Marine Biotechnology

, Volume 9, Issue 5, pp 543–549 | Cite as

Differential Gene Expression in a Marine Sponge in Relation to Its Symbiotic State

  • Laura SteindlerEmail author
  • Silvia Schuster
  • Micha Ilan
  • Adi Avni
  • Carlo Cerrano
  • Sven Beer
Short Communication


The molecular mechanisms involved in the establishment and maintenance of sponge photosymbiosis, and in particular the association with cyanobacteria, are unknown. In the present study we analyzed gene expression in a common Mediterranean sponge (Petrosia ficiformis) in relation to its symbiotic (with cyanobacteria) or aposymbiotic status. A screening approach was applied to identify genes expressed differentially in symbiotic specimens growing in the light and aposymbiotic specimens growing in a dark cave at a short distance from the illuminated specimens. Out of the various differentially expressed sequences, we isolated two novel genes (here named PfSym1 and PfSym2) that were up-regulated when cyanobacterial symbionts were harbored inside the sponge cells. The sequence of one of these genes (PfSym2) was found to contain a conserved domain: the scavenger receptor cysteine rich (SRCR) domain. This is the first report on the expression of sponge genes in relation to symbiosis and, according to the presence of an SRCR domain, we suggest possible functions for one of the genes found in the sponge-cyanobacteria symbiosis.


cyanobacteria differential gene expression sponge suppression subtractive hybridization symbiosis 



This work was supported by grant 2000-321 from the United States–Israel Binational Science Foundation (BSF) to M.I. and S.B. L.S. received a scholarship from the Rieger Foundation for Environmental Studies that assisted in the travel costs for sampling sponge specimens.


  1. 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 panacea: harbor also for putatively-toxic bacteria? Mar Biol 130, 529–536CrossRefGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Limpan DJ (1990) Basic local alignment search tool. J Mol Biol 215, 403–410PubMedGoogle Scholar
  3. Arillo A, Bavestrello G, Burlando B, Sarà M (1993) Metabolic integration between symbiotic cyanobacteria and sponges—a possible mechanism. Mar Biol 117, 159–162CrossRefGoogle Scholar
  4. Blumbach B, Pancer Z, Diehl-Seifert B, Steffen R, Münkner J, Müller I, Müller WEG (1998) The putative sponge aggregation receptor: isolation and characterization of a molecule composed of scavenger receptor cysteine-rich domains and short consensus repeats. J Cell Sci 111, 2635–2644PubMedGoogle Scholar
  5. Dangott L, Jordan JE, Bellet RA, Garbers DL (1989) Cloning of the mRNA for the protein that crosslinks to the egg peptide speract. Proc Natl Acad Sci USA 86, 2128–2132PubMedCrossRefGoogle Scholar
  6. Davidson SK, Koropatnick TA, Kossmehl R, Sycuro L, McFall-Ngai MJ (2004) NO means ‘yes’ in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol 6, 1139–1151PubMedCrossRefGoogle Scholar
  7. Feldmann J (1933) Sur Quelques cyanophycées vivant dans le tissu des éponges de banyules. Arch Zool Exp Gén 75, 331–404Google Scholar
  8. Grant AJ, Trautman DA, Menz I, Hinde R (2006) Separation of two cell signaling molecules from a symbiotic sponge that modify algal carbon metabolism. Biochem Biophys Res Commun 348, 92–98PubMedCrossRefGoogle Scholar
  9. 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
  10. Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters.FEMS Microbiol Ecol 55, 167–177PubMedCrossRefGoogle Scholar
  11. Kimbell JR, McFall-Ngai MJ (2004) Symbiont-induced changes in host actin during the onset of a beneficial animal-bacterial association. Appl Environ Microbiol 70, 1434–1441PubMedCrossRefGoogle Scholar
  12. Lauckner G (1980) “Diseases in porifera.” In: Diseases of Marine Animals, Kinne O, ed. (Chichester: John Wiley & Sons)Google Scholar
  13. Olson JB, Gochfeld DJ, Slattery M (2006) Aplysina red band syndrome: a new threat to Caribbean sponges. Dis Aquat Organ 71, 163–168PubMedCrossRefGoogle Scholar
  14. Pancer Z, Münkner J, Müller I, Müller WEG (1997) A novel member of an ancient superfamily: sponge Geodia cydonium, (Porifera) putative protein that features scavenger receptor cysteine-rich repeats. Gene 193, 211–218PubMedCrossRefGoogle Scholar
  15. Perović-Ottstadt S, Adell T, Proksch P, Wiens M, Korzhev M, Gamulin V, Müller IM, Müller WEG (2004) A (1→3)-β-d-glucan recognition protein from the sponge Suberites domuncula. Eur J Biochem 271, 1924–1937PubMedCrossRefGoogle Scholar
  16. Preston CM, Wu KY, Molinski TF, De Long EF (1996) A psychrophilic crenarchaeon inhabits a maine sponge: Crenarchaeum symbiosum gen. nov. sp. nov. Proc Natl Acad Sci USA 93, 6241–6246PubMedCrossRefGoogle Scholar
  17. Regoli F, Cerrano C, Chierici E, Bompadre S, Bavastrello G (2000) Susceptibility to oxidative stress of the Mediterranean demosponge Petrosia ficiformis: role of endosymbionts and solar irradiance. Mar Biol 137, 453–461CrossRefGoogle Scholar
  18. Resnick D, Pearson A, Krieger M (1994) The SRCR superfamily: a family reminiscent of the Ig superfamily. Trends Biochem Sci 19, 5–8PubMedCrossRefGoogle Scholar
  19. Reynolds WS, Schwarz JA, Weis VM (2000) Symbiosis-enhanced gene expression in cnidarian-algal associations: cloning and characterization of a cDNA, sym32, encoding a possible cell adhesion protein. Comp Biochem Physiol A Mol Integr Physiol 126, 33–44PubMedCrossRefGoogle Scholar
  20. Riley J, Butler R, Ogilvie D, Finniear R, Jenner D, Powell S, Anand R, Smith JC, Markham AF (1990) A novel, rapid method for the isolation of terminal sequences from yeast artificial chromosome (YAC) clones. Nucleic Acids Res 18, 2887–2890PubMedCrossRefGoogle Scholar
  21. Rodriguez-Lanetty M, Phillips WS, Weis VM (2006) Transcriptome analysis of a cnidarian—dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics 7, 23PubMedCrossRefGoogle Scholar
  22. Rützler K (1990) “Associations between Caribbean sponges and photosynthetic organisms.” In: New Perspectives in Sponge Biology, Rützler K, ed. (Washington, DC: Smithsonian Institution Press) pp 455–466Google Scholar
  23. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning, A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory)Google Scholar
  24. Sanger F (1981) Determination of nucleotide sequence in DNA. Science 214, 1205–1210PubMedCrossRefGoogle Scholar
  25. Sarà M, Vacelet J (1973) “Ecologie de démosponges.” In: Traité de Zoologie. Anatomie Systematiqui, Biologie, Grassé PP, ed. (Paris: Masson) pp 462–576Google Scholar
  26. Sarà M, Bavastrello G, Cattaneo-Vietti R, Cerrano C (1998) Endosymbiosis in sponges: relevance for epigenesist and evolution. Symbiosis 25, 57–70Google Scholar
  27. Schwarz JA, Weis VM (2003) Localization of a symbiosis-related protein, Sym32, in the Anthopleura elegantissima-Symbiodinium muscatinei association. Biol Bull 205, 339–350PubMedCrossRefGoogle Scholar
  28. Steindler L, Huchon D, Avni A, Ilan M (2005) 16S rRNA phylogeny of sponge-associated cyanobacteria. Appl Environ Microbiol 71, 4127–4131PubMedCrossRefGoogle Scholar
  29. Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W—improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680PubMedCrossRefGoogle Scholar
  30. 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
  31. Vacelet J, Donadey C (1977) Electron microscope study of the association between some sponges and cyanobacteria. J Exp Mar Biol Ecol 30, 301–314CrossRefGoogle Scholar
  32. Vacelet J, Vacelet E, Gaino E, Gallissian MF (1994) “Bacterial attack of spongin skeleton during the 1986–1990 Mediterranean sponge disease.” In: Sponges in Time and Space, Van Soest RWM, Van Kempen TMG, Braekman JC, eds. (Rotterdam: Balkema) pp 355–362Google Scholar
  33. Visick KL, McFall-Ngai MJ (2000) An exclusive contract: specificity in the Vibrio fischeri-Euprymna scolopes partnership. J Bacteriol 182, 1779–1787PubMedCrossRefGoogle Scholar
  34. Wiens M, Korzhev M, Perović-Ottstadt S, Luthringer B, Brandt D, Klein S, Müller WEG (2007) Toll-like receptors are part of the innate immune defense system of sponges (Demospongiae: Porifera). Mol Biol Evol 24, 792–804PubMedCrossRefGoogle Scholar
  35. Wilkinson CR (1983) Phylogeny of bacterial and cyanobacterial symbionts in marine sponges. Endocytobiology 2, 993–1002Google Scholar
  36. Wilkinson CR (1992) “Symbiotic interactions between marine sponges and algae.” In: Algae and Symbiosis: Plants, Animals, Fungi, Viruses. Interactions Explored, Reisser W, ed. (London: Biopress) pp 112–151Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Laura Steindler
    • 1
    • 2
    Email author
  • Silvia Schuster
    • 1
  • Micha Ilan
    • 2
  • Adi Avni
    • 1
  • Carlo Cerrano
    • 3
  • Sven Beer
    • 1
  1. 1.Department of Plant Sciences, George S. Wise Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael
  2. 2.Department of Zoology, George S. Wise Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael
  3. 3.Dipartimento per lo Studio del Territorio e delle sue RisorseUniversity of GenovaGenovaItaly

Personalised recommendations