Microbial Ecology

, Volume 54, Issue 1, pp 101–111 | Cite as

Sponge-specific Bacterial Associations of the Mediterranean Sponge Chondrilla nucula (Demospongiae, Tetractinomorpha)

  • Vera Thiel
  • Sven Leininger
  • Rolf Schmaljohann
  • Franz Brümmer
  • Johannes F. Imhoff
Article

Abstract

A stable and specific bacterial community was shown to be associated with the Mediterranean sponge Chondrilla nucula. The associated bacterial communities were demonstrated to be highly similar for all studied specimens regardless of sampling time and geographical region. In addition, analysis of 16S rDNA clone libraries revealed three constantly C. nucula-associated bacterial phylotypes belonging to the Acidobacteria, the Gamma- and Deltaproteobacteria present in sponge specimens from two Mediterranean regions with distinct water masses (Ligurian Sea and Adriatic Sea). For the first time, candidate division TM7 bacteria were found in marine sponges. A major part (79%) of the C. nucula-derived 16S rDNA sequences were closely related to other sponge-associated bacteria. Phylogenetic analysis identified 14 16S rRNA gene sequence clusters, seven of which consisted of exclusively sponge-derived sequences, whereas the other seven clusters contained additional environmental sequences. This study adds to a growing database on the stability and variability of microbial consortia associated with marine sponges.

Abbreviations

SAB cluster

Sponge-associated bacterial cluster

CN cluster

Chondrilla nucula-associated cluster

AS

Adriatic Sea

LS

Ligurian Sea

References

  1. 1.
    Abrams, ES, Stanton, VP (1992) Use of denaturing gradient gel-electrophoresis to study conformational transitions in nucleic-acids. Method Enzymol 212: 71–104CrossRefGoogle Scholar
  2. 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. 3.
    Altschul, SF, Gish, W, Miller, W, Myers, EW, Lipman, DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410PubMedGoogle Scholar
  4. 4.
    Arillo, A, Bavestrello, G, Burlando, B, Sará, M (1993) Metabolic integration between symbiotic cyanobacteria and sponges—a possible mechanism. Mar Biol 117: 159–162CrossRefGoogle Scholar
  5. 5.
    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: 1731–1737PubMedGoogle Scholar
  6. 6.
    Brinig, MM, Lepp, PW, Ouverney, CC, Armitage, GC, Relman, DA (2003) Prevalence of bacteria of division TM7 in human subgingival plaque and their association with disease. Appl Environ Microbiol 69: 1687–1694PubMedCrossRefGoogle Scholar
  7. 7.
    Brümmer, F, Calcinai, B, Götz, M, Leitermann, F, Nickel, M, Schillak, L, Sidri, M, Zucht, W (2004) Overview on the sponge fauna of the Limski kanal, Croatia, Northern Adriatic Sea. Boll Musei Institut Biol (Genova) 68: 219–227Google Scholar
  8. 8.
    Burja, AM, Hill, RT (2001) Microbial symbionts of the Australian Great Barrier Reef sponge, Candidaspongia flabellata. Hydrobiologia 461: 41–47CrossRefGoogle Scholar
  9. 9.
    Carballo, JL, Gomez, P, Cruz-Barraza, JA, Flores-Sanchez, DM (2003) Sponges of the family Chondrillidae (Porifera: Demospongiae) from the Pacific coast of Mexico, with the description of three new species. P Biol Soc Wash 116: 515–527Google Scholar
  10. 10.
    Cho, JC, Giovannoni, SJ (2004) Cultivation and growth characteristics of a diverse group of oligotrophic marine Gammaproteobacteria. Appl Environ Microbiol 70: 432–440PubMedCrossRefGoogle Scholar
  11. 11.
    Clarke, KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18: 117–143CrossRefGoogle Scholar
  12. 12.
    Clarke, KR, Gorley, RN (2001) PRIMER v5: User manual/tutorial, PRIMER-E. Plymouth UK, 91Google Scholar
  13. 13.
    Clarke, KR, Warwick, RM (1994) Similarity-based testing for community pattern—the 2-way layout with no replication. Mar Biol 118: 167–176CrossRefGoogle Scholar
  14. 14.
    Donachie, SP, Hou, S, Lee, KS, Riley, CW, Pikina, A, Belisle, C, Kempe, S, Gregory, TS, Bossuyt, A, Boerema, J, Liu, J, Freitas, TA, Malahoff, A, Alam, M (2004) The Hawaiian Archipelago: A microbial diversity hotspot. Microb Ecol 48: 509–520PubMedCrossRefGoogle Scholar
  15. 15.
    Felsenstein, J (1981) Evolutionary trees from DNA-sequences—a maximum-likelihood approach. J Mol Evol 17: 368–376PubMedCrossRefGoogle Scholar
  16. 16.
    Ferrari, BC, Binnerup, SJ, Gillings, M (2005) Microcolony cultivation on a soil substrate membrane system selects for previously uncultured soil bacteria. Appl Environ Microbiol 71: 8714–8720PubMedCrossRefGoogle Scholar
  17. 17.
    Fuchs BM, Woebken D, Zubkov MV, Burkill, P, Amann, R (2005) Molecular identification of picoplankton populations in contrasting waters of the Arabian Sea. Aquat Microb Ecol 39: 145–157Google Scholar
  18. 18.
    Gaino, E, Pansini, M, Pronzato, R (1977) Aspects of association between Chondrilla nucula Schmidt (Demonspongiae) and its symbiotic extracellular microorganisms (Bacteria and Cyanophyceae) in natural and experimental conditions. Cah Biol Mar 18: 303–310Google Scholar
  19. 19.
    Guindon, S, Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704PubMedCrossRefGoogle Scholar
  20. 20.
    Guindon, S, Lethiec, F, Duroux, P, Gascuel, O (2005) PHYML Online—a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33: W557–W559PubMedCrossRefGoogle Scholar
  21. 21.
    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
  22. 22.
    Hentschel, U, Usher, KM, Taylor, MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55: 167–177PubMedCrossRefGoogle Scholar
  23. 23.
    Hill, M, Hill, A, Lopez, N, Harriott, O (2006) Sponge-specific bacterial symbionts in the Caribbean sponge, Chondrilla nucula (Demospongiae, Chondrosida). Mar Biol 148: 1221–1230CrossRefGoogle Scholar
  24. 24.
    Holmes, B, Blanch, H (2006) Genus-specific associations of marine sponges with group I crenarchaeotes. Mar Biol 1–14Google Scholar
  25. 25.
    Hooper, NJA, van Soest, RWM (2002) Systema Porifera: a guide to the classification of sponges. Kluwer/Plenum, New York, 1707Google Scholar
  26. 26.
    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
  27. 27.
    Hugenholtz, P, Tyson, GW, Webb, RI, Wagner, AM, Blackall, LL (2001) Investigation of candidate division TM7, a recently recognized major lineage of the domain bacteria with no known pure-culture representatives. Appl Environ Microbiol 67: 411–419PubMedCrossRefGoogle Scholar
  28. 28.
    Jurkevitch, E (2000) The genus Bdellovibrio. In Dworkin, M, Flakow, S, Rosenberg, E, Schleifer, KH, Stackebrandt, E (Eds.) The Prokaryotes, vol. online, Springer, New York, http://141.150.157.117:8080/prokPUB/chaprender/jsp/showchap.jsp?chapnum=8327
  29. 29.
    Klautau, M, Russo, CAM, Lazoski, C, Boury-Esnault, N, Thorpe, JP, Sole-Cava, AM (1999) Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution 53: 1414–1422CrossRefGoogle Scholar
  30. 30.
    Kunzmann, K (1996) Associated fauna of selected sponges (Hexactinellida and Demospongiae) from the Weddel Sea, Antarctica. Alfred-Wegener-Institut für Polar- und MeeresforschungGoogle Scholar
  31. 31.
    Kuzmanovic (1985) Preliminarna istrazivanja dinamike vodenih masa Limskog Kanala (Zavrsni Izvjestaj). Rep. “Institut Ruder Boskovic,” Rovinj, CroatiaGoogle Scholar
  32. 32.
    Lane, DL (1991) 16S/23S rRNA sequencing. In Stackebrandt, E, Goodfellow, M (Eds.) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  33. 33.
    Lopez-Garcia, P, Duperron, S, Philippot, P, Foriel, J, Susini, J, Moreira, D (2003) Bacterial diversity in hydrothermal sediment and epsilonproteobacterial dominance in experimental microcolonizers at the Mid-Atlantic Ridge. Environ Microbiol 5: 961–976PubMedCrossRefGoogle Scholar
  34. 34.
    Ludwig, W, Strunk, O, Westram, R, Richter, L, Meier, H, Yadhukumar, Buchner, A, Lai, T, Steppi, S, Jobb, G, Forster, W, Brettske, I, Gerber, S, Ginhart, AW, Gross, O, Grumann, S, Hermann, S, Jost, R, Konig, A, Liss, T, Lussmann, R, May, M, Nonhoff, B, Reichel, B, Strehlow, R, Stamatakis, A, Stuckmann, N, Vilbig, A, Lenke, M, Ludwig, T, Bode, A, Schleifer, KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363–1371PubMedCrossRefGoogle Scholar
  35. 35.
    Maidak, BL, Cole, JR, Parker, CT, Garrity, GM, Larsen, N, Li, B, Lilburn, TG, McCaughey, MJ, Olsen, GJ, Overbeek, R, Pramanik, S, Schmidt, TM, Tiedje, JM, Woese, CR (1999) A new version of the RDP (Ribosomal Database Project). Nucleic Acids Res 27: 171–173PubMedCrossRefGoogle Scholar
  36. 36.
    Maldonado, M, Cortadellas, N, Trillas, MI, Rutzler, K (2005) Endosymbiotic yeast maternally transmitted in a marine sponge. Biol Bull 209: 94–106PubMedCrossRefGoogle Scholar
  37. 37.
    Millot, C (1999) Circulation in the Western Mediterranean Sea. J Mar Syst 20: 423–442CrossRefGoogle Scholar
  38. 38.
    Müller, WEG, Zahn, RK, Kurelec, B, Müller, I (1984) A catalogue of the sponges near Rovinj. Thalassia Jugoslavika 20: 13–23Google Scholar
  39. 39.
    Muyzer, G, Dewaal, EC, Uitterlinden, AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S ribosomal-RNA. Appl Environ Microbiol 59: 695–700PubMedGoogle Scholar
  40. 40.
    Novosel, M, Bakran-Petricioli, T, Pozar-Domac, A, Kruzic, P, Radic, I (2002) The benthos of the northern part of the Velebit Channel (Adriatic Sea, Croatia). Nat Croat 11: 387–409Google Scholar
  41. 41.
    Olson, JB, McCarthy, PJ (2005) Associated bacterial communities of two deep-water sponges. Aquat Microb Ecol 39: 47–55Google Scholar
  42. 42.
    Petri, R, Imhoff, JF (2001) Genetic analysis of sea-ice bacterial communities of the Western Baltic Sea using an improved double gradient method. Polar Biol 24: 252–257CrossRefGoogle Scholar
  43. 43.
    Quaiser, A, Ochsenreiter, T, Lanz, C, Schuster, SC, Treusch, AH, Eck, J, Schleper, C (2003) Acidobacteria form a coherent but highly diverse group within the bacterial domain: evidence from environmental genomics. Mol Microbiol 50: 563–575PubMedCrossRefGoogle Scholar
  44. 44.
    Reiswig, HM (1973) Water transport, respiration and energetics of 3 tropical marine sponges. J Exp Mar Biol Ecol 14: 231–249CrossRefGoogle Scholar
  45. 45.
    Ridley, CP, Faulkner, DJ, Haygood, MG (2005) Investigation of Oscillatoria spongeliae-dominated bacterial communities in four dictyoceratid sponges. Appl Environ Microbiol 71: 7366–7375PubMedCrossRefGoogle Scholar
  46. 46.
    Schirmer, A, Gadkari, R, Reeves, CD, Ibrahim, F, DeLong, EF, Hutchinson, CR (2005) Metagenomic analysis reveals diverse polyketide synthase gene clusters in microorganisms associated with the marine sponge Discodermia dissoluta. Appl Environ Microbiol 71: 4840–4849PubMedCrossRefGoogle Scholar
  47. 47.
    Schmidt, O (1862) Die Spongien des Adriatischen Meeres. Verlag Wilhelm Engelmann, Leipzig, 88Google Scholar
  48. 48.
    Taylor, MW, Schupp, PJ, Dahllof, I, Kjelleberg, S, Steinberg, PD (2004) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6: 121–130PubMedCrossRefGoogle Scholar
  49. 49.
    Thiel, V, Neulinger, SC, Staufenberger, T, Schmaljohann, R, Imhoff, JF (2007) Spatial distribution of sponge-associated bacteria in the marine sponge Tethya aurantium. FEMS Microbiol Ecol 59(1): 47–63PubMedCrossRefGoogle Scholar
  50. 50.
    Usher, KM, Fromont, J, Sutton, DC, Toze, S (2004) The biogeography and phylogeny of unicellular cyanobacterial symbionts in sponges from Australia and the Mediterranean. Microb Ecol 48: 167–177PubMedCrossRefGoogle Scholar
  51. 51.
    Usher, KM, Kuo, J, Fromont, J, Sutton, DC (2001) Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461: 9–13CrossRefGoogle Scholar
  52. 52.
    Usher, KM, Sutton, DC, Toze, S, Kuo, J, Fromont, J (2004) Biogeography and phylogeny of Chondrilla species (Demospongiae) in Australia. Mar Ecol Prog Ser 270: 117–127Google Scholar
  53. 53.
    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
  54. 54.
    Vacelet, J (1971) Étude en microscopie électronique de l’association entre une cyanophycée chroococcale et une éponge du genre Verongia. J Microsc (Paris) 12: 363–380Google Scholar
  55. 55.
    Vacelet, J, Donadey, C (1977) Electron microscope study of the association between some sponges and bacteria. J Exp Mar Biol Ecol 30: 301–314CrossRefGoogle Scholar
  56. 56.
    Webster, NS, Hill, RT (2001) The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by an alpha-Proteobacterium. Mar Biol 138: 843–851CrossRefGoogle Scholar
  57. 57.
    Webster, NS, Webb, RI, Ridd, MJ, Hill, RT, Negri, AP (2001) The effects of copper on the microbial community of a coral reef sponge. Environ Microbiol 3: 19–31PubMedCrossRefGoogle Scholar
  58. 58.
    Webster, NS, Wilson, KJ, Blackall, LL, Hill, RT (2001) Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol 67: 434–444PubMedCrossRefGoogle Scholar
  59. 59.
    Wilkinson, CR (1979) Bdellovibrio-like parasite of cyanobacteria symbiotic in marine sponges. Arch Microbiol 123: 101–103CrossRefGoogle Scholar
  60. 60.
    Wilkinson, CR (1978) Microbial associations in sponges. I. Ecology, physiology and microbal populations of reef sponges. Mar Biol 49: 161–167CrossRefGoogle Scholar
  61. 61.
    Wilkinson, CR (1978) Microbial associations in sponges. II. Numerical analysis of sponge and water bacterial population. Mar Biol 49: 169–176CrossRefGoogle Scholar
  62. 62.
    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

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Vera Thiel
    • 1
  • Sven Leininger
    • 2
  • Rolf Schmaljohann
    • 1
  • Franz Brümmer
    • 2
  • Johannes F. Imhoff
    • 1
  1. 1.Leibniz-Institut für Meereswissenschaften, IFM-GEOMARKielGermany
  2. 2.Biologisches InstitutUniversität StuttgartStuttgartGermany
  3. 3.Department of BiologyUniversity of BergenBergenNorway

Personalised recommendations