Cited by 78Marine Sponges and Natural ProductsMarine Invertebrate Physiology and EcologyPaleontology and Evolutionary Biology

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The unique skeleton of siliceous sponges (Porifera; Hexactinellida and Demospongiae) that evolved first from the Urmetazoa during the Proterozoic: a review

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Müller, W. E. G., Jinhe Li, Schröder, H. C., Li Qiao, Xiaohong Wang·2007·Biogeosciences

Published version of a preprint

Abstract

Abstract. Sponges (phylum Porifera) had been considered as an enigmatic phylum, prior to the analysis of their genetic repertoire/tool kit. Already with the isolation of the first adhesion molecule, galectin, it became clear that the sequences of sponge cell surface receptors and of molecules forming the intracellular signal transduction pathways triggered by them, share high similarity with those identified in other metazoan phyla. These studies demonstrated that all metazoan phyla, including Porifera, originate from one common ancestor, the Urmetazoa. The sponges evolved prior to the Ediacaran-Cambrian boundary (542 million years ago [myr]) during two major "snowball earth events", the Sturtian glaciation (710 to 680 myr) and the Varanger-Marinoan ice ages (605 to 585 myr). During this period the ocean was richer in silica due to the silicate weathering. The oldest sponge fossils (Hexactinellida) have been described from Australia, China and Mongolia and are thought to have existed coeval with the diverse Ediacara fauna. Only little younger are the fossils discovered in the Sansha section in Hunan (Early Cambrian; China). It has been proposed that only the sponges possessed the genetic repertoire to cope with the adverse conditions, e.g. temperature-protection molecules or proteins protecting them against ultraviolet radiation. The skeletal elements of the Hexactinellida (model organisms Monorhaphis chuni and Monorhaphis intermedia or Hyalonema sieboldi) and Demospongiae (models Suberites domuncula and Geodia cydonium), the spicules, are formed enzymatically by the anabolic enzyme silicatein and the catabolic enzyme silicase. Both, the spicules of Hexactinellida and of Demospongiae, comprise a central axial canal and an axial filament which harbors the silicatein. After intracellular formation of the first lamella around the channel and the subsequent extracellular apposition of further lamellae the spicules are completed in a net formed of collagen fibers. The data summarized here substantiate that with the finding of silicatein a new aera in the field of bio/inorganic chemistry started. For the first time strategies could be formulated and experimentally proven that allow the formation/synthesis of inorganic structures by organic molecules. These findings are not only of importance for the further understanding of basic pathways in the body plan formation of sponges but also of eminent importance for applied/commercial processes in a sustainable use of biomolecules for novel bio/inorganic materials.

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  1. Aizenberg, J., Weaver, J. C., Thanawala, M. S., Sundar, V. C., Morse, D. E., and Fratzel, P.: Skeleton von \\textitEuplectella sp.: structural hierarchy from nanoscale to the macroscale, Science, 309, 275–278, 2005. · DOI
  2. Brasier, M., Green, O., and Shields, G.: Ediacarian sponge spicule clusters from southwest Mongolia and the origins of the Cambrian fauna, Geology, 25, 303–306, 1997. · DOI
  3. Butterfield, N. J.: Macroevolution and macroecology trough deep time, Palaeontology, 50, 41–55, 2007. · DOI · Paper page
  4. Carlisle, E. M.: Silicon as an essential trace element in animal nutrition, Ciba Foundation Symposium 121, John Wiley, Chichester, 123–136, 1986. · DOI
  5. Cha, J. N., Shimizu, K., Zhou, Y., Christianssen, S. C., Chmelka, B. F., Stucky, G .D., and Morse D. E.: Silicatein filaments and subunits from a marine sponge direct the polymerization of silica and silicones \\textitin vitro, Proc. Natl. Acad. Sci. USA, 96, 361–365, 1999. · DOI
  6. Cifelli, R.: Radiation of Cenozoic planktonic Foraminifera, Syst. Zool., 18, 154–168, 1969. · DOI
  7. Eckert, C., Schröder, H. C., Brandt, D., Perovic-Ottstadt, S., and Müller, W. E. G.: A histochemical and electron microscopic analysis of the spiculogenesis in the demosponge \\textitSuberites domuncula, J. Histochem. Cytochem., 54, 1031–1040, 2006. · DOI
  8. Efremova, S. M., Margulis, B. A., Guzhova, I. V., Itskovich, V. B., Lauenroth, S., Müller, W. E. G., and Schröder, H. C.: Heat shock protein Hsp70 expression and DNA damage in Baikalian sponges exposed to model pollutants and wastewater from Baikalsk Pulp and paper plant, Aquat. Toxicol., 57, 267–280, 2002. · DOI
  9. Ehrlich, H., Hanke, T., Simon, P., Goebel, C., Heinmann, S., Born, R., and Worch, H.: Demineralisation von natürlichen Silikat-basierten Biomaterialien: neue Strategie zur Isolation organischer Gerüststrukturen, BIOmaterialien, 6, 297–302, 2005. · DOI
  10. Garrone, R.: Evolution of metazoan collagens, Progr. Molec. Subcell. Biol., 21, 191–139, 1998. · DOI
  11. Haeckel, E.: Kunstformen der Natur, Bibliographisches Institut, Leipzig, 1899. · DOI
  12. Hayes, J. M.: Global methanotrophy at the Archean-Proterozoic transition, in: Early Life on Earth, edited by Bengtson, S., Columbia University Press, New York, 220–236, 1994.
  13. Hoffmann, P. A. and Schrag, D. P.: The snowball Earth hypothesis: testing the limits of global change, Terra Nova, 129–155, 2002. · DOI · Paper page
  14. Krasko, A., Müller, I. M., and Müller, W. E. G.: Evolutionary relationships of the metazoan \\textitß$\\gamma $-crystallins, including the one from the marine sponge \\textitGeodia cydonium, Proc. Royal Soci. Lond. B, 264, 1077–1084, 1997. · DOI
  15. Krasko, A., Schröder, H. C., Hassanein, H. M. A., Batel, R., Müller, I. M., and Müller, W. E. G.: Identification and expression of the SOS-response, \\textitaidB-like, gene in the marine sponge \\textitGeodia cydonium: implication for the phylogenetic relationships of metazoan Acyl-CoA dehydrogenases and Acyl-CoA oxidases, J. Molec. Evol., 47, 343–352, 1998. · DOI
  16. Krasko, A., Lorenz, B., Batel, R., Schröder, H. C., Müller, I. M., and Müller, W. E. G.: Expression of silicatein and collagen genes in the marine sponge \\textitSuberites domuncula is controlled by silicate and myotrophin, Europ. J. Biochem., 267, 4878–4887, 2000. · DOI
  17. Krasko, A., Schröder, H. C., Batel, R., Grebenjuk, V. A., Steffen, R., Müller, I. M., and Müller, W. E. G.: Iron induces proliferation and morphogenesis in primmorphs from the marine sponge \\textitSuberites domuncula, DNA & Cell Biol., 21, 67–80, 2002. · DOI
  18. Krasko, A., Gundacker, D., Leys, S. P., Schröder, H. C., Müller, I. M., and Müller, W. E. G.: Molecular and functional analysis of the (6-4) photolyase from the hexactinellid \\textitAphrocallistes vastus, Biochim. Biophys. Acta., 1651, 41–49, 2003. · DOI
  19. Li, C. W., Chen, J. Y., and Hua T. E.: Precambrian sponges with cellular structures, Science, 279, 879–882 1998. · DOI · Paper page
  20. Morris, C. S.: Why molecular biology needs palaeontology, Develop. Suppl., 1–13, 1994. · DOI
  21. Müller, W. E. G.: Origin of Metazoa: sponges as living fossils, Naturwiss., 85, 11–25, 1998. · DOI
  22. Müller, W. E. G.: Spatial and temporal expression patterns in animals, in: Encyclopedia of Molecular Cell Biology and Molecular Medicine, edited by: Meyers, R. A., WILEY-VCH Press, Weinheim, 13, 269–309, 2005.
  23. Müller, W. E. G.: The stem cell concept in sponges (Porifera): metazoan traits, Seminars in Cell & Develop. Biol., 17, 481–491, 2006. · DOI
  24. Müller, W. E. G. and Müller, I. M.: Origin of the metazoan immune system: Identification of the molecules and their functions in sponges, Integr. Comp. Biol., 43, 281–292, 2003. · DOI
  25. Müller, W. E. G., Schröder, H. C., Skorokhod, A., Bünz, C., Müller, I. M., and Grebenjuk, V. A.: Contribution of sponge genes to unravel the genome of the hypothetical ancestor of metazoa (Urmetazoa), Gene, 276, 161–173, 2001. · DOI
  26. Müller, W. E. G., Krasko, A., Le Pennec, G., Steffen, R., Ammar, M. S. A., Wiens, M., Müller, I. M., and Schröder, H. C.: Molecular mechanism of spicule formation in the demosponge \\textitSuberites domuncula: Silicatein – collagen – myotrophin, Progress Molec. Subcell. Biol., 33, 195–221, 2003. · DOI
  27. Müller, W. E. G., Wiens, M., Adell, T., Gamulin, V., Schröder, H. C., and Müller, I. M.: The Bauplan of the Urmetazoa: The basis of the genetic complexity of Metazoa using the siliceous sponges [Porifera] as living fossils, Int. Rev. Cytol., 235, 53–92, 2004a. · DOI
  28. Müller, W. E. G., Grebenjuk, V. A., Thakur, N. L., Thakur, A. N., Batel, R., Krasko, A., Müller, I. M., and Breter, H. J.: Oxygen-controlled bacterial growth in the sponge \\textitSuberites domuncula: Towards a molecular understanding of the symbiotic relationships between sponge and bacteria, Appl. Envir. Microbiol., 70, 2332–2341, 2004b. · DOI
  29. Müller, W. E. G., Rothenberger, M., Boreiko, A., Tremel, W., Reiber, A., and Schröder, H. C.: Formation of siliceous spicules in the marine demosponge \\textitSuberites domuncula, Cell & Tissue Res., 321, 285–297, 2005. · DOI
  30. Müller, W. E. G., Belikov, S. I., Tremel, W., Perry, C. C., Gieskes, W. W. C., Boreiko, A., and Schröder, H. C.: Siliceous spicules in marine demosponges (example \\textitSuberites domuncula), Micron., 37, 107–120, 2006a. · DOI
  31. Müller, W. E. G., Kaluzhnaya, O. V., Belikov, S. I., Rothenberger, M., Schröder, H. C., Reiber, A., Kaandorp, J. A., Manz, B., Mietchen, D., and Volke, F.: Magnetic resonance imaging of the siliceous skeleton of the demosponge \\textitLubomirskia baicalensis, J. Struct. Biol., 153, 31–41, 2006b. · DOI
  32. Müller, W. E. G., Wendt, K., Geppert, C., Wiens, M., Reiber, A., and Schröder, H. C.: Novel photoreception system in sponges? Unique transmission properties of the stalk spicules from the hexactinellid \\textitHyalonema sieboldi, Biosensors and Bioelectronics, 21, 1149–1155, 2006c. · DOI
  33. Müller, W. E. G., Schröder, H. C., Wrede, P., Kaluzhnaya, O. V., and Belikov, S. I.: Speciation of sponges in Baikal-Tuva region (an outline), J. Zool. Syst. Evol. Res., 44, 105–117, 2006d. · DOI
  34. Müller, W. E. G., Eckert, C., Kropf, K., Wang, X., Schloßmacher, U., Seckert, C., Wolf, S. E., Tremel, W., and Schröder, H. C.: Formation of the giant spicules of the deep sea hexactinellid \\textitMonorhaphis chuni (Schulze 1904): electron microscopic and biochemical studies, Cell & Tissue Res., https://doi.org/10.1007/s00441-007-0402-x, 2007. · DOI
  35. Nichols, S. A., Dirks, W., Pearse, J. S., and King, N.: Early evolution of animal cell signaling and adhesion genes. Proc. Natl. Acad. Sci. USA, 103, 12 451–12 456, 2006. · DOI
  36. Pancer, Z., Kruse, M., Müller, I., and Müller, W. E. G.: On the origin of adhesion receptors of metazoa: cloning of the integrin $\\alpha $ subunit cDNA from the sponge \\textitGeodia cydonium, Molec. Biol. Evol., 14, 391–398, 1997. · DOI
  37. Perovi\\'c-Ottstadt, S., Adell, T., Proksch, P., Wiens, M., Korzhev, M., Gamulin, V., Müller, I. M., and Müller, W. E. G.: A (1$\\to$3)-β-d-glucan recognition protein from the sponge \\textitSuberites domuncula: mediated activation of fibrinogen-like protein and epidermal growth factor gene expression, Eur. J. Biochem., 271, 1924–1937, 2004a. · DOI
  38. Pechenik, J. A.: Biology of the Invertebrates, McGraw Hill, Boston, 2000.
  39. Pilcher, H.: Back to our roots, Nature, 435, 1022–1023, 2005. · DOI
  40. Pfeifer, K., Haasemann, M., Gamulin, V., Bretting, H., Fahrenholz, F., and Müller, W. E. G.: S-type lectins occur also in invertebrates: high conservation of the carbohydrate recognition domain in the lectin genes from the marine sponge \\textitGeodia cydonium, Glycobiol., 3, 179–184, 1993. · DOI
  41. Pilcher, H.: Back to our roots, Nature, 435, 1022–1023, 2005. · DOI
  42. Reitner, J. and Wörheide, G.: Non-Lithistid fossil Demospongiae – Origins of their Palaeobiodiversity and Highlights in History of Preservation, in: Systema Porifera: A Guide to the Classification of Sponges, edited by: Hooper, J. N. A. and Van Soest, R., Kluwer, New York, pp 52–68, 2002. · DOI · Paper page
  43. Retallack, G. J.: Were the Ediacaran fossils lichens?, Paleobiology, 20, 523–544, 1994. · DOI
  44. Rigby, J. K. and Hou, Xian-Guang.: Lower Cambrian demosponges and hexactinellid sponges from Yunnan, \\textitChina, J. Paleont., 69, 1009–1019, 1995. · DOI
  45. Sanford, F.: Physical and chemical analysis of the siliceous skeleton in six sponges of two groups (Demospongiae and Hexactinellida), Micr. Res. Techn., 62, 336–355, 2003. · DOI
  46. Schröder, H. C., Krasko, A., Ushijima, H., Gamulin, V., Schütze, J., Müller, I. M., and Müller, W. E. G.: Emergence and disappearance of an immune molecule, an antimicrobial lectin, in basal Metazoa: the tachylectin family, J. Biol. Chem., 278, 32 810–32 817, 2003a. · DOI
  47. Schröder, H. C., Krasko, A., Le Pennec, G., Adell, T., Wiens, M., Hassanein, H., Müller, I. M., and Müller, W. E. G.: Silicase, an enzyme which degrades biogenous amorphous silica: Contribution to the metabolism of silica deposition in the demosponge \\textitSuberites domuncula, Prog. Mol. Subcell. Biol., 33, 250–268, 2003b. · DOI
  48. Schröder, H. C., Perovi\\'c-Ottstadt, S., Rothenberger, M., Wiens, M., Schwertner, H., Batel, R., Korzhev, M., Müller, I. M., and Müller, W. E. G.: Silica transport in the demosponge \\textitSuberites domuncula: fluorescence emission analysis using the PDMPO probe and cloning of a potential transporter, Biochem. J., 381, 665==673, 2004a. · DOI
  49. Schröder, H. C., Perovi-Ottstadt, S., Wiens, M., Batel, R., Müller, I. M., and Müller, W. E. G.: Differentiation capacity of the epithelial cells in the sponge \\textitSuberites domuncula, Cell & Tissue Res., 316, 271–280, 2004b. · DOI
  50. Schröder, H. C., Boreiko, A., Korzhev, M., Tahir, M. N., Tremel, W., Eckert, C., Ushijima, H., Müller, I. M., and Müller, W. E. G.: Co-Expression and functional interaction of silicatein with galectin: matrix-guided formation of siliceous spicules in the marine demosponge \\textitSuberites domuncula, J. Biol. Chem., 281, 12 001–12 009, 2006. · DOI
  51. Schröder, H. C., Brandt, D., Schloßmacher, U., Wang, X., Tahir, M. N., Tremel, W., Belikov, S. I., and Müller, W. E. G., Enzymatic production of biosilica-glass using enzymes from sponges: Basic aspects and application in nanobiotechnology (material sciences and medicine), Naturwissenschaften, 94, 339–359, 2007. · DOI
  52. Seilacher, A.: Vendozoa: Organismic construction in the proterozoic biosphere, Lethaia, 22, 229–239, 1989. · DOI · Paper page
  53. Shimizu, K., Cha, J., Stucky, G. D., and Morse, D. E.: Silicatein alpha: cathepsin L-like protein in sponge biosilica, Proc. Natl. Acad. Sci. USA, 95, 6234–6238, 1998. · DOI
  54. Sly, W. S. and Hu, P. Y.: Human carbonic anhydrases and carbonic anhydrase deficiencies, Annu. Rev. Biochem., 64, 375–401, 1995. · DOI
  55. Thakur, N. L., Perovi-Ottstadt, S., Batel, R., Korzhev, M., Diehl-Seifert, B., Müller, I. M., and Müller, W. E. G.: Innate immune defense of the sponge \\textitSuberites domuncula against gram-positive bacteria: induction of lysozyme and AdaPTin, Mar. Biol., 146, 271–282, 2005. · DOI
  56. Towe, K. M.: Environmental conditions surrounding the origin and early evolution of life, Precambrian Res., 16, 10010, 1981. · DOI
  57. Towe, K. M.: Oxygen-collagen priortiy and the metzoan fossil record, Proc. Natl. Acad. Sci. USA, 65, 78100788, 1970. · DOI · Paper page
  58. Uriz, M. J., Turon, X., and Becerro, M. A.: Silica deposition in Demospongiae: spiculogenesis in \\textitCrambe crambe, Cell & Tissue Res., 301, 299–309, 2000. · DOI
  59. Uriz, M. J., Turon, X., and Beccero, M. A.: Silica deposition in demosponges, Progr. Molec. Subcell. Biol., 33, 163–193, 2003. · DOI
  60. Uriz, M. J.: Mineral skeletogenesis in sponges, Canadian J. Zool., 84, 322–356, 2006. · DOI
  61. Wang, X., Li, J., Qiao, L., Schröder, H. C., Eckert, C., Kropf, K., and Müller, W. E. G.: The giant spicules of the deep sea hexactinellidan sponges of the genus \\textitMonorhaphis (Hexactinellida: Amphidiscosida: Monorhaphididae), Acta Zoologica Sinica, in press, 2007.
  62. Wiens, M. and Müller, W. E. G.: Cell death in Porifera: molecular players in the game of apoptotic cell death in living fossils, Can. J. Zool./Rev. Can. Zool., 84, 307–321, 2006. · DOI
  63. Wiens, M., Mangoni, A., D'Esposito, M., Fattorusso, E., Korchagina, N., Schröder, H. C., Grebenjuk, V. A., Krasko, A., Batel, R., Müller, I. M., and Müller, W. E. G.: The molecular basis for the evolution of the metazoan bodyplan: extracellular matrix-mediated morphogenesis in marine demosponges, J. Mol. Evol., 57, 1–16, 2003. · DOI
  64. Wiens, M., Perovi-Ottstadt, S., Müller, I. M., and Müller, W. E. G.: Allograft rejection in the mixed cell reaction system of the demosponge \\textitSuberites \\textitdomuncula is controlled by differential expression of apoptotic genes, Immunogenetics, 56, 597–610, 2004. · DOI
  65. Wiens, M., Korzhev, M., Krasko, A., Thakur, N. L., Perović-Ottstadt, S., Breter, H. J., Ushijima, H., Diehl-Seifert, B., Müller, I. M., and Müller, W. E. G.: Innate immune defense of the sponge \\textitSuberites domuncula against bacteria involves a MyD88-dependent signaling pathway: induction of a perforin-like molecule, J. Biol. Chem., 280, 27 949–27 959, 2005. · DOI
  66. Wiens, M., Belikov, S. I., Kaluzhnaya, O. V., Krasko, A., Schröder, H. C., Perovic-Ottstadt, S., and Müller, W. E. G.: Molecular control of serial module formation along the apical-basal axis in the sponge \\textitLubomirskia baicalensis: silicateins, mannose-binding lectin and Mago Nashi, Develop. Genes Evol., 216, 229–242, 2006. · DOI
  67. Wöhler, F.: Ueber künstliche Bildung des Harnstoffs, Annalen der Physik und Chemie, 12, 253–256, 1828. · DOI

Metadata

Authors
Müller, W. E. G., Li, J., Schröder, H. C., Qiao, L., & Wang, X.
Affiliations
  • Johannes Gutenberg University Mainz (DE)
  • Tsinghua University (CN)
Venue
Biogeosciences
Published
2007-05-03
Volume
4
Issue
2
Pages
219-232
ISSN
  • 1726-4170 (ISSN-L)
  • 1726-4189
OpenAlex
W2164879214
Cited by
78
References
80
Citations by year
2025: 2 · 2024: 1 · 2023: 3 · 2021: 3 · 2020: 2 · 2019: 5 · 2018: 3 · 2017: 2 · 2016: 5 · 2015: 5 · 2014: 8 · 2013: 8 · 2012: 4
FWCI
5.34
Type
journal article
Language
en
Open access
Locations
  • Biogeosciences (publishedVersion, cc-by)
  • HAL (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • European Commission
  • Deutsche Forschungsgemeinschaft
  • National Natural Science Foundation of China
  • Bundesministerium für Bildung und Forschung
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Marine Sponges and Natural Products
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Evolutionary Biology
Keywords
sponges, Hexactinellida, Demospongiae, sponge skeleton, spicules, silicatein, silica biomineralization, metazoan origin, Proterozoic, Sturtian glaciation, Marinoan glaciation, Ediacaran, galectins

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Müller, W. E. G., Li, J., Schröder, H. C., Qiao, L., & Wang, X. (2007). The unique skeleton of siliceous sponges (Porifera; Hexactinellida and Demospongiae) that evolved first from the Urmetazoa during the Proterozoic: a review. Biogeosciences. https://doi.org/10.5194/bg-4-219-2007