusual eukaryotic ribosomal RNA fromGiardia lamblia.Science 243, 75–77.

    Google Scholar 

  • Stanier, R.Y. (1970) Some aspects of the biology of cells and their possible evolutionary significance, in C.H.P Knight and B.D. Knight (eds.),Symposia of the Society for General Microbiology. XX,Prokaryotic and Eukaryotic Cells, Cambridge University Press, Cambridge, England. pp 1–38 + 3 Plates.

    Google Scholar 

  • Suzuki, K., Ohta, N. and Kuroiwa, T, (1992) Isolation of cell-nuclear, mitochondrial and chloroplast DNA from ultra-small eukaryoteCyanidioschyzon merolae, Protoplasma 171, 80–84.

    Google Scholar 

  • Suzuki, K., Kawano, K. and Kuroiwa, T. (1994a) Single mitochondrion in hot-spring algae: Behavior of mitochondria inCyanidium caldarium andGaldieria sulphuraria (Rhodophyta, Cyanidiophyceae),Phycologia 33(4, 298–300.

    Google Scholar 

  • Suzuki, T. Ehara, T., Osafune, T., Kuroiwa, H., Kawano, S. and Kuroiwa, T. (1994b) Behavior of mitochondria, chloroplasts and their nuclei during the mitotic cycle in the ultramicroalgaCyanidioschyzon merolae, Europ. J. of Cell Biol. 63, 280–288.

    Google Scholar 

  • Takahashi, H., Suzuki, K., Ohta, N., Suzuki, T., Takano, H., Kawano, S. and Kuroiwa, T. (1993) An electrophoretic karyotype ofCyanidioschyzon merolae.Cytologia 58, 477–482.

    Google Scholar 

  • Taylor, F.J.R. (1976) Autogeneous theories for the origin of eukaryotes.Taxon 25, 377–390.

    Google Scholar 

  • Taylor, F.J.R. (1987) An overview of the status of evolutionary cell symbiosis theories, (Endocytobioloy III)Ann. N.Y.Ac.Sci. 503, 1–16.

    Google Scholar 

  • Valentin, K., Maid, U., Emich, A. and Zetsche, K. (1992) Organization and expression of a phycobiliprotein gene cluster from the unicellular red algaCyanidium caldarium.Plant Mol. Biol. 20, 267–276.

    Google Scholar 

  • Van den Eynde, H., De Baere, R. and De Wachter, R. (1988a) Sequence and secondary structure ofPorphyra umbilicalis 5S rRNA. Relevance for the evolutionary origin of red algae,Nucleic Acids Res. 16, 10919.

    Google Scholar 

  • Van den Eynde, H., De Baere, R., De Roeck, E., Van de Peer, Y., Vandenberghe, A., Willekens, P. and De Wachter, R. (1988b) The 5S ribosomal RNA sequences of a red algal rhodoplast and a gymnosperm chloroplast. Implications for the evolution of plastids and cyanobacteria,J. Mol. Evol. 27, 126–132.

    Google Scholar 

  • Uzzell, T. and Spolsky, C. (1974) Mitochondria and plastids as endosymbionts: A revival of special creation?. Amer. Sci.62(3), 334–343.

    Google Scholar 

  • Zenvirt, D., Volokita, M. and Kaplan, A. (1985) Photosynthesis and inorganic carbon accumulation in the acidophilic algaCyanidioschyzon merolae, Plant Physiology 77, 237–239.

    Google Scholar 

  • Zetsche, K. (1994) Molecular organization and expression of the plastid genome ofGaldieria sulphuraria (=Cyanidium caldarium) and other unicellular red, in J. Seckbach (ed.),Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells, Kluwer Academic Publishers, Dordrecht, pp. 255–262.

    Google Scholar 

  • Zetsche, K. and Valentin, K. (1994) Structure, coding capacity and gene sequences of the plastid genome from red algae,Endocytobiosis and Cell Res. 10, 107–127.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Dedicated toDr. Jerome F. Fredrick, an enthusiast of our favorite algaCyanidium, on his retirement from directorship of Dodge Chemical Laboratories in Bronx, NYC.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Seckbach, J. The first eukaryotic cells — Acid hot-spring algae. J Biol Phys 20, 335–345 (1995). https://doi.org/10.1007/BF00700452

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00700452

Keywords

Navigation