Skip to main content

Diatoms as Endosymbionts

  • Chapter
  • First Online:

Part of the book series: Cellular Origin, Life in Extreme Habitats and Astrobiology ((COLE,volume 19))

Abstract

Diatoms, or their plastids, are symbionts of four different families of foraminifera. Evidence suggests that the evolution of these families was driven by their symbiotic relationships. All hosts are many times larger than their ancestors, have complex subcompartmentalization, and have multiple nuclei and internal organelles (e.g., Golgi, mitochondria). The diatom symbionts and the captured plastids are photosynthetically active. Symbiotic diatoms have a 104 kDa glycoprotein epitope on their surfaces that is recognized by receptors on the host’s reticulopodia. Less than two dozen species of diatoms are involved in the phenomenon. All are small (≤10 μm). Nitzschia frustulum var. symbiotica is the most common species. This species along with two other species of Nitzschia, N. laevis Hustedt and N. panduriformis var. continua Grunow in Cleve and Grunow, Nanofrustulum shiloi (Lee, Reimer, and McEnery), Amphora roettgerii Lee and Reimer, and Amphora erezii Reimer and Lee, were isolated from over 75% of the associations. Several diatom species have unusual mechanisms for size regeneration. Host homogenate experiments suggest that there are signals that cause the symbiotic diatoms not to form frustules and to release their photosynthetates. Benefits to the holobiont and to each symbiont are discussed.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Buchardt, B. and Hansen, H.J. (1977) Oxygen isotope fractionation and algal symbiosis in benthic foraminifera from the Gulf of Elat, Israel. Bull. Geol. Soc. Den. 26: 185–194.

    CAS  Google Scholar 

  • Carpenter, W.B. (1862) Introduction to the Study of Foraminifera. Hardwicke, London, pp. 1–319.

    Google Scholar 

  • Chai, J. and Lee, J.J. (1999a) Initial recognition of endosymbiotic diatoms by the larger foraminifer Amphistegina lobifera. Symbiosis 26: 39–53.

    Google Scholar 

  • Chai, J. and Lee, J.J. (1999b) Establishment and maintenance of endosymbiotic diatoms by the larger foraminifer Amphistegina lobifera. In: E. Wagner, J. Norman, H. Greppin, J.H.P. Hackstein, R.G. Herrmann, K.V. Kowalik, H.E.A. Schenk and J. Seckbach (eds.) Endocytobiology VII. Universities of Freiburg and Geneva, Germany and Geneva, pp. 137–152.

    Google Scholar 

  • Chai, J. and Lee, J.J. (2000) Recognition, establishment and maintenance of diatom endosymbioses in foraminifera. In: J.J. Lee and P.H. Muller (eds.) Advances in the Biology of Foraminifera. Micropaleontology 46 (supplement 1). Micropaleontology Press, New York, pp. 182–195.

    Google Scholar 

  • Correia, M.J. and Lee, J.J. (2000) Chloroplast retention by Elphidium excavatum (Terquem). Is it a selective process? Symbiosis 29: 343–355.

    Google Scholar 

  • Correia, M.J. and Lee, J.J. (2002a) Fine structure of the plastids retained by the foraminifer Elphidium excavatum (Terquem). Symbiosis 32: 15–26.

    Google Scholar 

  • Correia, M.J. and Lee, J.J. (2002b) How long do the plastids retained by Elphidium excavatum (Terquem) last in their host? Symbiosis 32: 27–38.

    Google Scholar 

  • Dietz-Elbrächter, G. (1971) Untersuchungen über die Zooxanthellen der Foraminifere Heterostegina depressa Orbigny 1826. Met. Forsch.-Ergebnisse 6: 41–47.

    Google Scholar 

  • Duguay, L. (1983) Comparative laboratory and field studies on calcification and carbon fixation in foraminiferal-algal associations. J. Foram. Res. 13: 252–261.

    Article  Google Scholar 

  • Duguay, L and Taylor, D.L. (1978) Primary production and calcification by the soritid foraminifer Archais angulatus (Fichel and Moll). J. Protozool. 25: 356–361.

    Google Scholar 

  • Erez, J. (1978) Vital effect on stable-isotope composition seen in foraminifera and coral skeletons. Nature 273: 199–202.

    Article  CAS  Google Scholar 

  • Faber, W.W. and Lee, J.J. (1991a) Histochemical evidence for digestion in Heterostegina depressa and Operculina ammonoides (Foraminifera). Endocytobiol. Cell Res. 8: 53–59.

    Google Scholar 

  • Faber, W.W. and Lee, J.J. (1991b) Feeding and growth of Peneroplis planatus (Fichel and Moll) Montfort. Symbiosis 10: 63–82.

    Google Scholar 

  • Freudenthal, H.D. (1962) Symbiodinium gen. nov., and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle and morphology. J. Protozool. 9: 45–52.

    Google Scholar 

  • Fritch, F.E. (1935) The Structure and reproduction of the algae. Vol. 1. Cambridge. 791 pp. 243 figs.

    Google Scholar 

  • Geitler, L. (1932) Der Formwechsel der pennaten Diatomeen. (Kieselalgen). Archiv. Protistenk. 78: 1–226.

    Google Scholar 

  • Geitler, L. (1969). Notizen über die Auxosporenbildung einiger pennater Diatomeen. Österreich. Botan. Zeitschrift 117: 265–275.

    Google Scholar 

  • Guillard, R.R.L. (1975) Culture of phytoplankton for feeding marine invertebrates. In: W.L. Smith and M.H. Chanley (eds) Culture of Marine Invertebrate Animals. Plenum Press, New York, pp. 29–60.

    Google Scholar 

  • Hallock, P. (1981) Light dependence in Amphistegina. J. Foram. Res. 11: 40–46

    Article  Google Scholar 

  • Hallock, P. (1985) Why are larger foraminifera large? Paleobiology 11: 195–208.

    Google Scholar 

  • Hallock, P., Forward, L.B. and Hansen, H.J. (1986) Environmental influence of test shape in Amphistegina. J. Foram. Res. 16: 224–231.

    Article  Google Scholar 

  • Hansen, H.J. and Burchardt, B. (1977) Depth distribution of Amphistegina in the Gulf of Elat, Israel. Utrecht Micropaleont. Bull. 15: 205–244.

    Google Scholar 

  • Hofker, J. (1927) The foraminifera of the Siboga Expedition; Part 1. Monographs Siboga Expedition 1899–1900 (Leiden) 4: 1–78.

    Google Scholar 

  • Hottinger, L. (1977) Foraminiféres operculinoformes. Mem. Musé. Hist. Nat., Paris Série C Sciences terre XL, 1–159.

    Google Scholar 

  • Hottinger, L. (1978) Comparative anatomy of elementary shell structure in selected larger foraminifera, In: R. Hedley and C.G. Adams (eds.) Foraminifera, vol. 3. Academic, London, UK, pp. 203–206.

    Google Scholar 

  • Hottinger, L. (1984) Foraminiféres de grande taile: signification des structures complexes de la coquille. Benthos 83: 2nd International Symposium on Benthic Foraminifera, Pau 1983, Pau et Bordeaux, pp. 309–315.

    Google Scholar 

  • Hottinger, L. (2000) Functional morphology of benthic foraminiferal shells, envelopes of cells beyond measure. In: J.J. Lee and P.H Muller (eds.) Advances in the Biology of Foraminifera. Micropaleontology 46 (supplement 1). Micropaleontology Press, New York, pp. 57–86.

    Google Scholar 

  • Hottinger, L. and Dreher, D. (1974) Differentiation of protoplasm in Nummulitidae (Foraminifera) from Elat, Red Sea. Mar. Biol. 25: 41–61.

    Article  Google Scholar 

  • Hottinger, L. and Leutenegger, S. (1980) The structure of calcarinid foraminifera. Schweiz. Palaontol. Abhand. 101: 115–150.

    Google Scholar 

  • Hottinger, L. Halicz, E. and Reiss, Z. (1993) Recent foraminifera from the Gulf of Aqaba, Red Sea. Slovenska Akademiga Znanosti in Umetnosti, Acadenia Scientiarium et Atrium Slovenica, Classis IV. Hist. Nat. 33: 1–179. plates 1–230.

    Google Scholar 

  • Hyams-Kaphzan O. and Lee, J.J. (2009) Cytological examination and location of symbionts in “living sands” – Baculogypsina. J. Foram. Res. 38: 298–304.

    Article  Google Scholar 

  • Knight, R. and Mantoura, R.C.F. (1985) Chloroplast and carotenoid pigments in foraminifera and their symbiotic algae: analysis by high performance liquid chromatography. Mar. Ecol. Prog. Ser. 23: 241–249.

    Article  CAS  Google Scholar 

  • Kuile ter B. and Erez, J. (1987) Uptake of inorganic carbon and internal cycling in symbiont-bearing benthic foraminifera. Mar. Biol. 94: 499–509.

    Article  Google Scholar 

  • Kuile ter, B, Erez, J. and Lee, J.J. (1987) The role of feeding in the metabolism of larger symbiont bearing foraminifera. Symbiosis 4: 335–350.

    Google Scholar 

  • Kuile ter, B.H., Kaplan, A. and Lee, J.J. (1988) Uptake of inorganic carbon by Fragilaria shiloi, the symbiont of the foraminifer Amphistegina lobifera. Symbiosis 6: 225–236.

    Google Scholar 

  • Kuile ter, B. Erez, J. and Padan, E. (1989a) Mechanisms for the uptake of inorganic carbon by two species of symbiont-bearing foraminifera. Mar. Biol. 103: 241–251.

    Google Scholar 

  • Kuile ter, B. Erez, J. and Padan, E. (1989b) Competition for inorganic carbon between the processes of photosynthesis and calcification in the symbiont-bearing foraminifer Amphistegina lobifera. Mar. Biol. 103: 253–259.

    Google Scholar 

  • Kuile ter, B. (1991) Mechanisms for calcification and carbon cycling in algal symbiont-bearing foraminifera. In: J.J. Lee and O.R. Anderson (eds.) Biology of Foraminifera. Academic Press. London, pp.73–90.

    Google Scholar 

  • Lee, J.J. (1983) Perspective on algal symbionts in larger foraminifera. Int. Rev. Cytol. Suppl. 14: 49–77.

    Google Scholar 

  • Lee, J.J. (1994) Diatoms and their chloroplasts as endosymbiotic partners for larger foraminifera, XI symposium on living and fossil diatoms. Mem. Calif. Acad. Sci. 17: 21–36.

    Google Scholar 

  • Lee, J.J. (1995) Infundibuliform frustule formation by endosymbiotic Fragilaria shiloi in primary isolation cultures from hosts in the Pacific Ocean. In: J.P. Kociolek and M.J. Sullivan (eds.) A Century of Diatom Research in North America. Koelz Scientific Books, Koenigstein, Germany, pp. 125–131.

    Google Scholar 

  • Lee, J.J. (2006) Symbiotic forms of life. In: J. Seckbach (ed.) Life as We Know It. Springer, Dordrecht, The Netherlands, pp, 307–324.

    Google Scholar 

  • Lee, J.J. and Correia, M. (2005) Endosymbiotic diatoms from previously unsampled habitats. Symbiosis 38: 251–260.

    CAS  Google Scholar 

  • Lee, J.J. and Hallock, P. (1987) Algal symbiosis as the driving force in the evolution of larger foraminifera. Ann. N. Y. Acad. Sci. 503: 330–347.

    Article  Google Scholar 

  • Lee, J.J. and Hallock, P.H. (eds.) (2000) Advances in the Biology of the Foraminifera. Micropaleontology 46 (supplement 1), Micropaleontology Press, New York, p. 368.

    Google Scholar 

  • Lee, J.J. and Lee, R.E. (1990) Chloroplast retention in elphids (foraminifera), In: P. Nardon, V. Gianinazzi-Pearson, A.R. Grenier, L. Margulis and D.C. Smith (eds.) Endocytobiology IV. Instite National de la Research Agronomique, INSA, Paris, France, pp. 215–220.

    Google Scholar 

  • Lee, J.J. and Reimer, C.W. (1984) Isolation and identification of endosymbiotic diatoms from larger foraminifera of the Great Barrier Reef, Australia, Makapuu Tide Pool, Oahu, Hawaii, and the Gulf of Elat, Israel, with the description of new species, Amphora Roetgerii, Navicula Hanseniana and Nitzschia frustulum variety symbiotica. Proc. VII Inter. Symp. Living and Fossil Diatoms (Mann, D. G., ed.) Koeltz Scientific Books, Koenigstein, Germany.

    Google Scholar 

  • Lee, J.J. and Reyes, D. (2006) Initial studies of dinoflagellate recognition in Soritinae. Symbiosis 42: 89–93.

    CAS  Google Scholar 

  • Lee, J.J. and Xenophontos, X. (1989) The unusual life cycle of Navicula muscatini. Diatom Res. 4: 69–77.

    Google Scholar 

  • Lee, J.J. and Zucker, W. (1969) Algal flagellate symbiosis in the foraminifera Archaias angulatus. J. Protozool. 16: 71–81.

    Google Scholar 

  • Lee, J.J., McEnery, M., Shilo, M. and Reiss, Z. (1979) Isolation and cultivation of diatom symbionts from larger foraminifera (Protozoa). Nature 280(5717): 57–58.

    Article  Google Scholar 

  • Lee, J.J., McEnery, M.E. and Garrison, J.R. (1980) Experimental studies of larger foraminifera and their symbionts from the Gulf of Elat on the Red Sea. J. Foram. Res. 10: 31–47.

    Article  Google Scholar 

  • Lee, J.J., McEnery, M.E., and Garrison, J.R. (1980a) Experimental studies of larger foraminifera and their symbionts from the Gulf of Elat on the Red Sea. J. Foram. Res. 10: 31–47.

    Google Scholar 

  • Lee, J. J., McEnery, M.E., Röttger, R. and Reimer, C.W. (1980b) The isolation, culture and identification of endosymbiotic diatoms from Heterostegina depressa d’Orbigny and Amphistegina lessonii d’Orbigny (larger foraminifera) from Hawaii. Botanica Marina 23: 297–302.

    Google Scholar 

  • Lee, J. J., Reimer, C.W. and McEnery, M.E. (1980c). The identification of diatoms isolated as endosymbionts from larger foraminifera from the Gulf of Elat (Red Sea) and the description of 2 new species, Fragilaria shiloi, sp. nov. and Navicula reisii sp. nov. Botanica Marina 23: 41–48.

    Google Scholar 

  • Lee, M.J., Ellis, R. and Lee, J.J. (1982) A comparative study of photoadaptation in four diatoms isolated as endosymbionts from larger foraminifera. Mar. Biol. 68: 193–197.

    Article  Google Scholar 

  • Lee, J.J., McEnery, M.E., Koestler, R.L., Lee, M.J., Reidy, J. and Shilo, M. (1983) Experimental studies of symbiont persistence in Amphistegina lessoni, a diatom-bearing species of larger foraminifera from the Red Sea, In: H.E.A. Schenk and W. Schwemmler (eds.) Endocytobiology II. Walter de Gruyter & Co., Berlin/New York, pp. 487–514.

    Google Scholar 

  • Lee, J.J., Saks, N.M., Kapiotou, F., Wilen, S.H. and Shilo, M. (1984) Effects of host cell extracts on cultures of endosymbiotic diatoms from larger foraminifera. Mar. Biol. 82: 113–120.

    Article  Google Scholar 

  • Lee, J.J., Erez, J., McEnery, M.E., Lagziel, A. and Xenophontos, X. (1986) Experiments on persistence of endosymbiotic diatoms in the larger foraminifer: Amphistegina lessonii. Symbiosis 1: 211–226.

    CAS  Google Scholar 

  • Lee, J., Lanners, E. and terKuile, B. (1988) The retention of chloroplasts by the foraminifer Elphidium crispum. Symbiosis 5: 45–60.

    CAS  Google Scholar 

  • Lee, J.J., Faber W.W. and Lee, R.E. (1991) Granular reticulopodal digestion – a possible preadaption to benthic foraminiferal symbiosis? Symbiosis 10: 47–51.

    Google Scholar 

  • Lee, J.J., Wray, C.G. and Lawrence, C. (1995) Could foraminiferal zooxanthellae be derived from environmental pools contributed to by different coelenterate hosts? Acta Protozool 34: 75–85.

    Google Scholar 

  • Lee, J.J., Correia, M., Reimer, C.W. and Morales, J. (2000) A revised description of the Nitzschia frustulum var. symbiotica complex, the most common of the endosymbiotic diatoms in larger foraminifera. In: J.J. Lee and P.H. Muller (eds.) Advances in the Biology of Foraminifera. Micropaleontology 46 (supplement 1). Micropaleontology Press, New York, pp. 170–182.

    Google Scholar 

  • Lee, J.J., Cervasco, M.H., Morales, J., Billik, M., Fine, M. and Levy, O. (2010) Symbiosis drove cellular evolution. Symbiosis 51: 13–25.

    Article  Google Scholar 

  • Lee, J.J., Correia, M., Reimer, C.W., and Morales, J. (2001) A revised description of the Nitzschia frustulum var. symbiotica complex, the most common of the endosymbiotic diatoms in larger foraminifera. In: J.J. Lee and P.H. Muller (eds.) Advances in the Biology of Foraminifera. Micropaleonto. 46 (supplement 1): 170–182.

    Google Scholar 

  • Leutenegger, S. (1977) Symbiosis between larger foraminifera and unicellular algae in the Gulf of Elat. Utrecht Micropaleontol. Bull. 1: 241–244.

    Google Scholar 

  • Leutenegger, S. (1984) Symbiosis in benthic foraminifera: specificity and host adaptation J. Foram. Res. 14: 16–35.

    Article  Google Scholar 

  • Leutenegger, S. and Hansen, H. (1979) Ultrastructural and radiotracer studies of pore-function in foraminifera. Mar. Biol. 5: 11–16.

    Article  Google Scholar 

  • Lipps, J.H. and Severin, K.P. (1986) Alveolina quoyi, a living fusiform foraminifer at Motupore Island, Papua, New Guinea. Sci. N. G. 11: 126–137.

    Google Scholar 

  • Lopez, R. (1979) Algal chloroplastsin the protoplasm of three species of benthic foraminifera: taxonomic affinity, viability and persistence. Mar. Biol. 53: 201–211.

    Google Scholar 

  • Mayama, S., Nagumot, T. and Kuriyama, A. (2000) Isolation and identification of endosymbiotic diatoms from planktonic and benthic species of foraminifera. Diatom 16: 3–10.

    Google Scholar 

  • McLaughlin, J.J.A. and Zahl, P.A. (1959) Axenic zooxanthellae from various invertebrate hosts. Ann N. Y. Acad. Sci. 77: 55–72.

    Article  Google Scholar 

  • Muller, P.H. (1978) 14Carbon fixation and loss in a foraminiferal-algal symbiont system. J. Foram. Res. 8: 35–41.

    Article  CAS  Google Scholar 

  • Muscatine, L. (1967) Glycerol excretion by symbiotic algae from corals and Tridacna, and its control by the host. Science 156: 516–519.

    Article  PubMed  CAS  Google Scholar 

  • Provasoli L., McLaughlin J.J.A. and Droop, M.R. (1957) The development of artifical media for marine algae. Arch. Mikrobiol. 25: 392–428.

    Article  Google Scholar 

  • Reichel, M. (1936) Etude sur les Alvéolines. Mémoires Suisses Paleontol. 57: 1–93.

    Google Scholar 

  • Reichel, M. (1937) Etude sur les Alvéolines. Mém. Suisses Paleontol. 59: 95–147.

    Google Scholar 

  • Reiss, Z. and Hottinger, L. (1984) The Gulf of Aqaba – Ecological Micropaleontology. Ecological Studies 50. Springer, Berlin, p. 354.

    Google Scholar 

  • Röttger, R., Irwan, R., Schmaljohann, R. and Franziskat, L. (1980) Growth of the symbiont-bearing foraminifera Amphistegina lessoni d’Orbigny and Heterostegina depressa d’Orbigny (Protozoa), In: W. Schwemmler and H.E.A. Schenk (eds) Endocytobiology, vol I. Walter de Gruyter & Co., Berlin, pp. 125–132.

    Google Scholar 

  • Schmaljohann, R. and Röttger, R. (1978) The ultrastructure and taxonomic identity of the symbiotic algae of Heterostegina depressa (Foraminifera, Nummulitidae). J. Mar. Biol. Assoc. UK 58: 227–237.

    Article  Google Scholar 

  • Sutton, D.C. and Hoegh-Guldberg, O. (1990) Host-zooxanthella interactions in four temperate marine invertebrate symbioses: assessment of host extract on symbionts. Biol. Bull. 178: 175–186.

    Article  Google Scholar 

  • Zmiri, A. Kahn, D. Hochstein, S. and Reiss, Z. (1974) Phototaxis and thermotaxis in some species of Amphistegina (Foraminifera). J. Protozool. 21: 133–138.

    Google Scholar 

Download references

Acknowledgments

Research over the years was supported by grants from the NSF, NIH, BSF, and PSC-CUNY. Many people have organized students or have themselves collected specimens for research including: Amatzia Gennin, Pamela Hallock, Arik Diamont, Angelo Colorni, Jonathan Erez, Beverly Goodman, and Beno ter Kuile. Among the many students and colleagues who have been involved in various phases of the work, particular mention should be made of the major contributions of Drs. Charles W. Reimer, Walter Faber, Pamela Hallock, Maria Correia, Jianyuan Chai, Zeev Reiss, Moshe Shilo, Megan Cervasco, and Jorge Morales.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John J. Lee .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media B.V

About this chapter

Cite this chapter

Lee, J.J. (2011). Diatoms as Endosymbionts. In: Seckbach, J., Kociolek, P. (eds) The Diatom World. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 19. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1327-7_20

Download citation

Publish with us

Policies and ethics