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

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Abstract

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.

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References

  • 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:https://doi.org/10.1007/s002270050273

    Article  Google Scholar 

  • Bergquist P, Kelly M (2004) Taxonomy of some halisarcida and homosclerophorida (Porifera: demospongiae) from the Indo-Pacific. N Z J Mar Freshw Res 38:51–66

    Article  Google Scholar 

  • 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:https://doi.org/10.1080/00222939200770131

    Article  Google Scholar 

  • Boury-Esnault N, Muricy G, Gallissian M-F, Vacelet J (1995) Sponges without skeleton: a new Mediterranean genus of Homoscleromorpha (Porifera, Demospongiae). Ophelia 43:25–43

    Article  Google Scholar 

  • de Caralt S, Uriz MJ, Ereskovsky AV, Wijffels RH (2007) Embryo development of Corticium candelabrum (Demospongiae: Homosclerophorida). Invertebr Biol 126:211–219. doi:https://doi.org/10.1111/j.1744-7410.2007.00091.x

    Article  Google Scholar 

  • Ereskovsky AV (2006) A new species of Oscarella (Demospongiae: plakinidae) from the western sea of Japan. Zootaxa 1376:37–51

    Google Scholar 

  • 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:https://doi.org/10.1080/00222930110069050

    Article  Google Scholar 

  • 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: 88–94

  • 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:https://doi.org/10.1002/bies.080058

    Article  Google Scholar 

  • 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:https://doi.org/10.1007/s00227-002-0785-x

    Article  Google Scholar 

  • 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:https://doi.org/10.1128/AEM.70.6.3724-3732.2004

    Article  CAS  Google Scholar 

  • Fuerst JA (2005) Intracellular compartmentation in Planctomycetes. Annu Rev Microbiol 59:299–328. doi:https://doi.org/10.1146/annurev.micro.59.030804.121258

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1111/j.1574-6968.1998.tb13179.x

    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. doi:https://doi.org/10.1111/j.1574-6941.2001.tb00816.x

    Article  CAS  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. doi:https://doi.org/10.1128/AEM.68.9.4431-4440.2002

    Article  CAS  Google Scholar 

  • Hentschel U, Uscher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177. doi:https://doi.org/10.1111/j.1574-6941.2005.00046.x

    Article  CAS  Google Scholar 

  • 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 35–56

    Google Scholar 

  • 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 44:329–341

    Google Scholar 

  • 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:https://doi.org/10.1007/s00227-001-0740-2

    Article  CAS  Google Scholar 

  • Muricy G (1999) An evaluation of morphological and cytological data sets for the phylogeny of Homosclerophorida (Porifera: Demospongiae). Mem Qld Mus 44:399–409

    Google Scholar 

  • 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 71–82

    Google Scholar 

  • Muricy J, Pearse JS (2004) New Species of Oscarella (Demospongiae: Plakinidae) from California. Proc Calif Acad Sci 55:598–612

    Google Scholar 

  • 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:https://doi.org/10.1139/z96-102

    Article  Google Scholar 

  • 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:https://doi.org/10.1080/002229399300353

    Article  Google Scholar 

  • 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:https://doi.org/10.1073/pnas.93.13.6241

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1071/MF06052

    Article  Google Scholar 

  • Sarà M, Bavestrello G, Cattaneo-Vietti R, Cerrano C (1998) Endosymbiosis in Sponges—Relevance for Epigenesis and Evolution. Symbiosis 25:57–70

    Google Scholar 

  • Schmitt S, Wehrl M, Bayer K, Siegl A, Hentschel U (2007) Marine sponges as models for commensal microbe–host interactions. Symbiosis 44:43–50

    Google Scholar 

  • 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:https://doi.org/10.1046/j.1462-2920.2003.00545.x

    Article  Google Scholar 

  • 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:https://doi.org/10.1128/MMBR.00040-06

    Article  CAS  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. doi:https://doi.org/10.1016/0022-0981(77)90038-7

    Article  Google Scholar 

  • 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:https://doi.org/10.1007/s10126-001-0065-7

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1007/s00227-007-0708-y

    Article  CAS  Google Scholar 

  • Wilkinson CR (1984) Immunological evidence for the Precambrian origin of bacterial symbiosis in marine sponges. Proc R Soc Lond B Biol Sci 220:509–517

    Article  Google Scholar 

Download references

Acknowledgments

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).

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Authors and Affiliations

  1. Department of Invertebrate Zoology, Biological Faculty, St. Petersburg State University, 7/9 Universitetskaya nab, 199034, St. Petersburg, Russia

    Andrey E. Vishnyakov & Alexander V. Ereskovsky

  2. Centre d’Océanologie de Marseille, Station marine d’Endoume, Aix-Marseille Université, CNRS UMR 6540-DIMAR, rue de la Batterie des Lions, 13007, Marseille, France

    Alexander V. Ereskovsky

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  1. Andrey E. Vishnyakov
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Correspondence to Andrey E. Vishnyakov.

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Communicated by Ulrich Sommer.

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Vishnyakov, A.E., Ereskovsky, A.V. Bacterial symbionts as an additional cytological marker for identification of sponges without a skeleton. Mar Biol 156, 1625–1632 (2009). https://doi.org/10.1007/s00227-009-1198-x

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