Marine Biology

, Volume 150, Issue 2, pp 313–319 | Cite as

Glycohistochemistry of a marine sponge, Chondrilla nucula (Porifera, Desmospongiae), with remarks on a possibly related antimicrobial defense strategy and a note on exopinacoderm function

  • W. MeyerEmail author
  • M. Sidri
  • F. Brümmer
Research Article


Based on carbohydrate histochemistry, including the use of lectins, and TEM, the study describes the distribution of terminal sugars in different structures of the demosponge Chondrilla nucula. The results of the general and specific carbohydrate histochemical approaches confirmed the presence of acidic and neutral glycoconjugates in the cells, and, with declining amounts from the ectosome to the mesohyl, in the extracellular matrix (ECM). AB-PAS staining indicated acidic complex carbohydrates particularly in the exopinacoderm, and more neutral ones in the cells and the ECM of the mesohyl. The PO-lectins applied demonstrated a general spectrum of free saccharide residues (α-d-mannose, α-/β-d-N-acetylglucosamine, α-d-N-acetylgalactosamine, α-d-galactose, β-d-galactose) in both sponge parts; α-l-fucose was only distinct in the ectosome. Sialic acids [siaα(2,3)-galactose, siaα(2,6)-N-acetylgalactosamine] were dominant in the very thin exopinacoderm, indicating O-linked high molecular weight glycoproteins. In this way a glycophysiologically ‘rigid’ outer mucus cover is developed as protection against mechanical hazards. Some of the free sugars (α-d-mannose, N-acetylglucosamine, N-acetylgalactosamine β-d-galactose, α-l-fucose) are known to prevent the adherence of different bacteria and fungi to cellular surfaces. Thus a high concentration of such sugars, may impede massive attacks of micro-inhabitants on mobile sponge cells, pinacocytes, and the exopinacoderm layer.


Sponge Sialic Acid Wheat Germ Agglutinin Free Sugar Dolichos Biflorus Agglutinin 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The skillfull technical assistance of M. Gähle and K. Rohn, and the help of Dr. A. Schnapper is gratefully acknowledged. Part of this work (MS, FB) was supported by the Federal Ministry of Education and Research, the University of Stuttgart and the Ministry of Science, Research and Arts of the State of Baden-Württemberg through the excellence center BIOTECmarin (03F0345D).


  1. Allison RT (1987) The effects of various fixatives on subsequent lectin binding to tissue sections. Histochem J 19:65–74CrossRefGoogle Scholar
  2. Alroy J, Ucci AA, Pereira MEA (1988) Lectin histochemistry: an update. In: DeLellis RA (ed) Advances in immunohistochemistry (neoplasms diagnosis). Raven Press, New York, pp 93–131Google Scholar
  3. Austin B (2002) The bacterial flora of fish. Sci World J 2:558–572CrossRefGoogle Scholar
  4. Baum C, Meyer W, Stelzer R, Fleischer L-G, Siebers D (2002) Average nanorough skin surface of the pilot whale (Globicephala melas, Delphinidae): considerations on the self-cleaning abilities based on nanoroughness. Mar Biol 140:653–657CrossRefGoogle Scholar
  5. Bond C, Harris A (1988) Locomotion of sponges and its physical mechanism. J Exp Zool 246:271–284CrossRefGoogle Scholar
  6. Boury-Esnault N (2002) Order Chondrosida Boury-Esnault & Lopés, 1985. Family Chondrillidae Gray, 1872. In: Hooper JNA, Van Soest RWM (eds) Systema Porifera: a guide to the classification of sponges. Kulwer/Plenum, New York, pp 291–297CrossRefGoogle Scholar
  7. Bretting H, Königsmann K (1979) Investigations on the lectin-producing cells in the sponge Axinella polypoides (Schmidt). Cell Tiss Res 201:487–497CrossRefGoogle Scholar
  8. Brümmer F, Calcinai B, Götz M, Leitermann F, Nickel M, Sidri M, Zucht W (2004) Overview on the sponge fauna of the Limski kanal, Croatia, Northern Adriatic Sea. Boll Mus Ist Biol Univ Genova 68:219–227Google Scholar
  9. Campbell BJ (1999) Biochemical and functional aspects of mucus and mucin-type glycoproteins. In: Mathiowitz E, Chickering DE, Lehr CM (eds) Bioadhesive drug delivery systems, drugs and the pharmaceutical sciences, vol 98. Marcel Dekker, New York, pp 85–130Google Scholar
  10. Carballo JL, Gómez P, Cruz-Barraza JA, Flores-Sánchez DM (2003) Sponges of the family Chondrillidae (Porifera: Demospongiae) from the Pacific coast of Mexico, with the description of three new species. Proc Biol Soc Wash 116:515–527Google Scholar
  11. Critchley IA, Douglas LJ (1987) Role of glycosides as epithelial cell receptors for Candida albicans. J Gen Microbiol 133:637–643PubMedGoogle Scholar
  12. Danguy A, Decaestecker C, Genten F, Salmon I, Kiss R (1998) Application of lectins and neoglycoconjugates in histology and pathology. Acta Anat 161:206–218CrossRefGoogle Scholar
  13. Daunter B, Forbes KL, Sanderson BM, Morrison J, Wright G (1992) Inhibition of binding of bacteria to amniochorionic membranes by amniotic fluid. Eur J Obstet Gynecol Reprod Biol 47:95–102CrossRefGoogle Scholar
  14. De Vos L, Rützler K, Boury-Esnault N, Donadey C, Vacelet J (1991) Atlas de morphologie des eponges—Atlas of sponge morphology, vol 117. Smithsonian Inst Press, WashingtonGoogle Scholar
  15. Fairchild CD, Jones IK, Glazer AN (1991) Absence of glycosylation on cyanobacterial phycobilisome linker polypeptides and rhodophytan phycoerythrins. J Bacteriol 173:2985–2992CrossRefGoogle Scholar
  16. Faulkner DJ (2002) Marine natural products. Nat Prod Rep 19:1–48PubMedPubMedCentralGoogle Scholar
  17. Faulkner DJ, Unson MD, Bewley CA (1994) The chemistry of some sponges and their symbionts. Pure Appl Chem 66:1983–1990CrossRefGoogle Scholar
  18. Fernandez-Busquets X, Burger MM (2003) Circular proteoglycans from sponges: first members of the spongican family. Cell Mol Life Sci 60:88–112CrossRefGoogle Scholar
  19. Gaino E, Pronzato R (1983) Étude en microscopie électronique du filament des formes étirées chez Chondrilla nucula (Porifera, Demospongiae). Ann Sci Nat Zool 5:221–234Google Scholar
  20. Geyer G (1973) Ultrahistochemie. Histochemische Arbeitsvorschriften für die Elektronenmikroskopie, 2nd edn. G Fischer, StuttgartGoogle Scholar
  21. Hanstede JG, Gerrits PO (1983) The effects of embedding in water-soluble plastics on the final dimensions of liver sections. J Microsc 131:79–90CrossRefGoogle Scholar
  22. Hayat MA (1993) Stains and cytochemical methods. Plenum, New YorkGoogle Scholar
  23. Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J, Horn M (2003) Microbial diversity of marine sponges. Prog Mol Subcell Biol 37:59–88CrossRefGoogle Scholar
  24. Hoiczyk E (1998) Structural and biochemical analysis of the sheath of Phormidium uncinatum. J Bacteriol 180:3923–3932PubMedPubMedCentralGoogle Scholar
  25. Hoiczyk E, Baumeister W (1997) Oscillin, an extracellular, Ca2+-binding glycoprotein essential for the gliding motility of cyanobacteria. Mol Microbiol 26:699–708CrossRefGoogle Scholar
  26. Imhoff JF, Stöhr R (2003) Sponge-associated bacteria: a general overview and special aspects of bacteria associated with Halochondria panicea. Prog Mol Subcell Biol 37:35–57CrossRefGoogle Scholar
  27. Izhar M, Nuchamowitz Y, Mirelman D (1982) Adherence of Shigella flexneri to guinea pig intestinal cells is mediated by a mucosal adhesion. Infect Immun 35:1110–1118PubMedPubMedCentralGoogle Scholar
  28. James J, Tas J (1984) Histochemical protein staining methods (Microscopy handbooks 04). Oxford University Press, Royal Microsc Soc, OxfordGoogle Scholar
  29. Jarchow J, Fritz J, Anselmetti D, Calabro A, Hascall VC, Gerosa D, Burger MM, Fernandez-Busquets X (2000) Supramolecular structure of a new family of circular proteoglycans mediating cell adhesion in sponges. J Struct Biol 132:95–105CrossRefGoogle Scholar
  30. Keyzers RA, Davies-Coleman MT (2005) Anti-inflammatory metabolites from marine sponges. Chem Soc Rev 34:355–365CrossRefGoogle Scholar
  31. Klautau M, Russo CAM, Lazoski C, Boury-Esnault N, Torpe J, Solé-Cava A (1999) Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution 53:1414–1422CrossRefGoogle Scholar
  32. Lamblin G, Degroote S, Perini JM, Delmotte P, Scharfman A, Davril M, Lo-Guidice JM, Houdret N, Dumur V, Klein A, Roussel P (2001) Human airway mucin glycosylation: a combinatory of carbohydrate determinants which vary in cystic fibrosis. Glycoconj J 18:661–684CrossRefGoogle Scholar
  33. Luft JH (1961) Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol 9:409–414CrossRefGoogle Scholar
  34. Maldonado M, Cortadellas N, Trillas MI, Rützler K (2005) Endosymbiontic yeast maternally transmitted in a marine sponge. Biol Bull 209:94–106CrossRefGoogle Scholar
  35. McGavin MH, Krajewska-Pietrasik D, Ryden C, Hook M (1993) Identification of a Staphylococcus aureus extracellular matrix-binding protein with broad specificity. Infect Immun 61:2479–2485PubMedPubMedCentralGoogle Scholar
  36. Mercurio M, Scalera-Liaci L, Corriero G (2001) La fauna a poriferi del bacino della strea di Porto Cesareo (Le). Biol Mar Medit 8:403–412Google Scholar
  37. Meyer W, Seegers U (2004) A preliminary approach to epidermal antimicrobial defense in the Delphinidae. Mar Biol 244:841–844Google Scholar
  38. Meyer W, Bollhorn M, Stede M (2000) Aspects of antimicrobial properties of skin secretions in the Common seal (Phoca vitulina). Dis Aquat Org 41:77–79CrossRefGoogle Scholar
  39. Meyer W, Neurand K, Tanyolac A (2001) General antimicrobial properties of the integument in fleece producing sheep and goats. Small Rumin Res 41:181–190CrossRefGoogle Scholar
  40. Meyer W, Seegers U, Schnapper A (2003a) Free sugars as antimicrobial agents on the epidermal surface of aquatic vertebrates. 96 Jahresvers Dtsch Zool Ges (Berlin), Abstracts, 135Google Scholar
  41. Meyer W, Seegers U, Herrmann J, Schnapper A (2003b) Further aspects of general antimicrobial properties of skin secretions of pinnipeds. Dis Aquat Org 44:177–179CrossRefGoogle Scholar
  42. Millonig G (1981) Advantages of a phosphate buffer for OsO4 solutions in fixation. J Appl Phys 32:1637Google Scholar
  43. Müller WE, Müller IM (2003) Analysis of the sponge (Porifera) gene repertoire: implications for the evolution of the metazoan body plan. Prog Mol Subcell Biol 37:1–33CrossRefGoogle Scholar
  44. Müller WEG, Zahn RK, Kurelec B, Müller I (1984) A catalogue of the sponges near Rovinj. Thalassia Jugoslavica 20:13–23Google Scholar
  45. Novosel M, Bakran-Petricioli T, Požar-Domac A, Kružic P, Radic I (2002) The benthos of the Northern part of the Velebit channel (Adriatic Sea, Croatia). Nat Croat 11:387–409Google Scholar
  46. Ollert MW, Söhnchen R, Korting HC, Ollert U, Bräutigam S, Bräutigam W (1993) Mechanisms of adherence of Candida albicans to cultured human epidermal keratinocytes. Infect Immun 61:4560–4568PubMedPubMedCentralGoogle Scholar
  47. Passow U (2000) Formation of transparent exopolymer particles, TEP, from dissolved precursor material. Mar Ecol Prog Ser 192:1–11CrossRefGoogle Scholar
  48. Pearse AGE (1968) Histochemistry. Theoretical and applied, 3rd edn, vol 1. Preparative and optical technology. Churchill Livingstone, EdinburghGoogle Scholar
  49. Pearse AGE (1980) Histochemistry. Theoretical and applied, 4th edn, vol 1. Preparative and optical technology. Churchill Livingstone, EdinburghGoogle Scholar
  50. Pearse AGE (1985) Histochemistry. Theoretical and applied, 4th edn, vol 2. Analytical technology. Churchill Livingstone, EdinburghGoogle Scholar
  51. Proksch P, Ebel R, Edrada RA, Wray V, Steube K (2003) Bioactive natural products from marine invertebrates and associated fungi. Prog Mol Subcell Biol 37:117–142CrossRefGoogle Scholar
  52. Reynolds ES (1963) The use of lead citrate of high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–212CrossRefGoogle Scholar
  53. Richardson KC, Jarett L, Finke EH (1960) Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35:313–323CrossRefGoogle Scholar
  54. Rittman BR, Mackenzie IC (1983) Effects of histological processing on lectin binding patterns in oral mucosa and skin. Histochem J 15:467–474CrossRefGoogle Scholar
  55. Romero-Steiner S, Witek T, Balish E (1990) Adherence of skin bacteria to human epithelial cells. J Clin Microbiol 28:27–31PubMedPubMedCentralGoogle Scholar
  56. Rützler K (1965) Systematik und Ökologie der Poriferen aus Littoral-schattengebieten der Nordadria. Z Morph Ökol Tiere 55:1–82CrossRefGoogle Scholar
  57. Schauer R (2004) Sialic acids: fascinating sugars in higher animals and man. Zoology 107:49–64CrossRefGoogle Scholar
  58. Schmitz FJ, McDonald FJ (1974) Isolation and identification of cerebrosides from the marine sponge Chondrilla nucula. J Lipid Res 15:158–164PubMedGoogle Scholar
  59. Sciscioli M, Feri D, Liquori GE, Lepore E, Santarelli G (2000) Lectin histochemistry and ultrastructure of microgranular cells in Cinachyra tarentina (Porifera, Demospongiae). Acta Histochem 102:219–230CrossRefGoogle Scholar
  60. Sharon N, Eshdat Y, Silverblatt FJ, Ofek I (1981) Bacterial adherence to cell surface sugars. CIBA Found Symp 80:119–141PubMedGoogle Scholar
  61. Sidri M (2004) Chondrilla nucula (Porifera, Demospongie): an example of successful plasticity. Ecological and morphological aspects. Dissertation Thesis, University of Stuttgart, Germany, 226 ppGoogle Scholar
  62. Sionov E, Roth D, Sandovsky-Losica H, Kashman Y, Rudi A, Chill L, Berdicevsky I, Segal E (2005) Antifungal effect and possible mode of activity of a compound from the marine sponge Dysidea herbacea. J Infect 50:453–460CrossRefGoogle Scholar
  63. Sobel JD, Myers PG, Kaye D, Levison ME (1981) Adherence of Candida albicans to human vaginal and buccal epithelial cells. J infect Dis 143:1, 76–82CrossRefGoogle Scholar
  64. Spicer SS, Schulte BA (1992) Diversity of cell glycoconjugates shown histochemically: a perspective. J Histochem Cytochem 40:1–38CrossRefGoogle Scholar
  65. Stempak JG, Ward RT (1964) An improved staining method for electron microscopy. J Cell Biol 22:697–701CrossRefGoogle Scholar
  66. Usher KM, Toze S, Fromont J, Kuo J, Sutton DC (2004) A new species of cyanobacterial symbiont from the marine sponge Chondrilla nucula. Symbiosis 36:183–192Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Institute of AnatomyUniversity of Veterinary MedicineHannoverGermany
  2. 2.Porifarma BVEdeThe Netherlands
  3. 3.Department of ZoologyUniversity of StuttgartStuttgartGermany

Personalised recommendations