Skip to main content
Log in

Ectyoplasia ferox, an Experimentally Tractable Model for Vertical Microbial Transmission in Marine Sponges

  • Invertebrate Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The oviparous sponge Ectyoplasia ferox is commonly found in Florida and the Bahamas. Every year in August and/or September about 6 days after a full moon, E. ferox will shed embryo-containing spawning material into the seawater from which hundreds to thousands of larvae will hatch per host individual. In order to investigate vertical microbial transmission in E. ferox, 16S rRNA gene library construction and denaturing gradient gel electrophoresis was employed. Microbial symbionts from six phyla and the unknown lineage SAUL were shown to be vertically transmitted. The identification of 21 VT clusters, of which 19 were situated within sponge-specific or sponge-coral-specific clusters, indicated that a large fraction of the symbiotic microbial consortium was present in the sexual reproductive stages. Spawning led to a 50 % reduction of microbial numbers in the adult sponge mesohyl. We furthermore provide the first evidence that the symbiotic microbial consortia of E. ferox were generally metabolically active within the reproductive stages. Finally, we propose E. ferox as a model system for vertical transmission owing to the ease of experimental access to all sexual reproductive stages, and to experimental tractability in the laboratory including the possibility of rearing symbiont-free juvenile sponges.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  2. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2006) At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71:7724–7736

    Article  Google Scholar 

  3. Brusca RC, Brusca GJ (1990) Phylum Porifera: the sponges. In: Sinauer AD (ed) Invertebrates. Sinauer, Sunderland, pp 181–210

    Google Scholar 

  4. Cytryn E, van Rijn J, Schramm A, Gieseke A, de Beer D, Dror M (2005) Identification of bacteria potentially responsible for oxic and anoxic sulfide oxidation in biofilters of a recirculating mariculture system. Appl Environ Microbiol 71(10):6134–6141

    Article  PubMed  CAS  Google Scholar 

  5. DeCaralt S, Uriz MJ, Wijffels RH (2007) Vertical transmission and successive location of symbiotic bacteria during embryo development and larva formation in Corticium candelabrum (Porifera: Demospongiae). J Mar Biol Ass UK 87:1693–1699

    Google Scholar 

  6. Enticknap JJ, Kelly M, Peraud O, Hill RT (2006) Characterization of a culturable alphaproteobacterial symbiont common to many marine sponges and evidence for vertical transmission via sponge larvae. Appl Environ Microbiol 72:3724–3732

    Article  PubMed  CAS  Google Scholar 

  7. Ereskovsky AV (2010) The comparative embryology of sponges. Springer, Heidelberg

    Book  Google Scholar 

  8. 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

    Article  Google Scholar 

  9. Ereskovsky AV, Gonobobleva E, Vishnyakov A (2005) Morphological evidence for vertical transmission of symbiotic bacteria in the viviparous sponge Halisarca dujardini Johnston (Porifera, Demospongiae, Halisarca). Mar Biol 146:869–875

    Article  Google Scholar 

  10. Ereskovsky AV, Tokina D (2004) Morphology and fine structure of the swimming larvae of Ircinia oros (Porifera, Demospongiae, Dictyoceratida). Invertebr Reprod Dev 45:137–150

    Article  Google Scholar 

  11. Ereskovsky AV, Willenz P (2008) Larval development in Guancha arnesenae (Porifera, Calcispongiae, Calcinea). Zoomorphology 127:175–187

    Article  Google Scholar 

  12. Erwin PM, López-Legentil S, González-Pech R, Turon X (2012) A specific mix of generalists: bacterial symbionts in Mediterranean Ircinia spp. FEMS Microbiol Ecol 79(3):619–637

    Article  PubMed  CAS  Google Scholar 

  13. 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

    Article  PubMed  CAS  Google Scholar 

  14. Friedrich AB, Hacker J, Fischer I, Proksch P, Hentschel U (2001) Temporal variations of the microbial community associated with the Mediterranean sponge Aplysina aerophoba. FEMS Microbiol Ecol 38:105–113

    Article  CAS  Google Scholar 

  15. Giles E, Kamke J, Moitinho-Silva L, Taylor M, Hentschel U, Ravasi T, Schmitt S Bacterial community profiles in low microbial abundance sponges. FEMS Microbiol Ecol. doi:10.1111/j.1574-6941.2012.01467.x

  16. Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J, Horn M (2003) Microbial diversity of marine sponges. In: Müller WEG (ed) Molecular marine biology of sponges. Springer, Heidelberg, pp 60–88

    Google Scholar 

  17. 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

    Article  PubMed  CAS  Google Scholar 

  18. Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10(9):641–654

    Article  PubMed  CAS  Google Scholar 

  19. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model. Nat Rev Microbiol 5(8):619–633

    Article  PubMed  CAS  Google Scholar 

  20. Kamke J, Taylor MW, Schmitt S (2010) Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons. ISME 4(4):498–508

    Article  CAS  Google Scholar 

  21. Kaye H (1991) Sexual reproduction in four Caribbean commercial sponges. II. Oogenesis and transfer of bacterial symbionts. Invertebr Reprod Dev 19:13–24

    Article  Google Scholar 

  22. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, London, pp 115–175

    Google Scholar 

  23. Lee OO, Chui PY, Wong YH, Pawlik JR, Qian PY (2009) Evidence for vertical transmission of bacterial symbionts from adult to embryo in the Caribbean sponge Svenzea zeai. Appl Environ Microbiol 75(19):6147–6156

    Article  PubMed  CAS  Google Scholar 

  24. Levi C, Levi P (1976) Embryogenese de Chondrosia reniformis (Nardo), demosponge ovipare, et transmission des bacteries symbiotiques. Ann Sci Nat Zool 18:367–380

    Google Scholar 

  25. Leys SP, Ereskovsky AV (2006) Embryogenesis and larval differentiation in sponges. Canad J Zool 84:262–287

    Article  Google Scholar 

  26. Lindquist N, Bolser R, Laing K (1997) Timing of larval release by two Caribbean demosponges. Mar Ecol Prog Ser 155:309–313

    Article  Google Scholar 

  27. Ludwig W et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  PubMed  CAS  Google Scholar 

  28. Maldonado M (2007) Intergenerational transmission of symbiotic bacteria in oviparous and viviparous demosponges, with emphasis on intracytoplasmically-compartmented bacterial types. J Mar Biol Ass UK 87:1701–1713

    Google Scholar 

  29. Maldonado M (2009) Embryonic development of verongid demosponges supports the independent acquisition of spongin skeletons as an alternative to the siliceous skeleton of sponges. Biol J Linnean Soc 97:427–447

    Article  Google Scholar 

  30. Maldonado M, Riesgo A (2009) Gametogenesis, embryogenesis, and larval features of the oviparous sponge Petrosia ficiformis (Haplosclerida, Demospongiae). Mar Biol 156:2181–2197

    Article  Google Scholar 

  31. Montalvo NF, Hill RT (2011) Sponge-associated bacteria are strictly maintained in two closely related but geographically distant sponge hosts. Appl Environ Microbiol 77(20):7207–7216

    Article  PubMed  CAS  Google Scholar 

  32. Muyzer G, Brinkhoff T, Nübel U, Santegoeds C, Schäfer H, Wawer C (1998) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) Molecular microbial ecology, manual 3.4.4. Kluwer, Dordrecht

    Google Scholar 

  33. Nyholm SV, Stewart JJ, Ruby EG, McFall-Ngai MJ (2009) Recognition between symbiotic Vibrio fischeri and the haemocytes of Euprymna scolopes. Environ Microbiol 11(2):483–493

    Article  PubMed  Google Scholar 

  34. Oren M, Steindler L, Ilan M (2005) Transmission, plasticity and the molecular identification of cyanobacterial symbionts in the Red Sea sponge Diacarnus erythraenus. Mar Biol 148:35–41

    Article  CAS  Google Scholar 

  35. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Gloeckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196

    Article  PubMed  CAS  Google Scholar 

  36. Rottmann M, Schroeder HC, Gramzow M, Renneisen K, Kurelec B, Dorn A, Friese U, Mueller WE (1987) Specific phosphorylation of proteins in pore complex-laminae from the sponge Geodia cydonium by the homologous aggregation factor and phorbol ester. Role of protein kinase C in the phosphorylation of DNA topoisomerase II. EMBO J 6:3939–3944

    PubMed  CAS  Google Scholar 

  37. Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  38. Schmitt S, Angermeier H, Schiller R, Lindquist N, Hentschel U (2008) Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Appl Environ Microbiol 74(24):7694–7708

    Article  PubMed  CAS  Google Scholar 

  39. Schmitt S, Hentschel U, Taylor MW (2012) Deep sequencing reveals diversity and community structure of complex microbiota in five Mediterranean sponges. Hydrobiologia 687:341–351

    Article  CAS  Google Scholar 

  40. Schmitt S, Tsai P, Bell J, Fromont F, Ilan M, Lindquist NL, Perez T, Rodrigo A, Schupp PJ, Vacelet J, Webster N, Hentschel U, Taylor MW (2012) Assessing the complex sponge microbiota—core, variable, and species-specific bacterial communities in marine sponges. ISME J 6(3):564–576

    Article  PubMed  CAS  Google Scholar 

  41. Schmitt S, Wehrl M, Lindquist N, Weisz JB, Hentschel U (2008b) Morphological and molecular analyses of microorganisms in Caribbean reef adult sponges and in corresponding reproductive material. In: Custódio MR, Lôbo-Hajdu G, Hajdu E, Muricy G (eds) Porifera research biodiversity, innovation and sustainability. Série Livros 28. Museu Nacional, Rio de Janeiro, pp 561–568

  42. Schmitt S, Weisz JB, Lindquist N, Hentschel U (2007) Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Appl Environ Microbiol 73(7):2067–2078

    Article  PubMed  CAS  Google Scholar 

  43. Sciscioli M, Lepore E, Gherardi M, Scalera Liaci L (1994) Transfer of symbiotic bacteria in the mature oocyte of Geodia sydonium (Porifera, Demospongiae): an ultrastructural study. Cah Biol Mar 35:471–478

    Google Scholar 

  44. Sharp KH, Eam B, Faulkner DJ, Haygood MG (2007) Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Environ Microbiol 73:622–629

    Article  PubMed  CAS  Google Scholar 

  45. Steger D, Ettinger-Epstein P, Whalan S, Hentschel U, de Nys R, Wagner M, Taylor MW (2008) Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environ Microbiol 10(4):1087–1094

    Article  PubMed  CAS  Google Scholar 

  46. Steindler L, Huchon D, Avni A, Ilan M (2005) 16S rRNA phylogeny of sponge-associated cyanobacteria. Appl Environ Microbiol 71(7):4127–4131

    Article  PubMed  CAS  Google Scholar 

  47. Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347

    Article  PubMed  CAS  Google Scholar 

  48. Usher K, Ereskovsky AV (2005) Larval development, ultrastructure and metamorphosis in Chondrilla australiensis Carter, 1873 (Demospongiae, Chondrosida, Chondrillidae). Invert Reprod Dev 47:51–62

    Article  Google Scholar 

  49. Usher KM, Kuo J, Fromont J, Sutton DC (2001) Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461:15–23

    Article  Google Scholar 

  50. Vacelet J (1975) Étude en microscopie électronique de l’association entre bactéries et spongiaires du genre Verongia (Dictyoceratida). J Microsc Biol Cell 23:271–288

    Google Scholar 

  51. Webster NS, Taylor MW (2012) Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol 14:335–346

    Article  PubMed  CAS  Google Scholar 

  52. Webster NS, Taylor MW, Behnam F, Lücker S, Rattei T, Whalan S, Horn M, Wagner M (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12(8):2070–2082

    PubMed  CAS  Google Scholar 

  53. Wehrl M, Steinert M, Hentschel U (2007) Bacterial uptake by the marine sponge Aplysina aerophoba. Microb Ecol 53:355–365

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the marine operations personnel of the National Undersea Research Center (NURC) of UNC Wilmington (Key Largo, FL), Hilde Angermeier (University of Würzburg) for excellent support during field work, and Alexander Ereskovsky (CNRS, Marseille, France) for valuable help in interpretation of the microscopic images. Research was supported by German Research Foundation (Deutsche Forschungsgmeinschaft) grant HE3299/1–3 to UH.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Susanne Schmitt or Ute Hentschel.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1

16S rRNA gene sequence-based maximum likelihood tree of Alpha- and Deltaproteobacteria (Supplementary Fig. 1a) and Gammaproteobacteria (Supplementary Fig. 1b). For details, see legend to Fig. 7. (PPTX 147 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gloeckner, V., Lindquist, N., Schmitt, S. et al. Ectyoplasia ferox, an Experimentally Tractable Model for Vertical Microbial Transmission in Marine Sponges. Microb Ecol 65, 462–474 (2013). https://doi.org/10.1007/s00248-012-0142-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-012-0142-7

Keywords

Navigation