Skip to main content
SpringerLink
Log in

Monitoring microbial diversity and natural product profiles of the sponge Aplysina cavernicola following transplantation

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

In order to assess the stability of the microbial community of the sponge Aplysina cavernicola under in situ conditions, sponges were transplanted from their original location (>40 m depth) to shallower, more light-exposed sites (7–15 m depth). Transmission electron microscopy revealed that the microbial community remained visually unchanged and free of cyanobacteria over the experimental time period of 3 months. Denaturing gradient gel electrophoresis (DGGE) of PCR-amplified partial 16S rRNA gene sequences allowed a distinction between the variable and permanent fraction of the bacterial community. Comparative sequence analysis of four variable DGGE bands revealed high sequence similarity to representatives of the Alpha- and Gammaproteobacteria and the phylum Bacteroidetes, which have been recovered previously from Mediterranean seawater as clone sequences or by cultivation. Seven (out of 12) permanent DGGE bands showed high sequence similarity to a sponge-specific, monophyletic 16S rRNA gene sequence cluster within the Acidobacteria division, and to a sequence cluster of uncertain affiliation. These sequence clusters represent members of a common microbial community that is shared among distantly related sponges from different, non-overlapping geographic regions. Four additional permanent DGGE bands showed high sequence similarity to a Betaproteobacterium, Burkholderia cepacia, which is not typically known as a marine bacterium. High-performance liquid chromatography analyses of sponge tissues revealed no changes in metabolite pattern, indicating that these compounds are expressed constitutively irrespective of the variations resulting from the transplantation experiment.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1a–d.
Fig. 2a, b.
Fig. 3.
Fig. 4.

Similar content being viewed by others

References

  • 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 130:529–536

    Article  Google Scholar 

  • Barns SM, Takala SL, Kuske CR (1999) Wide distribution and diversity of members of the bacterial kingdom Acidobacterium in the environment. Appl Environ Microbiol 65:1731–1737

    CAS  PubMed  Google Scholar 

  • Betancourt-Lozano M, Gonzalez-Farias F, Gonzalez-Acosta B, Garcia-Gasca A, Bastida-Zavala JR (1998) Variation of antimicrobial activity of the sponge Aplysina fistularis (Pallas, 1766) and its relation to associated fauna. J Exp Mar Biol Ecol 223:1–18

    Article  Google Scholar 

  • Bewley CA, Holland ND, Faulkner DJ (1996) Two classes of metabolites from Theonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia 52:716–722

    CAS  PubMed  Google Scholar 

  • Borowitzka MA, Hinde R, Pironet F (1988) Carbon fixation by the sponge Dysidea herbacea and its endosymbiont Oscillatoria spongeliae. In: Choat JH (ed) Proc 6th Int Coral Reef Symp. Symposium Executive Committee, Townsville, pp 151–155

  • Butler SL, Doherty CJ, Hughes JE, Nelson JW, Govan JR (1995) Burkholderia cepacia and cystic fibrosis: do natural environments present a potential hazard? J Clin Microbiol 33:1001–1004

    CAS  PubMed  Google Scholar 

  • Carney JR, Rinehart KL (1995) Biosynthesis of brominated tyrosine metabolites by Aplysina fistularis. J Nat Prod 58:971–985

    CAS  PubMed  Google Scholar 

  • Ebel R, Brenzinger M, Kunze A, Gross HJ, Proksch P (1997) Wound activation of protoxins in marine sponge Aplysina aerophoba. J Chem Ecol 23:1451–1462

    CAS  Google Scholar 

  • Ebel R, Marin A, Proksch P (1999) Organic-specific distribution of dietary alkaloids in the marine opisthobranch Tylodina perversa. Biochem Syst Ecol 27:769–777

    Article  CAS  Google Scholar 

  • Friedrich AB (1998) Bakterien des Schwammes Aplysina cavernicola: Detektion, Charakterisierung und phylogenetische Einordnung. Masters thesis, Universität Würzburg, Würzburg, Germany

  • 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 hybridization (FISH). Mar Biol 134:461–470

    Article  Google Scholar 

  • 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 38:105–113

    Article  CAS  Google Scholar 

  • Goldenstein K, Fendert T, Proksch P, Winterfeldt E (2000) Enantioselective preparation and enzymatic cleavage of spiroisoxazoline amides. Tetrahedron 56:4173–4185

    Article  CAS  Google Scholar 

  • 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 35:305–312

    CAS  PubMed  Google Scholar 

  • 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 68:4431–4440

    Article  CAS  PubMed  Google Scholar 

  • Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774

    CAS  PubMed  Google Scholar 

  • Muyzer G, Brinkhoff T, Nübel U, Santegoeds C, Schäfer H, Wawer C (1998) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) Molecular microbial ecology, manual 3.4.4. Kluwer, Dordrecht, pp 1–27

  • Ohlson JB, Harmody DK, McCarthy PJ (2002) Alphaproteobacteria cultivated from marine sponges display branching rod morphology. FEMS Microbiol Lett 211:169–173

    Article  PubMed  Google Scholar 

  • Olsen GJ, Matsuda H, Hagstrom R, Overbeek R (1994) FastDNAml: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comput Applic Biosci 10:41–48

    CAS  Google Scholar 

  • Pansini M (1997) Effects of light on the morphology, distribution and ecology of some Mediterranean sponges. Biol Mar Mediterr 4:74–80

    Google Scholar 

  • Pile AJ (1997) Finding Reiswig's missing carbon: quantification of sponge feeding using dual-beam flow cytometry. In: Lessios HA, MacIntyre IG (eds) Proc 8th Int Coral Reef Symp, vol 2. Smithsonian Tropical Research Institute, Balboa, Panama, pp 1403–1410

  • Prakash D, Chauhan A, Jain RK (1996) Plasmid-encoded degradation of p-nitrophenol by Pseudomonas cepacia. Biochem Biophys Res Commun 224:375–381

    Article  CAS  PubMed  Google Scholar 

  • Regoli F, Cerrano C, Chierici E, Bompadre S, Bavestrello G (2000) Susceptibility to oxidative stress of the Mediterranean demosponge Petrosia ficiformis: role of endosymbionts and solar irradiance. Mar Biol 137:453–461

    Article  CAS  Google Scholar 

  • Reiswig HM (1974) Water transport, respiration and energetics of three tropical marine sponges. J Exp Mar Biol Ecol 14:231–249

    Google Scholar 

  • Rützler K (1981) An unusual bluegreen alga symbiotic with two new species of Ulosa (Porifera: Hymeniavidonidae) from Carrie Bow Cay, Belize. Mar Ecol 2:35–50

    Google Scholar 

  • Rützler K (1985) Associations between Caribbean sponges and photosynthetic organisms. In: Rützler K (ed) New perspectives in sponge biology. Smithsonian Institution Press, Washington, D.C., pp 455–466

  • Sara M (1971) Ultrastructural aspects of the symbiosis between two species of the genus Aphanocapsa (Cyanophyceae) and Ircinia variabilis (Demospongiae). Mar Biol 11:214–221

    Google Scholar 

  • Sievert SM, Kuever J, Muyzer G (2000) Identification of 16S ribosomal DNA–defined bacterial populations at a shallow submarine hydrothermal vent near Milos Island (Greece). Appl Environ Microbiol 66:3102–3109

    Article  CAS  PubMed  Google Scholar 

  • Strunk O, Ludwig W (1997) ARB software program package. http://www.arb-home.de, cited June 2002

  • 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 Sect C Biosci 48:939–945

    CAS  Google Scholar 

  • Thakur NL, Hentschel U, Krasko A, Pabel CT, Anila AC, Müller WEG (2003) Antibacterial activity of the sponge Suberites domuncula and its primmorphs: potential basis for chemical defense. Aquatic Microb Ecol (in press)

    Google Scholar 

  • 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) 44:199–210

    Google Scholar 

  • Thoms C (2000) Untersuchungen zur frasshemmenden Aktivität von Schwamminhaltstoffen gegenüber Fischen. Masters thesis, Universität Bremen, Bremen, Germany

  • 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 301:311–322

    CAS  PubMed  Google Scholar 

  • 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 119:1–11

    CAS  Google Scholar 

  • Vacelet J (1959) Repartition generale des éponges et systematique des éponges cornees de la region de Marseille et de quelques stations Mediterraneenes. Recl Trav Stn Mar Endoume Fac Sci Mars 16:39–109

    Google Scholar 

  • Vacelet J (1971) Étude en microscopie électronique de l´association entre une cyanophycée chroococcale et une éponge du genre Verongia. J Microsc 12:363–380

    Google Scholar 

  • Vacelet J (1975) Étude en microscopie électronique de l'association entre bactéries et spongiaires du genre Verongia (Dictyoceratida). J Microsc Biol Cell 23:271–288

    Google Scholar 

  • Vacelet J, Donadey C (1977) Electron microscope study of the association between some sponges and bacteria. J Exp Mar Biol Ecol 30:301–314

    Google Scholar 

  • van Soest R (1996) Porifera, Schwämme. In: Westheide W, et al (eds) Spezielle Zoologie, Teil 1: Einzeller und wirbellose Tiere. Fischer, Stuttgart, pp 98–119

  • Vogel S (1977) Current-induced flow through living sponges in nature. Proc Natl Acad Sci USA 74:2069–2071

    CAS  PubMed  Google Scholar 

  • Webster NS, Hill RT (2001) The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by a αProteobacterium. Mar Biol 138:843–851

    CAS  Google Scholar 

  • Webster NS, Webb RI, Ridd MJ, Hill RI, Negri AP (2001) The effects of copper on the microbial community of a coral reef sponge. Environ Microbiol 31:19–31

    Article  Google Scholar 

  • Wehrl M (2001) Untersuchungen zur Interaktion des marinen Schwammes Aplysina aerophoba mit assoziierten Mikroorganismen. Masters thesis, Universität Würzburg, Würzburg, Germany

  • Weiss B, Ebel R, Elbrächter M, Kirchner M, Proksch P (1996) Defense metabolites from the marine sponge Verongia aerophoba. Biochem Syst Ecol 24:1–12

    Article  CAS  Google Scholar 

  • Wilkinson CR (1987) Significance of microbial symbionts in sponge evolution and ecology. Symbiosis 4:135–145

    Google Scholar 

  • Wilkinson CR, Fay P (1979) Nitrogen fixation in coral reef sponges with symbiotic bacteria. Nature 279:527–529

    CAS  Google Scholar 

  • Wilkinson CR, Garrone R (1980) Nutrition in marine sponges. Involvement of symbiotic bacteria in the uptake of dissolved carbon. In: Smith D, et al (eds) Nutrition in lower Metazoa. Pergamon, Oxford, pp 157–161

  • Wilkinson CR, Vacelet J (1979) Transplantation of marine sponges to different conditions of light and current. J Exp Mar Biol Ecol 37:91–104

    Google Scholar 

  • Wilkinson CR, Nowak M, Austin B, Colwell RR (1981) Specificity of bacterial symbionts in Mediterranean and Great Barrier Reef sponges. Microb Ecol 7:13–21

    Google Scholar 

  • Willenz P, Hartman WD (1989) Micromorphology and ultrastructure of Caribbean sclerosponges. I. Ceratoporella nicholsoni and Stromatospongia norae (Ceratoporellidae: Porifera). Mar Biol 103:387–402

    Google Scholar 

  • Zanetti F, De Luca G, Stampi S (2000) Recovery of Burkholderia pseudomallei and B. cepacia from drinking water. Int J Food Microbiol 59:67–72

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge J. Kuever (MPI Bremen) for sharing his knowledge on DGGE analysis and for interesting discussions, C. Gernert (Universität Würzburg) for excellent technical assistance and the staff of the Hydra-Institut für Meereswissenschaften at Elba, Italy, for diving and technical support. This work was generously supported by grants to P.P. (Fonds der chemischen Industrie) and to U.H. (SFB 567) and by BMBF grant "BiotecMarin" to P.P. (03F0345C) and U.H. (03F0345E). The experiments comply with the current laws of the country in which the experiments were performed.

Author information

Authors and Affiliations

  1. Institut für Pharmazeutische Biologie, Universität Düsseldorf, Universitätsstrasse 1, Geb. 26.23, 40225, Düsseldorf, Germany

    C. Thoms & P. Proksch

  2. Lehrstuhl für Mikrobiologie, Technische Universität München, Am Hochanger 4, 85350, Freising, Germany

    M. Horn & M. Wagner

  3. Institut für Molekulare Infektionsbiologie, Universität Würzburg, Röntgenring 11, 97070, Würzburg, Germany

    U. Hentschel

Authors
  1. C. Thoms
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Horn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Wagner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. U. Hentschel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. Proksch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to U. Hentschel.

Additional information

Communicated by O. Kinne, Oldendorf/Luhe

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thoms, C., Horn, M., Wagner, M. et al. Monitoring microbial diversity and natural product profiles of the sponge Aplysina cavernicola following transplantation. Marine Biology 142, 685–692 (2003). https://doi.org/10.1007/s00227-002-1000-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-002-1000-9

Keywords

Search

Navigation