Polar Biology

, Volume 29, Issue 8, pp 662–667 | Cite as

Dense populations of Archaea associated with the demosponge Tentorium semisuberites Schmidt, 1870 from Arctic deep-waters

  • Thomas Pape
  • Friederike Hoffmann
  • Nadia-Valérie Quéric
  • Karen von Juterzenka
  • Joachim Reitner
  • Walter Michaelis
Original Paper

Abstract

The associated microbial community in the mesohyl of the Arctic deep-water sponge Tentorium semisuberites Schmidt, 1870 (Hadromerida, Demospongiae) is dominated by Archaea. This is the result of an integral approach applying analyses of microbial lipid biomarkers as well as microscopic investigations using differential fluorescence in situ hybridisation with universal probes and counterstaining with 4′,6′-diamidino-2-phenylindole (DAPI) on sponge sections based on samples collected in the Greenland Sea in 2001, 2002 and 2005. The distribution of isoprenoidal C40 hydrocarbons of the biphytane series suggests that affiliates of both major archaeal kingdoms, the Crenarchaeota and the Euryarchaeota, are present in the choanosome of T. semisuberites. Positive signals using the oligonucleotide probe ARCH915 indicate high numbers of Archaea in the mesohyl of this sponge. Based on optical estimations 70–90% of all microbial DAPI signals accounted for archaeal cells. Archaea in these high proportions have never been described in an Arctic deep-sea hadromerid sponge, nor in any other demosponge species. Similar observations in specimens collected over a time scale of 4 years suggest permanent sponge-Archaea associations.

References

  1. Amann RI, Krumholz L, Stahl DA (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172:762–770PubMedGoogle Scholar
  2. Barthel D, Tendal OS (1993) The sponge association of the abyssal Norwegian-Greenland Sea: species composition, substrate relationships and distribution. Sarsia 78:83–96Google Scholar
  3. Chappe B, Michaelis W, Albrecht P (1980) Molecular fossils of Archaebacteria as selective degradation products of kerogen. In: Douglas AG, Maxwell JR (eds) Advances in Organic Geochemistry 1979. Pergamon Press, Oxford, pp 265–274Google Scholar
  4. Daims H, Brühl A, Amann R, Schleifer K-H, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444PubMedGoogle Scholar
  5. DeLong EF, King LL, Massana R, Cittone H, Murray A, Schleper C, Wakeham SG (1998) Dibiphytanyl ether lipids in nonthermophilic Crenarchaeotes. Appl Environ Microbiol 64:1133–1138PubMedGoogle Scholar
  6. 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
  7. Hoffmann F, Janussen D, Dröse W, Arp G, Reitner J (2003) Histological investigation of organisms with hard skeletons: a case study of siliceous sponges. Biotech Histochem 78:191–199PubMedCrossRefGoogle Scholar
  8. Hoffmann F, Larsen O, Rapp HT, Osinga R (2005a) Oxygen dynamics in choanosomal sponge explants. Mar Biol Res 1:160–163CrossRefGoogle Scholar
  9. Hoffmann F, Larsen O, Thiel V, Rapp HT, Pape T, Michaelis W, Reitner J (2005b) An anaerobic world in sponges. Geomicrobiol J 22:1–10CrossRefGoogle Scholar
  10. Ilan M, Abelson A (1995) The life of a sponge in a sandy lagoon. Biol Bull 189:363–369CrossRefGoogle Scholar
  11. Koga Y, Nishihara M, Morii H, Akagawa-Matsushita M (1993) Ether polar lipids of methanogenic bacteria: structures, comparative aspects, and biosyntheses. Microbiol Rev 57:164–182PubMedGoogle Scholar
  12. Kröncke I (1998) Macrofauna communities in the Amundsen Basin, at the Morris Jesup Rise and at the Yermak Plateau (Eurasian Arctic Ocean). Polar Biol 19:383–392CrossRefGoogle Scholar
  13. Madrid VM, Taylor GT, Scranton MI, Chistoserdov AY (2001) Phylogenetic diversity of bacterial and archaeal communities in the anoxic zone of the Cariaco Basin. Appl Environ Microbiol 67:1663–1674PubMedCrossRefGoogle Scholar
  14. Manz W, Arp G, Schumann-Kindel G, Szewzyk U, Reitner J (2000) Widefield deconvolution epifluorescence microscopy combined with fluorescence in situ hybridization reveals the spatial arrangement of bacteria in sponge tissue. J Microbiol Methods 40:125–134PubMedCrossRefGoogle Scholar
  15. Margot H, Acebal C, Toril E, Amils R, Fernandez Puentes JL (2002) Consistent association of crenarchaeal Archaea with sponges of the genus Axinella. Mar Biol 140:739–745CrossRefGoogle Scholar
  16. Pape T, Blumenberg M, Seifert R, Egorov VN, Gulin SB, Michaelis W (2005) Lipid geochemistry of methane-seep-related Black Sea carbonates. In: Peckmann J, Goedert JL (eds) Palaeogeogr, Palaeoclimat, Palaeoecol (special issue: Geobiology of Ancient and Modern Methane-Seeps), vol 227, pp 31–47Google Scholar
  17. Pape T, Blumenberg M, Thiel V, Michaelis W (2004) Biphytanes as biomarkers for sponge-associated Archaea. In: Pansini M, Pronzato R, Bavestrello G, Manconi R (eds) Sponge science in the new Millenium. Boll Mus Ist Biol Univ Genova 68:509–515Google Scholar
  18. Pernthaler A, Preston CM, Pernthaler J, DeLong EF, Amann R (2002) Comparison of fluorescently labeled oligonucleotide and polynucleotide probes for the detection of pelagic marine bacteria and archaea. Appl Environ Microbiol 68:661–667PubMedCrossRefGoogle Scholar
  19. Preston CM, Wu KY, Molinski TF, DeLong EF (1996) A psychrophilic crenarcheon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. P Natl Acad Sci USA 93:6241–6246CrossRefGoogle Scholar
  20. Reitner J (1993) Modern cryptic microbialite/metazoan facies from Lizard Island (Great Barrier Reef, Australia) formation and concepts. Facies 29:3–40CrossRefGoogle Scholar
  21. Sinninghe Damsté JS, Schouten S, Hopmans EC, van Duin ACT, Geenevasen JAJ (2002) Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota. J Lipid Res 43:1641–1651CrossRefGoogle Scholar
  22. Stahl DA, Amann RI (1991) Development and application of nucleic acid probes in bacterial systematics. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chicester, pp 205–248Google Scholar
  23. Thiel V, Blumenberg M, Hefter J, Pape T, Pomponi S, Reed J, Reitner J, Wörheide G, Michaelis W (2002) A chemical view of the most ancient metazoa—biomarker chemotaxonomy of hexactinellid sponges. Naturwissenschaften 89:60–66PubMedCrossRefGoogle Scholar
  24. 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
  25. Vacelet J, Fiala-Médioni A, Fisher CR, Boury-Esnault N (1996) Symbiosis between methane-oxidizing bacteria and a deep-sea carnivorous cladorhizid sponge. Mar Ecol Prog Ser 145:77–85CrossRefGoogle Scholar
  26. Webster NS, Negri AP, Munro MMHG, Battershill CN (2004) Diverse microbial communities inhabit Antarctic sponges. Environ Microbiol 6:288–300PubMedCrossRefGoogle Scholar
  27. Webster NS, Watts JEM, Hill RT (2001) Detection and phylogenetic analysis of novel Crenarchaeote and Euryarchaeote 16S ribosomal RNA gene sequence from a Great Barrier Reef sponge. Mar Biotechnol 3:600–608PubMedCrossRefGoogle Scholar
  28. Wilkinson CR (1983) Phylogeny of bacterial and cyanobacterial symbionts in marine sponges. In: Schenk HEA, Schwemmler W (eds) Endocytobiology. II. Intracellular space as oligogenetic ecosystem. de Gruyter, Berlin, pp 993–1002Google Scholar
  29. Witte U (1995) Reproduktion, Energiestoffwechsel und Biodepositionsleistung dominanter Porifera aus der Tiefsee des Europäischen Nordmeeres. Bericht Sonderforschungsbereich 313, vol 53. University of Kiel, Kiel, pp 1–98Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Thomas Pape
    • 1
    • 6
  • Friederike Hoffmann
    • 2
    • 3
  • Nadia-Valérie Quéric
    • 4
  • Karen von Juterzenka
    • 4
    • 5
  • Joachim Reitner
    • 2
  • Walter Michaelis
    • 1
  1. 1.Institute of Biogeochemistry and Marine ChemistryUniversity of HamburgHamburgGermany
  2. 2.Center of Geosciences, GeobiologyUniversity of GöttingenGöttingenGermany
  3. 3.Max Planck Institute for Marine MicrobiologyBremenGermany
  4. 4.Alfred-Wegener-Institute for Polar and Marine Research, Deep Sea ResearchBremerhavenGermany
  5. 5.Institute for Polar EcologyChristian-Albrechts-University of KielKielGermany
  6. 6.Research Center Ocean MarginsUniversity of BremenBremenGermany

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