, Volume 51, Issue 1, pp 13–25 | Cite as

Symbiosis drove cellular evolution

Symbiosis fueled evolution of lineages of Foraminifera (eukaryotic cells) into exceptionally complex giant protists
  • John J. Lee
  • Megan H. Cervasco
  • Jorge Morales
  • Morgan Billik
  • Maoz Fine
  • Oren Levy


Anthropocentric cultural bias led to conceptualizations of evolution as a tree with branches leading to a crown of vertebrates and higher plants. Gradually refined over the years it became part of common scientific culture to think of eukaryotic evolution as process by which cells, limited by surface to volume ratios and other factors, became specialized, leading to multi-cellularity and eventually to the crowned tree. Knowledge of other pathways of cellular evolution is available, but not broadly recognized. Molecular systematics, genetic analyses and ultrastructural comparisons have changed our outlook on evolution and the diversity of life. The discovery of a huge (average size 2.1 cm) unicellular, new, exceptionally complex, dinoflagellate-hosting soritid foraminiferan from the Heron-Wistori Channel, (GBR Australia) gave impetus to re-explore some old ideas on cellular evolution and place them in a contemporary context. In particular, it caused change in perspective of the evolution of the collective group known as larger foraminifera (LF). They exemplify the power by which symbiosis drove the evolution of a predisposed and malleable group of organisms. The factors that underlay foraminiferan predisposition to symbioses with algae are discussed. Each of the evolutionary lines of LF has developed, in its own way, amazing structural adaptations making them extremely complex giant cells.


Cellular evolution Endosymbiotic algae Larger foraminifera 


  1. Adl SM, Simpson AGB, Farmer M, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendosa L, Moestrup Ø, Mozley-Standridge S, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MFJR (2005) The newer higher level classification of Eukaryotes with emphasis on the taxonomy of protists. J Eukarot Microbiol 52:399–451CrossRefGoogle Scholar
  2. Anderson OR, Be AWH (1976) The ultrastructure of a planktonic foraminifer, Globigerinoides sacculifer (Brady), and its symbiotic dinoflagellates. J Foramin Res 6:1–21CrossRefGoogle Scholar
  3. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Syst 34:661–689CrossRefGoogle Scholar
  4. Carpenter WB (1862) Introduction to the study of Foraminifera. Hardwicke, London, pp 1–319Google Scholar
  5. Chai J, Lee JJ (1999a) Initial recognition of endosymbioticdiatoms by the larger foraminifer Amphistegina lobifera. Symbiosis 26:39–53Google Scholar
  6. Chai J, Lee JJ (1999b) Establishment and maintenance ofendosymbiotic diatoms by the larger foraminifer Amphisteginalobifera. In: Wagner E, Norman J, Greppin H, Hackstein JHP, Herrmann RG, Kowalik KV, Schenk HEA, Seckbach J (eds) Endocytobiology VII. Universities of Freiburg and Geneva, pp 137–152Google Scholar
  7. Chai J, Lee JJ (2000) Recognition, establishment and maintenance of diatom endosymbioses in foraminifera. In: Lee JJ, Muller PH (eds) Advances in the biology of foraminifera. Micropaleontology 46 (supplement 1):182–195Google Scholar
  8. Chang SS, Trench RK (1982) Peridinin-Chlorophyll a proteins from the symbiotic dinoflagellate Symbiodinium (=Gymnodinium) microadriaticum Freudenthal. Proc R Soc Lond B 215:191–210CrossRefGoogle Scholar
  9. Corliss J (1989a) The protozoan and the cell: a brief twentieth century overview. J Hist Biol 22:307–323CrossRefPubMedGoogle Scholar
  10. Corliss J (1989b) Protistan diversity and origins of multicellular/multitissued organisms. Bollitine Zoologie 56:227–234Google Scholar
  11. Correia MJ, Lee JJ (2000) Chloroplast retention by Elphidium excavatum (Terquem). Is it a selective process? Symbiosis 29:343–355Google Scholar
  12. Correia MJ, Lee JJ (2002a) Fine structure of the plastids retained by the foraminifer Elphidium excavatum (Terquem). Symbiosis 32:15–26Google Scholar
  13. Correia MJ, Lee JJ (2002b) How long do the plastids retained by Elphidium excavatum (Terquem) last in their host? Symbiosis 32:27–38Google Scholar
  14. Doyle WL, Doyle MM (1940) The structure of zooxanthellae. Papers from Tortugas Laboratory 32:129–142Google Scholar
  15. Faber WW, Lee JJ (1991) Histochemical evidence for digestion in Heterostegina depressa and Operculina ammonoides (Foraminifera). Endocytobiology and Cell Research 8:53–59Google Scholar
  16. Faber WW, Anderson OR, Lindsey JL, Carron DA (1988) Algal-foraminiferal symbiosis in the planktonic foraminifer Globigerinella aequilateralis: I. Occurence and stability of two mutually exclusive chrysophyte endosymbionts and their ultrastructure. J Foraminiferal Res 18:334–343CrossRefGoogle Scholar
  17. Faber WW, Anderson OR, Carron DA (1989) Algal foraminiferal symbiosis in the planktonic foraminifer Globigerinella aequilateralis: II. Effects of two symbiont species on foraminiferal growth and longevity. J Foraminiferal Res 19:185–193CrossRefGoogle Scholar
  18. Garcia-Cuetos L, Pochon X, Pawlowski J (2005) Molecular evidence for host-symbiont specificity in soritid foraminifera. Protistology 156:399–412CrossRefGoogle Scholar
  19. Gastrich MD (1988) Ultrastructure of a new intracellular symbiotic alga found within planktonic foraminifera. J Phycol 23:623–632CrossRefGoogle Scholar
  20. Grell KG (1973) Protozoology. Springer-Verlag, Berlin, p 554Google Scholar
  21. Haeckel E (1886) Generelle morphologie der organismen. Vol. 1, 574 pp, Vol. 2, 462 pp. Reimer, G. BerlinGoogle Scholar
  22. Hallock P (1985) Why are larger foraminifera large? Paleobiology 11:195–208Google Scholar
  23. Hallock P, Forward LB, Hansen HJ (1986) Environmental influence of test shape in Amphistegina. J Foramin Res 16:224–231CrossRefGoogle Scholar
  24. Hawkins EK, Lee JJ (1990) Fine structure of the cell surface of a cultured endosymbiotic strain of Porphyridium sp. (Rhodophyta). Trans Am Microsc Soc 109:352–360CrossRefGoogle Scholar
  25. Hawkins EK, Lee JJ (2001) Architecture of the Golgi apparatus of a scale forming alga: biogenesis and transport of scales. Protoplasma 216:387–395CrossRefGoogle Scholar
  26. Hawkins EK, Lee JJ, Correia M (2003) Polar localization of filamentous actin in cells of the scale-forming alga Pleurochrysis sp. Protoplasma 220:233–236CrossRefPubMedGoogle Scholar
  27. Hofker J (1927) The foraminifera of the Siboga Expedition; Part 1. Monographs Siboga Expedition 1899-1900 (Leiden) 4:1–78Google Scholar
  28. Hohenegger J (1999) Larger foraminifera-microscopical greenhouses indicating shallow-water tropical and subtropical environments in the present and past. Ocasional papers Kagoshima Univ. Research Center for the Pacific Islands 32:19–45Google Scholar
  29. Hottinger L (1978) Comparative anatomy of elementary shell structure in selected larger foraminifera. In: Hedley R, Adams CG (eds) Foraminifera, vol. 3. Academic, London, pp 203–206Google Scholar
  30. Hottinger L (1984) Foraminiféres de grande taile: signification des structures complexes de la coquille. Benthos 83: 2nd International Symposium on Benthic Foraminifera, Pau 1983. Pp. 309–315. Pau et BordeauxGoogle Scholar
  31. Hottinger L (2000) Functional morphology of benthic foraminiferal shells, envelopes of cells beyond measure. In: Lee JJ, Muller PH (eds) Advances in the biology of foraminifera. Micropaleontology 46 (supplement 1):57–86Google Scholar
  32. Hottinger L, Dreher D (1974) Differentiation of protoplasm in Nummulitidae (Foraminifera) from Elat, Red Sea. Mar Biol 25:41–61CrossRefGoogle Scholar
  33. Hottinger L, Leutenegger S (1980) The structure of calcarinid foraminifera. Schweizerische Palaontolgische Abhandlungen 101:115–150Google Scholar
  34. Hyams-Kaphzan O, Lee JJ (2009) Cytological examination and location of symbionts in “living sands”-Baculogypsina. J Foramin Res 38:298–304CrossRefGoogle Scholar
  35. Hyman L (1940) The invertebrates: protozoa through Ctenophora. McGraw-Hill, New York, pp 44–45Google Scholar
  36. Iglesias-Prieto R, Matta JL, Robins WA, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89:10302–10305CrossRefPubMedGoogle Scholar
  37. Kremer BP, Schmaljohann R, Röttger R (1980) Features and nutritional significance of photosynthates produced by unicellular algae symbiotic with larger foraminifera. Mar Ecol Prog Ser 2:225–228CrossRefGoogle Scholar
  38. Langer MR, Lipps JH (1995) Phylogenetic incongruence between dinoflagellate endosymbionts (Symbiodinium) and their host foraminifera (Sorites): small subunit ribosomal RNA gene sequence evidence. Mar Micropaleontol 26:179–186CrossRefGoogle Scholar
  39. Lee JJ (1990) Fine structure of the rhodophycean Porhyridium purpureum in situ in Peneroplis pertusus (Forskål) and P. acicularis (Batsch) and in axenic culture. J Foramin Res 20:162–169CrossRefGoogle Scholar
  40. Lee JJ (2006) Symbiotic forms of life. In: Seckbach J (ed) Life as we know it. Springer, Dordrecht, pp 307–324Google Scholar
  41. Lee JJ, Zucker W (1969) Algal flagellate symbiosis in the foraminifera Archaias angulatus. J Protozool 16:71–81Google Scholar
  42. Lee JJ, Hallock P (1987) Algal symbiosis as the driving force in the evolution of larger foraminifera. Annals New York Academy of Science 503:330–347CrossRefGoogle Scholar
  43. Lee JJ, Hallock PH (eds) (2000) Advances in the biology of the Foraminifera. Micropaleontology 46 (supplement 1). Micropaleontology Press, New York, pp368Google Scholar
  44. Lee JJ, Correia M (2005) Endosymbiotic diatoms from previously unsampled habitats. Symbiosis 38:251–260Google Scholar
  45. Lee JJ, Reyes D (2006) Initial studies of dinoflagellate recognition in Soritinae. Symbiosis 42:89–93Google Scholar
  46. Lee JJ, Crockett LJ, Hagen J, Stone R (1974) The taxonomic identity and physiological ecology of Chlamydomonas hedleyi sp. From the foraminifer Archaias angulatus. Br Phycol J 9:407–422CrossRefGoogle Scholar
  47. Lee JJ, McEnery ME, Kahn E, Schuster F (1979) Symbiosis and the evolution of larger foraminifera. Micropaleontology 25:118–140CrossRefGoogle Scholar
  48. Lee MJ, Ellis R, Lee JJ (1982) A comparative study of photoadaptation in four diatoms isolated as endosymbionts from larger foraminifera. Mar Biol 68:193–197CrossRefGoogle Scholar
  49. Lee JJ, Saks NM, Kapiotou F, Wilen SH, Shilo M (1984) Effects of host cell extracts on cultures of endosymbiotic diatoms from larger foraminifera. Mar Biol 82:113–120CrossRefGoogle Scholar
  50. Lee J, Lanners E, terKuile B (1988) The retention of chloroplasts by the foraminifer Elphidium crispum. Symbiosis 5:45–60Google Scholar
  51. Lee JJ, Faber WW, Lee RE (1991) Granular reticulopodal digestion—A possible preadaption to benthic foraminiferal symbiosis? Symbiosis 10:47–51Google Scholar
  52. Lee JJ, Wray CG, Lawrence C (1995) Could foraminiferal zooxanthellae be derived from environmental pools contributed to by different coelenterate hosts? Acta Protozool 34:75–85Google Scholar
  53. Lee JJ, Morales J, Bacus S, Diamont A, Hallock P, Pawlowski J, Thorpe J (1997) Progress in characterizing the endosymbiotic dinoflagellates of soritid foraminifera and related studies on some stages of the life cycle of Marginopora vertebralis. J Foramin Res 27:254–263CrossRefGoogle Scholar
  54. Lee JJ, Correia M, Reimer CW, Morales J (2001) A revised description of the Nitzschia frustulum var. symbiotica complex, the most common of the endosymbiotic diatoms in larger foraminifera. In: Lee JJ, Muller PH (eds) Advances in the Biology of Foraminifera. Micropaleontology 46 (supplement 1): 170–182Google Scholar
  55. Lee JJ, Fine M, Levy O, Morales J (2009) A note on asexual reproduction of a Marginopora sp. from a modern deep-water population in the Heron-Wistari Channel, Australia. J Foramin Res 39:4–7CrossRefGoogle Scholar
  56. Lee JJ, Cervasco M, Morales J, Billick MG, Fine M, Levy O. 2010. A new genus of symbiotic dinoflagellates, Symbiodinoides, from some soritid foraminifera and a new species, Symbiodinoides dubinskyi from the Heron-Wistori Channel,Great Barrier Reef, Australia. (Journal of Eukaryotic Microbiology (In review)Google Scholar
  57. Leutenegger S (1977) Symbiosis between larger foraminifera and unicellular algae in the Gulf of Elat. Utrecht Micropaleontol Bull 1:241–244Google Scholar
  58. Leutenegger S (1984) Symbiosis in benthic foraminifera: specificity and host adaptation. J Foramin Res 14:16–35CrossRefGoogle Scholar
  59. Leutenegger S, Hansen H (1979) Ultrastructural and radiotracer studies of pore-function in foraminifera. Mar Biol 5:11–16CrossRefGoogle Scholar
  60. Lipps JH, Severin KP (1986) Alveolina quoyi, a living fusiform foraminifer at Motupore Island, Papua, New Guinea. Sci N Guin 11:126–137Google Scholar
  61. Lopez R (1979) Algal chloroplastsin the protoplasm of three species of benthic foraminifera: taxonomic affinity, viability and persistence. Mar Biol 53:201–211CrossRefGoogle Scholar
  62. Müller-Merz E, Lee JJ (1976) Symbiosis in the larger foraminiferan Sorites marginales (with notes on Archaias spp). J Protozool 23:390–396Google Scholar
  63. Newell ND (1949) Phyletic size increase, an important trend illustrated by fossil invertebrates. Evolution 3:103–124CrossRefPubMedGoogle Scholar
  64. Pawlowski J, Holzmann M, Fahrni JF, Pochon X, Lee JJ (2001) Molecular identification of algal endosymbionts in large miliolid foraminifera: 2 Dinoflagellates. J Eukaryot Microbiol 48:368–373CrossRefPubMedGoogle Scholar
  65. Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078CrossRefGoogle Scholar
  66. Pochon X, LaJeunesse TC, Pawlowski J (2004) Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Mar Biol 146:17–27CrossRefGoogle Scholar
  67. Pochon X, Montoya-Burgos J, Stadelman B, Pawlowski J (2006) Molecular phylogeny, Evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol 38:20–30CrossRefPubMedGoogle Scholar
  68. Reichel M (1936) Etude sur les Alvéolines. Mémoires Suisses Paleontologie 57:1–93Google Scholar
  69. Reichel M (1937) Etude sur les Alvéolines. Mémoires Suisses Paleontologie 59:95–147Google Scholar
  70. Schoenberg DA, Trench RK (1980a) Genetic variation in Symbiodinium (Gymnodinium) microadriaticum Freudenthal and specificityin its symbiosis with marine invertebrates. I. Isoenzyme and soluble protein patterns of axenic cultures of S. microadriaticum. Proc R Soc Lond B 207:405–427CrossRefGoogle Scholar
  71. Schoenberg DA, Trench RK (1980b) Genetic variation in Symbiodinium (Gymnodinium) microadriaticum Freudenthal and specificityin its symbiosis with marine invertebrates. II. Morphological variation in S. microadriaticum. Proc R Soc Lond B 207:429–444CrossRefGoogle Scholar
  72. Schoenberg DA, Trench RK (1980c) Genetic variation in Symbiodinium (Gymnodinium) microadriaticum Freudenthal and specificityin its symbiosis with marine invertebrates. III. Specificity and infectivity of S. microadriaticum. Proc R Soc Lond B 207:445–460CrossRefGoogle Scholar
  73. Spiro HJ (1987) Symbiosis in the planktonic foraminifer Orbulina universa and the isolation of its symbiotic dinoflagellate, Gymnodinium beii sp. nov. J Phycol 21:307–317CrossRefGoogle Scholar
  74. Sutton DC, Hoegh-Guldberg O (1990) Host-zooxanthella interactions in four temperate marine invertebrate symbioses: assessment of host extract on symbionts. Biol Bull 178:175–186CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • John J. Lee
    • 1
    • 2
  • Megan H. Cervasco
    • 1
    • 2
  • Jorge Morales
    • 3
  • Morgan Billik
    • 1
  • Maoz Fine
    • 4
    • 5
  • Oren Levy
    • 5
  1. 1.Department of BiologyCity College of City University of New YorkNew YorkUSA
  2. 2.Department of InvertebratesAmerican Museum of Natural HistoryNew YorkUSA
  3. 3.Central Electron Microscope FacilityCity College of City University of New YorkNew YorkUSA
  4. 4.The Interuniversity Institute for Marine ScienceEilatIsrael
  5. 5.The Mina and Everard Goodman Faculty of Life SciencesBar-Ilan UniversityRamat-GanIsrael

Personalised recommendations