Centrohelida and Other Heliozoan-Like Protists

  • Rebecca J. Gast
Living reference work entry


The Centrohelida has arisen through the dissolution of the Heliozoa and the gradual removal of morphologically similar, but ultrastructurally and genetically distinct taxa from the group. The taxonomy of these other heliozoan-like protists is still largely influx, as are the groups within the Centrohelida. Centrohelida and heliozoan-like protists are heterotrophic, free-living species that are found in most aquatic benthic environments where they feed on bacteria and other protists, including algae. Morphologically the cells are conspicuous, generally round in shape with eye-catching raylike axopodia. They can be found in habitats that represent a wide range of temperatures and salinities, including extreme environments. Most are free floating, but some attach to substrates by a stalk. Interest in the heliozoan-like protists (“sun animalcules”) is largely in regard to cell biology. Their size (some can be 500 μm in diameter) and axopodial structure have made them useful subjects for biochemical and ultrastructural studies of microtubules.


Axoplast Axopodia Centrohelids Centroplast Heliozoa 



Revised from the original chapter of Colette Febvre-Chevalier


  1. Adl, S. M., Simpson, A. G. B., Farmer, M. A., Andersen, R. A., Anderson, O. R., Barta, J. R., Bowser, S. S., Brugerolle, G., Fensome, R. A., Fredericq, S., James, T. Y., Karpov, S., Kugrens, P., Krug, J., Lane, C. E., Lewis, L. A., Lodge, J., Lynn, D. H., Mann, D. G., McCourt, R. M., Mendoza, L., Moestrup, O., Mozley-Standridge, S. E., Nerad, T. A., Shearer, C. A., Smirnov, A. V., Spiegel, F. W., & Taylor, F. J. R. (2005). The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. Journal of Eukaryotic Microbiology, 52(5), 399–451.CrossRefPubMedGoogle Scholar
  2. Adl, S. M., Simpson, A. G. B., Lane, C. E., Lukeš, J., Bass, D., Bowser, S. S., Brown, M. W., Burki, F., Dunthorn, M., Hampl, V., Heiss, A., Hoppenrath, M., McManus, H., Mitchell, E. A., Mozley-Stanridge, S. E., Parfrey, L. W., Pawlowski, J., Rueckert, S., Shadwick, L., Schoch, C. L., Smirnov, A., & Spiegel, F. W. (2012). The revised classification of eukaryotes. The Journal of Eukaryotic Microbiology, 59(5), 429–514.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Amaral Zettler, L. A., Messerli, M. A., Laatsch, A. D., Smith, P. J. S., & Sogin, M. L. (2000). From genes to genomes: Beyond biodiversity in Spain’s Rio Tinto. Biological Bulletin, 204, 205–209.CrossRefGoogle Scholar
  4. Anderson, O. R. (1988). Comparative protozoology: Ecology, physiology, life history. New York: Springer Science + Business Media.CrossRefGoogle Scholar
  5. Arikawa, M., Saito, A., Omura, G., Khan, S. M. M. K., Suetomo, Y., Kakuta, S., & Suzaki, T. (2006). Ca2+-dependent in vitro contractility of a precipitate isolated from an extract of the heliozoon Actinophrys sol. Cell Motility and the Cytoskeleton, 63(2), 57–65.CrossRefPubMedGoogle Scholar
  6. Bardele, C. F. (1972). Cell cycle, morphogenesis and ultrastructure in the pseudoheliozoan Clathrulina elegans. Zeitschrift für Zellforschung, 130, 219–242.CrossRefGoogle Scholar
  7. Bardele, C. F. (1975). The fine structure of the centrohelidan heliozoan Heterophrys marina. Cell Tissue Research, 161, 85–102.CrossRefPubMedGoogle Scholar
  8. Bass, D., Chao, E. E.-Y., Nikolaev, S., Yabuki, A., Ishida, K., Berney, C., Pakzad, U., Wylezich, C., & Cavalier-Smith, T. (2009). Phylogeny of novel naked filose and reticulose cercozoa: Granofilosea cl.n. and Proteomyxidea revised. Protist, 160, 75–109.CrossRefPubMedGoogle Scholar
  9. Bĕlař, K. (1923). Untersuchungen an Actinophrys sol Ehrenberg. I. Die Morphologie des Formwechels. Archiv für Protistenkunde, 46, 1–96.Google Scholar
  10. Brugerolle, G., & Mignot, J.-P. (1983). Caractéristiques ultrastructurales de l’hélioflagelle Tetradimorpha Hsiung et lur intérêt pour l’étude Phylétique des héliozoaires. Journal of Protozoology, 30(3), 473–480.CrossRefGoogle Scholar
  11. Brugerolle, G., & Mignot, J.-P. (1984). The cell characters of two helioflagellates related to the centroheliolian lineage: Dimorpha and Tetradimorpha. Origins of Life, 13(314), 305.CrossRefGoogle Scholar
  12. Burki, F., Inagaki, Y., Bråte, J., Archibald, J. M., Keeling, P. J., Cavalier-Smith, T., Sakaguchi, M., Hashimoto, T., Horak, A., Kumar, S., Klaveness, D., Jakobsen, K. S., Pawlowski, J., & Shalchian-Tabrizi, K. (2009). Large-scale phylogenomic analyses reveal that two enigmatic protest lineages, Telonemia and Centroheliozoa, are related to photosynthetic chromalveolates. Genome Biology and Evolution, 1, 231–238.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cachon, J., & Cachon, M. (1978). Sticholonche zanclea Hertwig. A reinterpretation of its phylogenetic position based upon new observations on its ultrastructure. Archiv für Protistenkunde, 120, 148–168.CrossRefGoogle Scholar
  14. Cachon, J., & Cachon, M. (1984). Various effects induced by chemical microtubule inhibitors and neurodrugs on the microtubular system of the heliozoan Sticholonche zanclea. Archiv für Protistenkunde, 128, 25–35.CrossRefGoogle Scholar
  15. Cachon, J., Cachon, M., Tilney, L. G., & Tilney, M. (1977). Movement by interaction between the dense material at the end of microtubules and non-actin microfilaments in Sticholonche zanclea. Journal of Cell Biology, 72, 314–338.CrossRefPubMedGoogle Scholar
  16. Cavalier-Smith, T., & Chao, E. E. (2003). Molecular phylogeny of centrohelid heliozoa, a novel lineage of bikont eukaryotes that arose by ciliary loss. Journal of Molecular Evolution, 56, 387–396.CrossRefPubMedGoogle Scholar
  17. Cavalier-Smith, T., & von der Heyden, S. (2007). Molecular phylogeny, scale evolution and taxonomy of centrohelid heliozoa. Molecular Phylogenetics and Evolution, 44, 1186–1203.CrossRefPubMedGoogle Scholar
  18. Cienkowsky, L. (1876). Über einige Rhizopoden und verwandte Organismen. Arch Mikroskop Anat, 12, 15–50.Google Scholar
  19. Davidson, L. A. (1975). Studies on the actinopods Heterophrys marina and Ciliophrys marina: Energetics and structural analysis of their contractile axopodia, general ultrastructure and phylogenetic relationships. PhD thesis, University of California at Berkeley.Google Scholar
  20. Davidson, L. A. (1976). Ultrastructure of membrane attachment sites of the extrusomes of Ciliophrys marina and Heterophrys marina (Actinopoda). Cell Tissue Research, 170, 353–365.CrossRefPubMedGoogle Scholar
  21. Dustin, P. (1978). Microtubules. New York: Springer.CrossRefGoogle Scholar
  22. Edds, K. (1975). Motility in Echinosphaerium nucleofilum. II. Cytoplasmic contractility and its molecular basis. Journal of Cell Biology, 66, 156–164.CrossRefPubMedGoogle Scholar
  23. Febvre-Chevalier, C. (1973a). Hedraiophrys hovassei nov. gen., nov. sp. Morphologie, biologie et cytologie. Protistologica, 9, 503–520.Google Scholar
  24. Febvre-Chevalier, C. (1973b). Un nouveau type d’association des microtubules axopodiaux chez les héliozoaires. Protistologica, 9, 35–43.Google Scholar
  25. Febvre-Chevalier, C. (1975). Étude cytologique de Gymnosphaera albida, Sasski 1894, (Héliozoaire Centrohélidié). Protistologica, 11, 331–344.Google Scholar
  26. Febvre-Chevalier, C. (1981). Preliminary study of the motility processes in the stalked heliozoan Actinocoryne contractilis. Biosystems, 14, 337–343.CrossRefPubMedGoogle Scholar
  27. Febvre-Chevalier, C. (1982). Revision of the taxonomy of the heliozoans with attention to electron microscopical criteria. Annales de l’Institut Océanographique de Paris, 58(S), 173–178.Google Scholar
  28. Febvre-Chevalier, C. (1985). Class Heliozoea Haeckel. In J. J. Lee, S. H. Hunter, & E. C. Bovee (Eds.), An illustrated guide to the protozoa (pp. 302–338). Kansas: Society of Protozoologists.Google Scholar
  29. Febvre-Chevalier, C. (1990). Phylum Actinopoda: Class Heliozoa. In L. Margulis, J. O. Corliss, M. Melkonian, & D. Chapman (Eds.), Handbook of protoctista (pp. 347–362). Boston: Jones & Bartlett.Google Scholar
  30. Febvre-Chevalier, C., & Febvre, J. (1980). Cytophysiologie de la motilité chez un héliozoaire pédonculé. Paris: Film SFRS.Google Scholar
  31. Febvre-Chevalier, C., & Febvre, J. (1984). Axonemal microtubules in Cienkowskya mereschkovskyi and a revision of heliozoan taxonomy. Origins of Life, 13, 315–338.CrossRefGoogle Scholar
  32. Febvre-Chevalier, C., Febvre, J., Bilbaut, A., Bone, Q. (1983, June). The ionic basis of the electrical activity associated with contraction in Actinocoryne contractilis Febv-Chev., (Heliozoa). Comparison with electrophysiological data from other protista. 5th International Meeting of the Society for Evolutionary Protistology, Banyuls-sur-Mer.Google Scholar
  33. Febvre-Chevalier, C., Bilbaut, A., Bone, Q., & Febvre, J. (1986). Sodium-calcium action potential associated with contraction in the heliozoan Actinocoryne contractilis. Journal of Experimental Biology, 122, 177–192.Google Scholar
  34. Haeckel, E. (1866). Generelle Morphologie der Organismen (Vol. 2, p. 462). Berlin: G. Reimer.CrossRefGoogle Scholar
  35. Hartmann, M. (1913). Rhizopoda. In G. Fischer (Ed.), Handwörterbuch der Naturwissenschaften (Vol. 8, pp. 422–446). Jena.Google Scholar
  36. Hausmann, K., & Patterson, D. J. (1982). Pseudopod formation and membrane production during prey capture by a heliozoan (feeding by Actinophrys II). Cell Motility, 2, 9–24.CrossRefGoogle Scholar
  37. Kakuta, S., & Suzaki, T. (2008). Ca(2+)- and glycoconjugates-dependent prey capture in the heliozoon Actinophrys sol. European Journal of Protistology, 44(3), 163–167.CrossRefPubMedGoogle Scholar
  38. Kühn, A. (1926). Morphologie der Tiere in Bildern. In Protozoen (Vol. 1, pp. 107–272). Berlin: Gebrüder Borntraeger.Google Scholar
  39. Leonov, M. M. (2010). Heliozoans (Heliozoa, Sarcodina, Protista) of fresh and marine waters of the European part of Russia: species composition, morphology, and distribution. Inland Water Biology, 3(4), 344–355.CrossRefGoogle Scholar
  40. Linnenbach, M., Hausmann, K., & Patterson, D. J. (1983). Ultrastructural study on the food vacuole cycle of a heliozoan (feeding by Actinophrys III). Protoplasma, 115, 43–51.CrossRefGoogle Scholar
  41. Little, M., Quinlan, R. A., Hoffman, E. J., & Luduena, R. F. (1983). Identification and characterization of axopodial tubulins from Echinosphaerium nucleofilum. European Journal of Cell Biology, 31, 5–61.Google Scholar
  42. Mignot, J. P. (1979). Etude ultrastructurale de la pédogamie chez Actinophrys sol (Héliozoaire). La division programique. Protistologica, 15, 387–406.Google Scholar
  43. Mikrjukov, K. A. (1996a). Revision of the genera and species composition of lower Centroheliozoa I. Family Heterophryidae Poche. Archiv für Protistenkunde, 147, 107–113.CrossRefGoogle Scholar
  44. Mikrjukov, K. A. (1996b). Revision of the genera and species composition of lower Centroheliozoa II. Family Raphidiophryidae n. fam. Archiv für Protistenkunde, 147, 205–212.CrossRefGoogle Scholar
  45. Mikrjukov, K. A. (1998). On the biology of the Heliozoa: The origin of radial forms in the benthic sarcodines. Russian Journal of Zoology, 2, 15–24.Google Scholar
  46. Mikrjukov, K. A. (1999). Taxonomic revision of scale-bearing Heliozoon-like amoebae (Pompholyxophryidae, Rotosphaerida). Acta Protozoologica, 38, 119–131.Google Scholar
  47. Mikrjukov, K. A. (2000a). Taxonomy and phylogeny of Heliozoa. I. The order Desmothoracida Hertwig et Lesser, 1874. Acta Protozoologica, 39, 81–97.Google Scholar
  48. Mikrjukov, K. A. (2000b). Taxonomy and phylogeny of Heliozoa. II. The order Dimorphida Siemensma, 1991 (Cercomondadea classis n.): Diversity and relatedness with Cercomonads. Acta Protozoologica, 39, 99–115.Google Scholar
  49. Mikrjukov, K. A., & Patterson, D. J. (2001). Taxonomy and phylogeny of Heliozoa. III. Actinophryids. Acta Protozoologica, 40, 2–25.Google Scholar
  50. Mikrjukov, K. A., Siemensma, F. J., & Patterson, D. J. (2000). Phylum Heliozoa. In J. J. Lee, G. F. Leedale, & P. Bradbury (Eds.), The illustrated guide to protozoa (2nd ed., pp. 860–871). Lawrence: Society of Protozoologists.Google Scholar
  51. Nikolaev, S. I., Berney, C., Fahrni, J. F., Bolivar, I., Polet, s., Mylnikov, A. P., Aleshin, V. V., Petrov, N. B., & Pawlowski, J. (2004). The twilight of Heliozoa and the rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proceedings of the National Academy of Sciences, 101, 8066–8071.CrossRefGoogle Scholar
  52. Ockleford, C. D., & Tucker, J. B. (1973). Growth, breakdown, repair and rapid contraction of microtubular azopodia in the heliozoa Actinophrys sol Ehrenberg, 1830. Microbios, 26, 165–208.Google Scholar
  53. Packroff, G. (2000). Protozooplankton in acidic mining lakes with special respect to ciliates. Hydrobiologia, 433, 157–166.CrossRefGoogle Scholar
  54. Patterson, D. J., & Dürrschmidt, M. (1987). Selective retention of chloroplasts by algivorous Heliozoa: Fortuitous chloroplast symbiosis? European Journal of Protistology, 23, 51–55.CrossRefPubMedGoogle Scholar
  55. Patterson, D. J., & Hausmann, K. (1981). Feeding by Actinophrys sol (Protista Heliozoa): 1. Light microscopy. Microbios, 31, 39–55.PubMedGoogle Scholar
  56. Penard, E. (1904). Les Héliozoaires d’eau douce (pp. 1–341). Genève: Henry Kündig.CrossRefGoogle Scholar
  57. Pickett-Heaps, J. D. (1969). The evolution of the mitotic apparatus. An attempt at comparative ultrastructural cytology in dividing plant cells. Cytobios, 1, 257–280.Google Scholar
  58. Pierce, R. W., & Coats, D. W. (1999). The feeding ecology of Actinophrys sol (Sarcodina:Heliozoa) in Chesapeake Bay. Journal of Eukaryotic Microbiology, 46(5), 451–457.CrossRefGoogle Scholar
  59. Rainer, H. (1968). Heliozoa. In F. Dahl (Ed.), Die Tierwelt Deutschlands (Vol. 56, pp. 3–174). Jena: Fischer.Google Scholar
  60. Roth, L. E., & Shigenaka, Y. (1970). Microtubules in the heliozoan axopodium. II. Rapid degradation by cupric and nickelous ions. Journal of Ultrastructure Research, 31, 356–374.CrossRefPubMedGoogle Scholar
  61. Roth, L. E., Philaja, D. J., & Shigenka, Y. (1970). Microtubules in the heliozoan axopodium. I. The gardion hypthesis of allosterism in structural proteins. Journal of Ultrastructure Research, 39, 7–37.CrossRefGoogle Scholar
  62. Sakaguchi, M., Hausmann, K., & Suzaki, T. (1998). Food capture and adhesion by the heliozoon Actinophrys sol. Protoplasma, 203(3–4), 130–137.CrossRefGoogle Scholar
  63. Smith, R., & Patterson, D. J. (1986). Analysis of heliozoan interrelationships: An example of the potentials and limitations of ultrastructural approaches to the study of protistan phylogeny. Proceedings of the Royal Society of London B, 227, 325–366.CrossRefGoogle Scholar
  64. Suzaki, T., Shigenaka, Y., Watanabe, S., & Toyohara, A. (1980). Food capture and ingestion in the large heliozoan Echinosphaerium nucleofilum. Journal of Cell Science, 42, 61–79.PubMedGoogle Scholar
  65. Tilney, L. G. (1971). How microtubule patterns are generated. The relative importance of nucleation and bridging of microtubules in the formation of the axoneme of Raphidiophrys. Journal of Cell Biology, 51, 837–854.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Tilney, L. G., & Byers, B. (1969). Studies on the microtubules in heliozoa. V. Factors controlling the organization of microtubules in the axonemal pattern in Echinosphaerium (Actinosphaerium) nucleofilum. Journal of Cell Biology, 43, 148–165.CrossRefPubMedPubMedCentralGoogle Scholar
  67. Tilney, L. G., & Porter, K. (1965). Studies on microtubules in heliozoa. I. Fine structure of Actinosphaerium with particular reference to axial rod structure. Protoplasma, 60, 317–344.CrossRefPubMedGoogle Scholar
  68. Tregouboff, G. (1953). Classe des Héliozoaires. In P. P. Grassé (Ed.), Traité de Zoologie I (pp. 437–489). Paris: Masson et Cie.Google Scholar
  69. Valkanov, A. (1940). Die Helizoen und Proteomyxien. Artbestand und sonstige kritische Bemerkungen. Archiv für Protistenkunde, 93, 225–254.Google Scholar
  70. Villeneuve, F. (1937). Sur la structure de Cienkowskya mereschkovskyi et d’Actinolophus pedunculatus, héliozoaires des eaux saumâtres de Sète. Achives de Zoologie Expérimentale et Générale, 78, 243–250.Google Scholar
  71. Yabuki, A., Chao, E. E., Ishida, K.-I., & Cavalier-Smith, T. (2012). Microheliella maris (Microhelida ord. n.), and untrastructurally highly distinctive new axopodial protest species and genuse, and the unity of phylum Heliozoa. Protist, 163, 356–388.CrossRefPubMedGoogle Scholar
  72. Zuelzer, M. (1909). Bau und Entwicklung von Wagnerella borealis Mereschk. Archiv für Protistenkunde, 17, 135–202.Google Scholar

Copyright information

© Springer International Publishing AG 2016

Authors and Affiliations

  1. 1.Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA

Personalised recommendations