Marine Biology

, Volume 156, Issue 8, pp 1625–1632 | Cite as

Bacterial symbionts as an additional cytological marker for identification of sponges without a skeleton

  • Andrey E. VishnyakovEmail author
  • Alexander V. Ereskovsky
Original Paper


Symbiotic bacteria from six Oscarella species (adults and embryos) collected in the Mediterranean Sea (O. lobularis, O. tuberculata, O. imperialis, O. microlobata, O. viridis) and the Sea of Japan (O. malakhovi) were investigated by scanning electron microscopy and transmission electron microscopy. In most cases, symbionts are rather numerous. Each sponge species has a definite set of bacterial morphological types. All bacteria are extracellular. Symbionts occupy the mesohyl of adult sponges or intercellular space in embryos and are often in contact with mesohylar filaments or cells. Bacteria of some morphotypes have characteristic blebs. Most symbionts are gram-negative, and two types of bacteria have traits of Archaea and one type of bacteria is similar to Planctomycetes. Data on morphology of bacterial symbionts can be a good additional character for identification of Oscarella species, which have no skeleton.


Sponge Archaea Symbiotic Bacterium Sponge Species Bacterial Symbiont 
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 authors are grateful to Chantal Bézac, Centre d’Océanologie de Marseille, France and Daria Tokina, Zoological Institute RAS, St. Petersburg, Russia, for technical assistance, Thierry Perez, Roland Graille and Pierre Chevaldonné for diving assistance. Financial support for this work was provided by grants RFBR NN 07-04-01097, 06-04-48660 and European Marie Curie Mobility program (fellowship of A. Ereskovsky, MIF1-CT-2006-040065).


  1. Althoff K, Schuett 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 (Berl) 130:529–536. doi: CrossRefGoogle Scholar
  2. Bergquist P, Kelly M (2004) Taxonomy of some halisarcida and homosclerophorida (Porifera: demospongiae) from the Indo-Pacific. N Z J Mar Freshw Res 38:51–66CrossRefGoogle Scholar
  3. Boury-Esnault N, Sol-Cava AM, Thorpe JP (1992) Genetic and cytological divergence between colour morphs of the Mediterranean sponge Oscarella lobularis Schmidt (Porifera, Demospongiae, Oscarellidae). J Nat Hist 26:271–284. doi: CrossRefGoogle Scholar
  4. Boury-Esnault N, Muricy G, Gallissian M-F, Vacelet J (1995) Sponges without skeleton: a new Mediterranean genus of Homoscleromorpha (Porifera, Demospongiae). Ophelia 43:25–43CrossRefGoogle Scholar
  5. de Caralt S, Uriz MJ, Ereskovsky AV, Wijffels RH (2007) Embryo development of Corticium candelabrum (Demospongiae: Homosclerophorida). Invertebr Biol 126:211–219. doi: CrossRefGoogle Scholar
  6. Ereskovsky AV (2006) A new species of Oscarella (Demospongiae: plakinidae) from the western sea of Japan. Zootaxa 1376:37–51Google Scholar
  7. Ereskovsky AV, Boury-Esnault N (2002) Cleavage pattern in Oscarella species (Porifera, Demospongiae, Homoscleromorpha): transmission of maternal cells and symbiotic bacteria. J Nat Hist 36:1761–1775. doi: CrossRefGoogle Scholar
  8. Ereskovsky AV, Ivanisevic J, Pérez T (2009a) Overview on the Homoscleromorpha sponges diversity in the Mediterranean. In Proc. of the First Mediterranean Symposium on the Coralligenous and other calcareous bio-concretions. Okianos, Tunisia, Tabarka: 88–94Google Scholar
  9. Ereskovsky AV, Borchiellini C, Gazave E, Ivanisevic J, Lapebie P, Pérez T, Renard E, Vacelet J (2009b) The Homoscleromorph sponge Oscarella lobularis, a promising sponge model in evolutionary and developmental biology. Bioessays 31:89–97. doi: CrossRefGoogle Scholar
  10. Erpenbeck D, Breeuwer JAJ, van der Velde HC, van Soest RWM (2002) Unravelling host and symbiont phylogenies of halichondrid sponges (Demospongiae, Porifera) using a mitochondrial marker. Mar Biol (Berl) 141:377–386. doi: CrossRefGoogle Scholar
  11. Fieseler L, Horn M, Wagner M, Hentschel U (2004) Discovery of the novel candidate phylum “Poribacteria” in marine sponges. Appl Environ Microbiol 70:3724–3732. doi: CrossRefGoogle Scholar
  12. Fuerst JA (2005) Intracellular compartmentation in Planctomycetes. Annu Rev Microbiol 59:299–328. doi: CrossRefGoogle Scholar
  13. Fuerst JA, Webb RI, Garson MJ, Hardy L, Reiswig HM (1998) Membrane-bounded nucleoids in microbial symbionts of marine sponges. FEMS Microbiol Lett 166:29–34. doi: CrossRefGoogle Scholar
  14. 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. doi: CrossRefGoogle Scholar
  15. 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. doi: CrossRefGoogle Scholar
  16. Hentschel U, Uscher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177. doi: CrossRefGoogle Scholar
  17. Imhoff JF, Stöhr R (2003) Sponge-associated bacteria: General overview and special aspects of bacteria associated with Halichondria panicea. In: Müller WEG (ed) Molecular Marine Biology of Sponges. Springer, Heidelberg, pp 35–56Google Scholar
  18. Lopez JV, McCarthy PJ, Janda KE, Willoughby R, Pomponi SA (1999) Molecular techniques reveal wide phyletic diversity of heterotrophic microbes associated with Discodermia spp. (Porifera: Demospongiae). Mem Qld Mus 44:329–341Google Scholar
  19. 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 (Berl) 140:739–745. doi: CrossRefGoogle Scholar
  20. Muricy G (1999) An evaluation of morphological and cytological data sets for the phylogeny of Homosclerophorida (Porifera: Demospongiae). Mem Qld Mus 44:399–409Google Scholar
  21. Muricy G, Diaz MC (2002) Order Homosclerophorida Dendy, 1905. Family Plakinidae Schulze, 1880. In: Hooper JAN, van Soest RWM (eds) Systema porifera. A guide to the classification of sponges, vol 1. Kluwer, NY, pp 71–82Google Scholar
  22. Muricy J, Pearse JS (2004) New Species of Oscarella (Demospongiae: Plakinidae) from California. Proc Calif Acad Sci 55:598–612Google Scholar
  23. Muricy G, Boury-Esnault N, Bezac C, Vacelet J (1996) Cytological evidence for cryptic speciation in Mediterranean Oscarella species (Porifera, Homoscleromorpha). Can J Zool 74:881–896. doi: CrossRefGoogle Scholar
  24. Muricy G, Bézac C, Gallissian M-F, Boury-Esnault N (1999) Anatomy, cytology and symbiotic bacteria of four Mediterranean species of Plakina Schulze, 1880 (Demospongiae, Homosclerophorida). J Nat Hist 33:159–176. doi: CrossRefGoogle Scholar
  25. 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 93:6241–6246. doi: CrossRefGoogle Scholar
  26. Riesgo A, Maldonado M, Durfort M (2007) Dynamics of gametogenesis, embryogenesis, and larval release in a Mediterranean homosclerophorid demosponge. Mar Freshw Res 58:398–417. doi: CrossRefGoogle Scholar
  27. Sarà M, Bavestrello G, Cattaneo-Vietti R, Cerrano C (1998) Endosymbiosis in Sponges—Relevance for Epigenesis and Evolution. Symbiosis 25:57–70Google Scholar
  28. Schmitt S, Wehrl M, Bayer K, Siegl A, Hentschel U (2007) Marine sponges as models for commensal microbe–host interactions. Symbiosis 44:43–50Google Scholar
  29. Taylor MW, Schupp PJ, Dahllöf I, Kjelleberg S, Steinberg PD (2004) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6:121–130. doi: CrossRefGoogle Scholar
  30. Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential. Microbiol Mol Biol Rev 71:295–347. doi: CrossRefGoogle Scholar
  31. Vacelet J, Donadey C (1977) Electron microscope study of the association between some sponges and bacteria. J Exp Mar Biol Ecol 30:301–314. doi: CrossRefGoogle Scholar
  32. Webster NS, Watts JE, Hill RT (2001) Detection and phylogenetic analysis of novel crenarchaeote and euryarchaeote 16S ribosomal RNA gene sequences from a Great Barrier Reef sponge. Mar Biotechnol 3:600–608. doi: CrossRefGoogle Scholar
  33. Weisz JB, Hentschel U, Lindquist N, Martens CS (2007) Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Mar Biol (Berl) 152:475–483. doi: CrossRefGoogle Scholar
  34. Wilkinson CR (1984) Immunological evidence for the Precambrian origin of bacterial symbiosis in marine sponges. Proc R Soc Lond B Biol Sci 220:509–517CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Andrey E. Vishnyakov
    • 1
    Email author
  • Alexander V. Ereskovsky
    • 1
    • 2
  1. 1.Department of Invertebrate Zoology, Biological FacultySt. Petersburg State UniversitySt. PetersburgRussia
  2. 2.Centre d’Océanologie de Marseille, Station marine d’EndoumeAix-Marseille Université, CNRS UMR 6540-DIMARMarseilleFrance

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