Advertisement

Microbial Diversity of Marine Sponges

  • U. Hentschel
  • L. Fieseler
  • M. Wehrl
  • C. Gernert
  • M. Steinert
  • J. Hacker
  • M. Horn
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 37)

Abstract

The recent application of molecular microbial ecology tools to sponge-microbe associations has revealed a glimpse into the biodiversity of these microbial communities, that is considered just ‘the tip of the iceberg’. This chapter provides an overview over these new findings with regard to identity, diversity and distribution patterns of sponge-associated microbial consortia. The sponges Aplysina aerophoba (Verongida), Rhopaloeides odorabile (Dicytoceratida) and Theonella swinhoei (Lithistida) were chosen as model systems for this review because they have been subject to both, cultivation-dependent and cultivation-independent approaches. A discussion of the microbial assemblages of Halichondria panicea is presented in the accompanying chapter by Imhoff and Stöhr. Considering that a large fraction of sponge-associated microbes is not yet amenable to cultivation, an emphasis has been placed on the techniques centering around the 16S rRNA gene. A section has been included that covers the potential of sponge microbial communities for drug discovery. Finally, a ‘sponge-microbe interaction model’ is presented that summarizes our current understanding of the processes that might have shaped the community structure of the microbial assemblages within sponges.

Keywords

Microbial Community Microbial Diversity Marine Sponge Sponge Cell Reef Sponge 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alksne LE, Projan SJ (2000) Bacterial virulence as a target for antimicrobial chemotherapy. Curr Opin Biotechnol 11:625–36PubMedCrossRefGoogle Scholar
  2. Althoff K, Schütt C, Steffen R, Batel R, Müller WEG (1998) Evidence for a symbiosis between bacteria of the genus Rhodobacter and the marine sponge Halichondria panicea: harbor also for putatively toxic bacteria? Mar Biol 130:529–536CrossRefGoogle Scholar
  3. Amann R, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169PubMedGoogle Scholar
  4. Bakus GJ, Targett NM, Schulte B (1986) Chemical ecology of marine organisms: an overview. J Chem Ecol 12:951–987CrossRefGoogle Scholar
  5. Barbieri E, Paster BJ, Hughes D, Zurek L, Moser DP, Teske A, Sogin ML (2001) Phylogenetic characterization of epibiotic bacteria in the accessory nidamental gland and egg capsules of the squid Loligo pealei (Cephalopoda: Loliginidae). Environ Microbiol 3:151–167PubMedCrossRefGoogle Scholar
  6. Beer S, Ilan M (1998) In situ measurements of photosynthetic irradiance responses of two Red Sea sponges growing under dim light conditions. Mar Biol 131:613–617CrossRefGoogle Scholar
  7. Bergquist PR (1978) Sponges. University of California Press, BerkeleyGoogle Scholar
  8. Bernan VS, Greenstein M, Maiese WM (1997) Marine microorganisms as a source of new natural products. Adv Appl Microbiol 43:57–90PubMedCrossRefGoogle Scholar
  9. Bewley CA, Holland ND, Faulkner DJ (1996) Two classes of metabolites from Theonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia 52:716–722PubMedCrossRefGoogle Scholar
  10. Bewley CA, Faulkner DJ (1998) Lithistid sponges: star performers or hosts to the stars. Angew Chem Int Ed Engl 37:2162–2178CrossRefGoogle Scholar
  11. Böhm M, Schröder HC, Müller IM, Müller WE, Gamulin V (2000) The mitogen-activated protein kinase p38 pathway is conserved in metazoans: cloning and activation of p38 of the SAPK2 subfamily from the sponge Suberites domuncula. Biol Cell 92:95–104PubMedCrossRefGoogle Scholar
  12. Borowitzka MA, Hinde R, Pironet F (1988) Carbon fixation by the sponge Dysidea herbacea and its endosymbiont Oscillatoria spongeliae. In Choat JH et al (eds) Proc 6th Int Coral Reef Symposium, Townsville, Australia, pp 151–155Google Scholar
  13. Brusca RC, Brusca GJ (1990) Phylum Porifera: the sponges. In: Sinauer AD (ed) Invertebrates. Sinauer Press, MA, pp 181–210Google Scholar
  14. Carney JR, Rinehart KL (1995) Biosynthesis of brominated tyrosine metabolites by Aplysina fistularis. J Nat Prod 58:971–985PubMedCrossRefGoogle Scholar
  15. Cary SC, Giovannoni SJ (1993) Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc Natl Acad Sci USA 90:5695–5699PubMedCrossRefGoogle Scholar
  16. Davy SK, Trautman DA, Borowitzka MA, Hinde R (2002) Ammonium excretion by a symbiotic sponge supplies the nitrogen requirements of its rhodophyte partner. J Exp Biol 205:3505–3511PubMedGoogle Scholar
  17. Ebel R, Brenzinger M, Kunze A, Gross HJ, Proksch P (1997) Wound activation of protoxins in marine sponge Aplysina aerophoba. J Chem Ecol 23:1451–1462CrossRefGoogle Scholar
  18. Fenical W (1996) Marine biodiversity and the medicine cabinet. The status of new drugs from marine organisms. Oceanography 9:23–27CrossRefGoogle Scholar
  19. Friedrich AB (1998) Bakterien des Schwammes Aplysina cavernicola: Detektion, Charakterisierung und phylogenetische Einordnung. Masters Thesis. University of Würzburg, GermanyGoogle Scholar
  20. Friedrich AB, Merkert H, Fendert T, Hacker J, Proksch P, Hentschel U (1999) Microbial diversity in the marine sponge Aplysina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridisation (FISH). Mar Biol 134:461–470CrossRefGoogle Scholar
  21. Friedrich AB, Fischer I, Proksch P, Hacker J, Hentschel U (2001) Temporal variation of the microbial community associated with the Mediterranean sponge Aplysina aerophoba. FEMS Microbiol Ecol 38:105–113CrossRefGoogle Scholar
  22. Fuerst JA, Webb RI, Garson MJ, Hardy L, Reiswig HM (1998) Membrane-bounded nucleoids in microbial symbionts of marine sponges. FEMS Microbiol Lett 166:29–34CrossRefGoogle Scholar
  23. Fuerst JA, Webb RI, Garson MJ, Hardy L, Reiswig HM (1999) Membrane-bounded nuclear bodies in a diverse range of microbial symbionts of Great Barrier Reef sponges. Mem Queensland Mus 44:193–203Google Scholar
  24. Gallissian MF, Vacelet J (1976) Ultrastructure des quelques stades de l’ovogenese de spongiaires du genre Verongia (Dictyoceratida). Ann Sci Nat Zool 18:381–404Google Scholar
  25. Gillespie DE, Brady SF, Bettermann AD, Cianciotto NP, Liles MR, Rondon MR, Clardy J, Goodman RM, Handelsman J (2002) Isolation of antibiotics turbomycin a and b from a metagenomic library of soil microbial DNA. Appl Environ Microbiol 68:4301–4306PubMedCrossRefGoogle Scholar
  26. Giovannoni SJ, Rappe MS (2000) Evolution, diversity and molecular ecology of marine prokaryotes. In: Kirchman DL (ed) Microbial ecology of the ocean. Wiley, New York, pp 47–84Google Scholar
  27. Glöckner FO, Zaichikov E, Belkova N, Denissova L, Pernthaler J, Pernthaler A, Amann R (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of actinobacteria. Appl Environ Microbiol 66:5053–5065PubMedCrossRefGoogle Scholar
  28. Görtz HD, Brigger T (1998) Intracellular bacteria in protozoa. Naturwissenschaften 85:359–368PubMedCrossRefGoogle Scholar
  29. Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM (1998) Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol 5:245–249CrossRefGoogle Scholar
  30. Haygood MG, Schmidt EW, Davidson SK, Faulkner DJ (1999) Microbial symbionts of marine invertebrates: opportunities for microbial biotechnology. J Mol Microbiol Biotechnol 1:33–43PubMedGoogle Scholar
  31. Head IM, Saunders JR, Pickup RW (1998) Microbial evolution, diversity and ecology: a decade of ribosomal RNA analysis of uncultivated microorganisms. Microb Ecol 35:1–21PubMedCrossRefGoogle Scholar
  32. Henne A, Schmitz RA, Bomeke M, Gottschalk G, Daniel R (2000) Screening of environmental DNA libraries for the presence of genes conferring lipolytic activity on Escherichia coli. Appl Environ Microbiol 66:3113–3116PubMedCrossRefGoogle Scholar
  33. Hentschel U, Hacker J (2001) Pathogenicity islands: the tip of the iceberg. Microbes Infect 3:545–548PubMedCrossRefGoogle Scholar
  34. Hentschel U, Schmid M, Wagner M, Fieseler L, Gernert C, Hacker J (2001) Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS Microbiol Ecol 35:305–312PubMedCrossRefGoogle Scholar
  35. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J, Moore BS (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68:4431–4440PubMedCrossRefGoogle Scholar
  36. Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774PubMedGoogle Scholar
  37. Hugenholtz P, Tyson GW, Blackall LL (2002) Design and evaluation of 16S rRNA-targeted oligonucleotide probes for fluorescence in situ hybridization. Methods Mol Biol179:29–42PubMedGoogle Scholar
  38. Kobayashi J, Ishibashi M (1993) Bioactive metabolites from symbiotic marine microorganisms. Chem Rev 93:1753–1769CrossRefGoogle Scholar
  39. Kreuter MH, Leake RE, Rinaldi F, Müller-Klieser W, Maidhof A, Müller WEG, Schröder HC (1990). Inhibition of intrinsic protein tyrosine kinase activity of EGF-receptor kinase complex from human breast cancer cells by the marine sponge metabolite (+)-aeroplysinin-1. Comp Biochem Physiol B 97:151–158PubMedCrossRefGoogle Scholar
  40. Levi C, Levi P (1976) Embryogenese de Chondrosia reniformis (Nardo), demosponge ovipare, et transmission des bacteries symbiotiques. Ann Sci Nat Zool 18:367–380Google Scholar
  41. Li CW, Chen JY, Hua TE (1998) Precambrian sponges with cellular structures. Science 279:879–882PubMedCrossRefGoogle Scholar
  42. Lindsay MR, Webb RI, Fuerst JA (1997) Pirellulosomes: a new type of membrane-bounded cell compartment in planctomycete bacteria of the genus Pirellula. Microbiology 143:739–748CrossRefGoogle Scholar
  43. Lopez JV, McCarthy, PJ, Janda, KE, Willoughby R, Pomponi SH (1999) Molecular techniques reveal wide phyletic diversity of heterotrophic microbes associated with Discodermia spp. (Porifera: Demospongiae). Memoirs Queensland Museum 44: 329–341. BrisbaneGoogle Scholar
  44. Ludwig W, Schleifer KH (1994) Bacterial phylogeny based on 16S and 23S rRNA sequence analysis. FEMS Microbiol Rev 15:155–173PubMedCrossRefGoogle Scholar
  45. MacNeil IA, Tiong CL, Minor C, August PR, Grossman TH, Loiacono KA, Lynch BA, Phillips T, Narula S, Sundaramoorthi R, Tyler A, Aldredge T, Long H, Gilman M, Holt D, Osburne MS (2000) Expression and isolation of antimicrobial small molecules from soil DNA libraries. J Mol Microbiol Biotechnol 3:1–8Google Scholar
  46. Müller W, Böhm M, Grebenjuk V, Skorokhod A, Müller I, Gamulin V (2002) Conservation of the positions of metazoan introns from sponges to humans. Gene 295:299PubMedCrossRefGoogle Scholar
  47. Müller WEG (1998) Molecular phylogeny of eumetazoa: genes in sponges (Porifera) give evidence for the monophyly of animals. Progr Mol Subcell Biol 9:89–126CrossRefGoogle Scholar
  48. Muyzer G, Brinkhoff T, Nübel U, Santegoeds C, Schäfer H, Wawer C (1998) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. Mol Microb Ecol 344:1–27Google Scholar
  49. Olson JB, Harmody DK, McCarthy PJ (2002) Alphaproteobacteria cultivated from marine sponges display branching rod morphology. FEMS Microbiol Lett 211:169–173PubMedGoogle Scholar
  50. Ohta S, Uno M, Yoshimura M, Hiraga Y, Ikegami S (1996) Rhopaloic acid A: a novel norsesterterpene from a marine sponge, Rhopaloeides sp., which inhibits gastrulation of starfish embryos. Tetrahedron Lett 37:2265–2266CrossRefGoogle Scholar
  51. Pabel C, Vater J, Wilde C, Franke P, Hofemeister J, Adler B, Bringmann G, Hacker J, Hentschel U (2003) Antimicrobial activities and matrix-assisted laser desorption/ionization mass spectrometry of Bacillus isolates from the marine sponge Aplysina aerophoba. Mar Biotechnol (in press)Google Scholar
  52. Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276:734–740PubMedCrossRefGoogle Scholar
  53. Pile AJ (1997) Finding Reiswig’s missing carbon: quantification of sponge feeding using dual-beam flow cytometry. Proc 8th Int Coral Reef Symp 2:1403–1410Google Scholar
  54. Preston CM, Wu KY, Molinski TF, DeLong EF (1996) A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc Natl Acad Sci USA 93:6241–624PubMedCrossRefGoogle Scholar
  55. Proksch P, Edrada RA, Ebel R (2002) Drugs from the seas: current status and microbiological implications. Appl Microbiol Biotechnol 59:125–134PubMedCrossRefGoogle Scholar
  56. Pryde SE, Richardson AJ, Stewart CS, Flint HJ (1999) Molecular analysis of the microbial diversity present in the colonic wall, colonic lumen, and cecal lumen of a pig. Appl Environ Microbiol 65:5372–5377PubMedGoogle Scholar
  57. Ravenschlag K, Sahm K, Pernthaler J, Amann R (1999) High bacterial diversity in permanently cold marine sediments. Appl Environ Microbiol 65:3982–3989PubMedGoogle Scholar
  58. Reiswig H (1974) Water transport, respiration and energetics of three tropical marine sponges. J Exp Mar Biol Ecol 14:231–249CrossRefGoogle Scholar
  59. Rondon MR, Goodman RM, Handelsman J (1999) The earth’s bounty: assessing and accessing soil microbial diversity. Trends Biotechnol 17:403–409PubMedCrossRefGoogle Scholar
  60. Rondon MR, August PR, Bettermann AD, Brady SF, Grossman TH, Liles MR, Loiacono KA, Lynch BA, MacNeil IA, Minor C, Tiong CL, Gilman M, Osburne MS, Clardy J, Handelsman J, Goodman RM (2000) Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl Environ Microbiol 66:2541–2547PubMedCrossRefGoogle Scholar
  61. Rützler K (1985) Associations between Caribbean sponges and photosynthetic organisms. In: Rützler K (ed) New perspectives in sponge biology. Smithsonian Institution Press, Washington, DC, pp 455–466Google Scholar
  62. Santavy DL, Willenz P, Colwell RR (1990) Phenotypic study of bacteria associated with the Caribbean sclerosponge, Ceratoporella nicholsoni. Appl Environ Microbiol 56:1750–1762PubMedGoogle Scholar
  63. Sauer C, Dudaczek D, Holldobler B, Gross R (2002) Tissue localization of the endosymbiotic bacterium ‘Candidatus Blochmannia floridanus’ in adults and larvae of the Carpenter ant Camponotus floridanus. Appl Environ Microbiol 68:4187–4193PubMedCrossRefGoogle Scholar
  64. Schleper C, Eck J (2001) Umweltgenomik: Charakterisierung und Nutzung nicht-kultivierter Mikroorganismen. Biospektrum 6:494–451Google Scholar
  65. Schleper C, Swanson RV, Mathur EJ, DeLong EF (1997) Characterization of a DNA polymerase from the uncultivated psychrophilic archaeon Cenarchaeum symbiosum. J Bacterid 179:7803–7811Google Scholar
  66. Schleper C, DeLong EF, Preston CM, Feldman RA, Wu KY, Swanson RV (1998) Genomic analysis reveals chromosomal variation in natural populations of the uncultured psychrophilic archaeon Cenarchaeum symbiosum. J Bacterid 180:5003–5009Google Scholar
  67. Schumann-Kindel G, Bergbauer M, Manz W, Szewzyk U, Reitner J (1997) Aerobic and anaerobic microorganisms in modern sponges: a possible relationship to fossilization processes. Facies 36:268–272Google Scholar
  68. Schmidt EW, Obraztova AY, Davidson SK, Faulkner DJ, Haygood MG (2000) Identification of the antifungal peptide-containing symbiont of the marine sponge Theonella swinhoei as a novel Delta-Proteobacterium ‘Candidatus Entotheonella palauensis’. Mar Biol 136:969–977CrossRefGoogle Scholar
  69. Schmitz FJ (1994) Cytotoxic compounds from sponges and associated microfauna. In: van Soest RWM, van Kempen TMG, Braekman JC (eds) Sponges in time and space. Proc 4th Int Porifera Congr Amsterdam, Balkema, RotterdamGoogle Scholar
  70. Seow KT, Meurer G, Gerlitz M, Wendt-Pienkowski E, Hutchinson CR, Davies J (1997) A study of iterative type II polyketide synthases, using bacterial genes cloned from soil DNA: a means to access and use genes from uncultured microorganisms. J Bacteriol179:7360–7368PubMedGoogle Scholar
  71. Sharma GM, Burkholder PR (1967) Studies on antimicrobial substances of sponges. I. Isolation, purification and properties of a new bromine-containing antimicrobial substance. J Antibiot Tokyo Ser A 20:200–203Google Scholar
  72. Steinert M, Hentschel U, Hacker J (2000) Symbiosis and pathogenesis: evolution of themicrobe-host interaction. Naturwissenschaften 87:1–11PubMedCrossRefGoogle Scholar
  73. Tajima K, Aminov RI, Nagamine T, Ogata K, Nakamura M, Matsui H, Benno Y (1999) Rumen bacterial diversity as determined by sequence analysis of 16S rDNA libraries. FEMS Microbiol Ecol 29:159–169CrossRefGoogle Scholar
  74. Teeyapant R, Woerdenbag HJ, Kreis P, Hacker J, Wray V, Witte L, Proksch P (1993) Antibiotic and cytotoxic activity of brominated compounds from the marine sponge Verongia aerophoba. Z Naturforsch C 48:939–945PubMedGoogle Scholar
  75. Thakur NL, Hentschel U, Krasko A, Pabel CT, Anil AC, Müller WEG (2003) Antibacterial activity of the sponge Suberites domuncula and its primmorphs: potential basis for chemical defense. Aquat Microb Ecol 31:77–83CrossRefGoogle Scholar
  76. Thompson JE, Barrow KD, Faulkner JD (1983) Localization of two brominated metabolites, aerothionin and homoaerothionin, in spherulous cells of the marine sponge Aplysina fistularis (=Verongia thiona).Acta Zool (Stockh) 44:199–210CrossRefGoogle Scholar
  77. Thompson JE, Murphy PT, Bergquist PR, Evans EA (1987) Environmentally induced variation in diterpene composition of the marine sponge Rhopaloides odorabile. Biochem Syst Ecol 15:595–606CrossRefGoogle Scholar
  78. Thorns C, Horn M, Wagner M, Hentschel U, Proksch P (2003) Monitoring microbial diversity and natural products profiles of the sponge Aplysina cavernicola following transplantation. Mar Biol 42:685–692Google Scholar
  79. Turon X, Galera J, Uriz MJ (1997) Clearance rates and aquiferous systems in two sponges with contrasting life-history strategies. J Exp Zool 278:22–36CrossRefGoogle Scholar
  80. Turon X, Becerro MA, Uriz MJ (2000) Distribution of brominated compounds within the sponge Aplysina aerophoba: coupling of X-ray microanalysis with cryofixation techniques. Cell Tissue Res 301:311–322PubMedCrossRefGoogle Scholar
  81. Tymiak AA, Rinehart KL (1981) Biosynthesis of dibromotyrosine-derived antimicrobial compounds from the marine sponge Aplysina fistularis (=Verongia aurea). J Am Chem Soc 103:6763–6765CrossRefGoogle Scholar
  82. Usher KM, Kuo J, Fromont J, Sutton DC (2001) Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461:15–23CrossRefGoogle Scholar
  83. Unson MD, Holland ND, Faulkner DJ (1994) A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue. Mar Biol 119:1–11CrossRefGoogle Scholar
  84. Vacelet J (1970) Description de cellules a bacteries intranucléaires chez des éponges Verongia. J Microsc 9:333–346Google Scholar
  85. Vacelet J (1971) Étude en microscopie électronique de l’association entre une cyanophycée chroococcale et une éponge du genre Verongia. J Microsc 12:363–380Google Scholar
  86. Vacelet J (1975) Étude en microscopie électronique de l’association entre bactéries et spongiaires du genre Verongia (Dictyoceratida). J Microsc Biol Cell 23:271–288Google Scholar
  87. Vacelet J, Donadey C (1977) Electron microscope study of the association between some sponges and bacteria. J Exp Mar Ecol 30:301–314CrossRefGoogle Scholar
  88. Vacelet J, Boury-Esnault N, Fiala-Medioni A, Fisher CR (1995) A methanotrophic carnivorous sponge. Nature 377:296CrossRefGoogle Scholar
  89. Vogel S (1977) Current-induced flow through living sponges in nature. Proc Natl Acad Sci USA 74:2069-2071Google Scholar
  90. Von Wintzingerode F, Gobel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Ecol 21:213–229Google Scholar
  91. Wagner-Dobler I, Beil W, Lang S, Meiners M, Laatsch H (2002) Integrated approach to explore the potential of marine microorganisms for the production of bioactive metabolites. Adv Biochem Eng Biotechnol 74:207–238PubMedGoogle Scholar
  92. Webb VL, Maas EW (2002) Sequence analysis of 16S rRNA gene of cyanobacteria associated with the marine sponge Mycale (Carmia) hentscheli. FEMS Microbiol Lett 207:43–7PubMedCrossRefGoogle Scholar
  93. Webster N, Hill RT (2001) The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by an α-proteobacterium. Mar Biol 138:843–851CrossRefGoogle Scholar
  94. Webster NS, Wilson KJ, Blackall LL, Hill RT (2001a) Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol 67:434–444CrossRefGoogle Scholar
  95. Webster NS, Webb RI, Ridd MJ, Hill RT, Negri AP (2001b) The effects of copper on the microbial community of a coral reef sponge. Environ Microbiol 31:19–31CrossRefGoogle Scholar
  96. Weiss B, Ebel R, Elbrächter M, Kirchner M, Proksch P (1996) Defense metabolites from the marine sponge Verongia aerophoba. Biochem Syst Ecol 24:1–12CrossRefGoogle Scholar
  97. Wehrl M (2001) Untersuchungen zur Interaktion des marinen Schwammes Aplysina aerophoba mit assoziierten Mikroorganismen. Masters Thesis, University of Würzburg, GermanyGoogle Scholar
  98. Weiss B, Ebel R, Elbrächter M, Kirchner M, Proksch P (1996) Defense metabolites from the marine sponge Verongia aerophoba. Biochem Syst Ecol 24:1–12CrossRefGoogle Scholar
  99. Wilkinson CR (1978a) Microbial associations in sponges. I. Ecology, physiology and microbialpopulations of coral reef sponges. Mar Biol 49:161–167CrossRefGoogle Scholar
  100. Wilkinson CR (1978b) Microbial associations in sponges. II. Numerical analysis of sponge and water bacterial populations. Mar Biol 49:169–176.CrossRefGoogle Scholar
  101. Wilkinson CR (1978c) Microbial associations in sponges. III. Ultrastructure of the in situ associations in coral reef sponges. Mar Biol 49:177–185CrossRefGoogle Scholar
  102. Wilkinson CR (1992) Symbiotic interactions between marine sponges and algae. In: Reisser W (ed) Algae and symbioses. Biopress, Bristol, pp 112–151Google Scholar
  103. Wilkinson CR, Fay P (1979) Nitrogen fixation in coral reef sponges with symbiotic cyanobacteria. Nature 279:527–529Google Scholar
  104. Wilkinson CR, Garrone R (1980) Nutrition in marine sponges. Involvement of symbiotic bacteria in the uptake of dissolved carbon. In: Smith DC, Tiffon Y (ed) Nutrition in the lower Metazoa. Pergamon Press, Oxford, pp 157–161Google Scholar
  105. Wilkinson CR, Nowak M, Austin B, Colwell RR (1981) Specificity of bacterial symbionts in Mediterranean and Great Barrier Reef sponges. Microb Ecol 7:13–21CrossRefGoogle Scholar
  106. Wilkinson CR, Garrone G, Vacelet J (1984) Marine sponges discriminate between food bacteria and bacterial symbionts: electron microscope radioautography and in situ evidence. Proc R Soc Lond B 220:519–528CrossRefGoogle Scholar
  107. Willenz P, Hartman WD (1989) Micromorphology and ultrastructure of Caribbean sclerosponges. I. Ceratoporella nicholsoni and Stromatospongia norae (Ceratoporellidae Porifera). Mar Biol 103:387–402CrossRefGoogle Scholar
  108. Wörheide G (1998) The reef cave dwelling ultraconservative coralline demosponge Astrosclera willeyana Lister 1900 from the Indo-Pacific. Facies 38:1–88CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2003

Authors and Affiliations

  • U. Hentschel
    • 1
  • L. Fieseler
    • 1
  • M. Wehrl
    • 1
  • C. Gernert
    • 1
  • M. Steinert
    • 1
  • J. Hacker
    • 1
  • M. Horn
    • 2
  1. 1.Institut für Molekulare InfektionsbiologieUniversität WürzburgWürzburgGermany
  2. 2.Abteilung Mikrobielle Ökologie, Institut für Ökologie und NaturschutzUniversität WienWienAustria

Personalised recommendations