Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Genomic insights into the marine sponge microbiome

Nature Reviews Microbiology volume 10, pages 641–654 (2012)Cite this article

Subjects

Key Points

  • Many marine sponges (phylum Porifera), the most ancient of the metazoan animals, contain dense and diverse microbial communities.

  • Members of ∼30 bacterial phyla and several archaeal lineages have been reported to contribute to the enormous microbial diversity in marine sponges. The symbiotic microbial consortia are located extracellularly in the mesohyl matrix. Transmission to the next generation occurs vertically through the reproductive stages, but horizontal transmission might also be possible. The mechanisms by which microbial diversity in sponges is shaped and maintained throughout the sponge life cycle, as well as through evolutionary time, are the subject of much current debate.

  • The metabolic capabilities of sponge-associated microorganisms are becoming increasingly well understood, largely as a result of metagenomic, metaproteogenomic and single-cell genomics studies. Furthermore, several putative symbiosis factors, such as proteins that contain eukaryotic domains (that is, ankyrin repeats, tetratrico peptide repeats and leucine-rich repeats), have been identified.

  • The genome of the sponge Amphimedon queenslandica provides new insights into metazoan evolution and also adds a new angle to investigating the mechanisms of sponge–microorganism interactions. Of particular interest are the pattern recognition receptors of the innate immune system, which recognize microbial ligands.

  • Metagenomic and single-cell genomics approaches are promising for the field of marine drug development, as they provide biotechnological access to pharmacologically important host- and symbiont-derived compounds.

  • Sponges represent an important and tractable model system for the study of metazoan evolution, host–microorganism interactions and chemical diversity.

Abstract

Marine sponges (phylum Porifera) often contain dense and diverse microbial communities, which can constitute up to 35% of the sponge biomass. The genome of one sponge, Amphimedon queenslandica, was recently sequenced, and this has provided new insights into the origins of animal evolution. Complementary efforts to sequence the genomes of uncultivated sponge symbionts have yielded the first glimpse of how these intimate partnerships are formed. The remarkable microbial and chemical diversity of the sponge–microorganism association, coupled with its postulated antiquity, makes sponges important model systems for the study of metazoan host–microorganism interactions, and their evolution, as well as for enabling access to biotechnologically important symbiont-derived natural products. In this Review, we discuss our current understanding of the interactions between marine sponges and their microbial symbiotic consortia, and highlight recent insights into these relationships from genomic studies.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Body plan and underwater images of marine sponges.
Figure 2: Diversity and specificity of marine sponge-associated microorganisms.
Figure 3: Pattern recognition receptors encoded by the Amphimedon queenslandica genome, in comparison to their human equivalents.

Similar content being viewed by others

References

  1. Bell, J. J. The functional roles of marine sponges. Estuar. Coast. Shelf Sci. 79, 341–353 (2008).

    Article  Google Scholar 

  2. Dayton, P. K. Interdecadal variation in an antarctic sponge and its predators from oceanographic climate shifts. Science 245, 1484–1486 (1989).

    Article  CAS  PubMed  Google Scholar 

  3. Bell, J. J. & Smith, D. Ecology of sponge assemblages (Porifera) in the Wakatobi region, south-east Sulawesi, Indonesia: richness and abundance. J. Mar. Biol. Assoc. UK 84, 581–591 (2004).

    Article  Google Scholar 

  4. Brusca, R. C. & Brusca, G. J. Invertebrates 2nd edn (Sinauer Associates, 2003).

    Google Scholar 

  5. Pawlik, J. R. The chemical ecology of sponges on Caribbean reefs: natural products shape natural systems. Bioscience 61, 888–898 (2011).

    Article  Google Scholar 

  6. Li, C. W., Chen, J. Y. & Hua, T. E. Precambrian sponges with cellular structures. Science 279, 879–882 (1998).

    Article  CAS  PubMed  Google Scholar 

  7. Love, G. D. et al. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457, 718–721 (2009).

    Article  CAS  PubMed  Google Scholar 

  8. Taylor, M. W., Radax, R., Steger, D. & Wagner, M. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 71, 295–347 (2007). An excellent, comprehensive review of sponge microbiology.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Vacelet, J. & Donadey, C. Electron microscope study of the association between some sponges and bacteria. J. Exp. Mar. Biol. Ecol. 30, 301–314 (1977).

    Article  Google Scholar 

  10. Wilkinson, C. R., Garrone, R. & Vacelet, J. Marine sponges discriminate between food bacteria and bacterial symbionts: electron microscope radioautography and in situ evidence. Proc. R. Soc. Lond. B 220, 519–528 (1984). An early paper in sponge microbiology that is noteworthy for its thought-provoking hypotheses, which are stimulating contemporary discussions.

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  12. Müller, W. E. G. & Müller, I. M. Origin of the metazoan immune system: identification of the molecules and their functions in sponges. Integr. Comp. Biol. 43, 281–292 (2003).

    Article  PubMed  Google Scholar 

  13. Wiens, M. et al. Toll-like receptors are part of the innate immune defense system of sponges (Demospongiae: Porifera). Mol. Biol. Evol. 24, 792–804 (2007).

    Article  CAS  PubMed  Google Scholar 

  14. Srivastava, M. et al. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466, 720–726 (2010). The first, and still only, complete genome from a sponge reveals that most gene families which are characteristic of true animals, including humans, were already present in the last common ancestor of all animals.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Gauthier, E. A., Du Pasquier, L. & Degnan, B. M. The genome of the sponge Amphimedon queenslandica provides new perspectives into the origin of Toll-like and interleukin 1 receptor pathways. Evol. Dev. 12, 519–533 (2010).

    Article  CAS  PubMed  Google Scholar 

  16. Blunt, J. W., Copp, B. R., Munro, M. H. G., Northcote, P. T. & Prinsep, M. R. Marine natural products. Nat. Prod. Rep. 28, 196–268 (2011).

    Article  CAS  PubMed  Google Scholar 

  17. Piel, J. Bacterial symbionts: prospects for the sustainable production of invertebrate-derived pharmaceuticals. Curr. Med. Chem. 13, 39–50 (2006).

    Article  CAS  PubMed  Google Scholar 

  18. Sipkema, D. et al. Multiple approaches to enhance the cultivability of bacteria associated with the marine sponge Haliclona (gellius) sp. Appl. Environ. Microbiol. 77, 2130–2140 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bright, M. & Bulgheresi, S. A complex journey: transmission of microbial symbionts. Nature Rev. Microbiol. 8, 218–230 (2010).

    Article  CAS  Google Scholar 

  20. Wilson, A. C. et al. Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol. Biol. 19, 249–258 (2010).

    Article  CAS  PubMed  Google Scholar 

  21. Dale, C. & Moran, N. A. Molecular interactions between bacterial symbionts and their hosts. Cell 126, 453–465 (2006).

    Article  CAS  PubMed  Google Scholar 

  22. Nyholm, S. V. & McFall-Ngai, M. J. The winnowing: establishing the squid–Vibrio symbiosis. Nature Rev. Microbiol. 2, 632–642 (2004). A brilliant example of the intricate interactions that can evolve between animal host and bacterial symbiont.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Webster, N. S. & Taylor, M. W. Marine sponges and their microbial symbionts: love and other relationships. Environ. Microbiol. 14, 335–346 (2012).

    Article  CAS  PubMed  Google Scholar 

  25. Won, Y.-J., Jones, W. J. & Vrijenhoek, R. C. Absence of cospeciation between deep-sea mytilids and their thiotrophic endosymbionts. J. Shellfish Res. 27, 129–138 (2008).

    Article  Google Scholar 

  26. Usher, K. M. & Ereskovsky, A. V. Larval development, ultrastructure and metamorphosis in Chondrilla australiensis Carter, 1873 (Demospongiae, Chondrosida, Chondrillidae). Invertebr. Reprod. Dev. 47, 51–62 (2005).

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Sharp, K. H., Eam, B., Faulkner, D. J. & Haygood, M. G. Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl. Environ. Microbiol. 73, 622–629 (2007).

    Article  CAS  PubMed  Google Scholar 

  29. Lee, O. O., Chui, P. Y., Wong, Y. H., Pawlik, J. R. & Qian, P. Y. Evidence for vertical transmission of bacterial symbionts from adult to embryo in the Caribbean sponge Svenzea zeai. Appl. Environ. Microbiol. 75, 6147–6156 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Webster, N. S. et al. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ. Microbiol. 12, 2070–2082 (2010). The first study to apply 16S rRNA gene pyrosequencing to sponge bacteria, revealing the high degree of overlap between bacterial communities in adult and larval sponges.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Hentschel, U. et al. Molecular evidence for a uniform microbial community in sponges from different oceans. Appl. Environ. Microbiol. 68, 4431–4440 (2002). The first molecular (16S rRNA gene) study to identify monophyletic sponge-specific clusters of bacteria.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Simister, R. L., Deines, P., Botte, E. S., Webster, N. S. & Taylor, M. W. Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environ. Microbiol. 14, 517–524 (2012).

    Article  CAS  PubMed  Google Scholar 

  33. Wilkinson, C. R. Immunological evidence for the Precambrian origin of bacterial symbioses in marine sponges. Proc. R. Soc. Lond. B 220, 509–517 (1984).

    Article  Google Scholar 

  34. Taylor, M. W., Thacker, R. W. & Hentschel, U. Genetics: evolutionary insights from sponges. Science 316, 1854–1855 (2007).

    Article  CAS  PubMed  Google Scholar 

  35. Lee, O. O. et al. Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. ISME J. 5, 650–664 (2011).

    Article  CAS  PubMed  Google Scholar 

  36. Schmitt, S. et al. Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J. 6, 564–576 (2012). An investigation that uses 16S rRNA gene pyrosequencing to describe the biogeography and host specificity of bacteria in 32 sponge species from eight worldwide locations.

    Article  CAS  PubMed  Google Scholar 

  37. Siegl, A. et al. Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J. 5, 61–70 (2011). The first study to apply single-cell techniques to investigate the genomes of uncultivated bacterial symbionts of sponges.

    Article  PubMed  Google Scholar 

  38. Fieseler, L., Horn, M., Wagner, M. & Hentschel, U. Discovery of the novel candidate phylum “Poribacteria” in marine sponges. Appl. Environ. Microbiol. 70, 3724–3732 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Preston, C. M., Wu, K. Y., Molinski, T. F. & DeLong, E. F. A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc. Natl Acad. Sci. USA 93, 6241–6246 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Pape, T. et al. Dense populations of Archaea associated with the demosponge Tentorium semisuberites Schmidt, 1870 from Arctic deep-waters. Polar Biol. 29, 662–667 (2006).

    Article  Google Scholar 

  41. Radax, R., Hoffmann, F., Rapp, H. T., Leininger, S. & Schleper, C. Ammonia-oxidizing archaea as main drivers of nitrification in cold-water sponges. Environ. Microbiol. 14, 909–923 (2012).

    Article  CAS  PubMed  Google Scholar 

  42. Wilkinson, C. R. in Algae and Symbioses: Plants, Animals, Fungi, Viruses, Interactions Explored (ed. W. Reisser) 111–151 (Biopress Limited, 1992).

    Google Scholar 

  43. Höller, U. et al. Fungi from marine sponges: diversity, biological activity and secondary metabolites. Mycol. Res. 104, 1354–1365 (2000).

    Article  Google Scholar 

  44. Baker, P. W., Kennedy, J., Dobson, A. D. W. & Marchesi, J. R. Phylogenetic diversity and antimicrobial activities of fungi associated with Haliclona simulans isolated from Irish coastal waters. Mar. Biotechnol. 11, 540–547 (2009).

    Article  CAS  Google Scholar 

  45. Quince, C. et al. Accurate determination of microbial diversity from 454 pyrosequencing data. Nature Methods 6, 639–641 (2009).

    Article  CAS  PubMed  Google Scholar 

  46. Kunin, V., Engelbrektson, A., Ochman, H. & Hugenholtz, P. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ. Microbiol. 12, 118–123 (2010).

    Article  CAS  PubMed  Google Scholar 

  47. Sunagawa, S., Woodley, C. M. & Medina, M. Threatened corals provide underexplored microbial habitats. PLoS ONE 5, e9554 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Cardenas, A., Rodriguez, L. M., Pizarro, V., Cadavid, L. F. & Arevalo-Ferro, C. Shifts in bacterial communities of two caribbean reef-building coral species affected by white plague disease. ISME J. 123, 502–512 (2012).

    Article  CAS  Google Scholar 

  49. Behrendt, L. et al. Microbial diversity of biofilm communities in microniches associated with the didemnid ascidian Lissoclinum patella. ISME J. 6, 1222–1237 (2012).

    Article  CAS  PubMed  Google Scholar 

  50. Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R. & Gordon, J. I. Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Rev. Microbiol. 6, 776–888 (2008).

    Article  CAS  Google Scholar 

  51. Dewhirst, F. E. et al. The human oral microbiome. J. Bacteriol. 192, 5002–5017 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Griffen, A. L. et al. Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J. 6, 1176–1185 (2012).

    Article  CAS  PubMed  Google Scholar 

  53. Zoetendal, E. G., Rajilic-Stojanovic, M. & de Vos, W. M. High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut 57, 1605–1615 (2008).

    Article  CAS  PubMed  Google Scholar 

  54. Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647–1651 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Grice, E. A. & Segre, J. A. The skin microbiome. Nature Rev. Microbiol. 9, 244–253 (2011).

    Article  CAS  Google Scholar 

  56. Taylor, M. W., Schupp, P. J., Dahllof, I., Kjelleberg, S. & Steinberg, P. D. Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ. Microbiol. 6, 121–130 (2004).

    Article  PubMed  Google Scholar 

  57. Wiedenbeck, J. & Cohan, F. M. Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol. Rev. 35, 957–976 (2011).

    Article  CAS  PubMed  Google Scholar 

  58. Dobrindt, U., Hochhut, B., Hentschel, U. & Hacker, J. Genomic islands in pathogenic and environmental microorganisms. Nature Rev. Microbiol. 2, 414–424 (2004).

    Article  CAS  Google Scholar 

  59. Sobecky, P. A. & Hazen, T. H. Horizontal gene transfer and mobile genetic elements in marine systems. Methods Mol. Biol. 532, 435–453 (2009).

    Article  CAS  PubMed  Google Scholar 

  60. Villareal, L. P. Viruses and the Evolution of Life (American Society for Microbiology Press, 2005).

    Book  Google Scholar 

  61. Suttle, C. A. Marine viruses--major players in the global ecosystem. Nature Rev. Microbiol. 5, 801–812 (2007).

    Article  CAS  Google Scholar 

  62. Claverie, J.-M. et al. Mimivirus and mimiviridae: giant viruses with an increasing number of potential hosts, including corals and sponges. J. Invertebr. Pathol. 101, 172–180 (2009).

    Article  CAS  PubMed  Google Scholar 

  63. Thomas, T. et al. Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J. 4, 1557–1567 (2010). The first metagenomic analysis of sponge microbiota, revealing insights into mechanisms of bacterium–sponge interactions and highlighting ANK-containing proteins as putative symbiosis factors.

    Article  CAS  PubMed  Google Scholar 

  64. Grimson, A. et al. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455, 1193–1197 (2008).

    Article  CAS  PubMed  Google Scholar 

  65. Taylor, M. W., Hill, R. T. & Hentschel, U. Meeting report: first international symposium on sponge microbiology. Mar. Biotechnol. 13, 1057–1061 (2011).

    Article  CAS  Google Scholar 

  66. Hallam, S. J. et al. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl Acad. Sci. USA 103, 18296–18301 (2006). The sequenced genome of C. symbiosum provides many new insights into the metabolic potential of this sponge symbiont.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Hallam, S. J. et al. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol. 4, e95 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Liu, M. Y., Kjelleberg, S. & Thomas, T. Functional genomic analysis of an uncultured δ-proteobacterium in the sponge Cymbastela concentrica. ISME J. 5, 427–435 (2011).

    Article  PubMed  Google Scholar 

  69. Radax, R. et al. Metatranscriptomics of the marine sponge Geodia barretti: tackling phylogeny and function of its microbial community. Environ. Microbiol. 14, 1308–1324 (2012).

    Article  CAS  PubMed  Google Scholar 

  70. Lopez-Legentil, S., Erwin, P. M., Pawlik, J. R. & Song, B. Effects of sponge bleaching on ammonia-oxidizing Archaea: distribution and relative expression of ammonia monooxygenase genes associated with the barrel sponge Xestospongia muta. Microb. Ecol. 60, 561–571 (2010).

    Article  CAS  PubMed  Google Scholar 

  71. Turque, A. S. et al. Environmental shaping of sponge associated archaeal communities. PLoS ONE 5, e15774 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Steger, D. et al. Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environ. Microbiol. 10, 1087–1094 (2008).

    Article  CAS  PubMed  Google Scholar 

  73. Bayer, K., Schmitt, S. & Hentschel, U. Physiology, phylogeny and in situ evidence for bacterial and archaeal nitrifiers in the marine sponge Aplysina aerophoba. Environ. Microbiol. 10, 2942–2955 (2008).

    Article  CAS  PubMed  Google Scholar 

  74. Hoffmann, F. et al. Complex nitrogen cycling in the sponge Geodia barretti. Environ. Microbiol. 11, 2228–2243 (2009).

    Article  CAS  PubMed  Google Scholar 

  75. Liu, M. Y., Fan, L., Zhong, L., Kjelleberg, S. & Thomas, T. Metaproteogenomic analysis of a community of sponge symbionts. ISME J. 6, 1515–1525 (2012). The first proteomic analysis of a sponge-associated microbiota, providing novel information on the activities, physiology and interactions of microorganisms with sponge hosts.

  76. Gill, S. R. et al. Metagenomic analysis of the human distal gut microbiome. Science 312, 1355–1359 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Goodman, A. L. et al. Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 6, 279–289 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Cazalet, C. et al. Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nature Genet. 36, 1165–1173 (2004).

    Article  CAS  PubMed  Google Scholar 

  79. Pan, X., Lührmann, A., Satoh, A., Laskowski-Arce, M. A. & Roy, C. R. Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 320, 1651–1654 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Voth, D. E. ThANKs for the repeat: intracellular pathogens exploit a common eukaryotic domain. Cell. Logist. 1, 128–132 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  81. Schmitz-Esser, S. et al. The genome of the amoeba symbiont “Candidatus Amoebophilus asiaticus” reveals common mechanisms for host cell interaction among amoeba-associated bacteria. J. Bacteriol. 192, 1045–1057 (2010).

    Article  CAS  PubMed  Google Scholar 

  82. Al-Khodor, S., Price, C. T., Kalia, A. & Abu Kwaik, Y. Functional diversity of ankyrin repeats in microbial proteins. Trends Microbiol. 18, 132–139 (2010).

    Article  CAS  PubMed  Google Scholar 

  83. Al-Khodor, S., Price, C. T., Habyarimana, F., Kalia, A. & Abu Kwaik, Y. A. Dot/Icm-translocated ankyrin protein of Legionella pneumophila is required for intracellular proliferation within human macrophages and protozoa. Mol. Microbiol. 70, 908–923 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Price, C. T., Al-Khodor, S., Al-Quadan, T. & Abu Kwaik, Y. Indispensable role for the eukaryotic-like ankyrin domains of the ankyrin B effector of Legionella pneumophila within macrophages and amoebae. Infect. Immun. 78, 2079–2088 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Lührmann, A., Nogueira, C. V., Carey, K. L. & Roy, C. R. Inhibition of pathogen-induced apoptosis by a Coxiella burnetii type IV effector protein. Proc. Natl Acad. Sci. USA 107, 18997–19001 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  86. D'Andrea, L. D. & Regan, L. TPR proteins: the versatile helix. Trends Biochem. Sci. 28, 655–662 (2003).

    Article  CAS  PubMed  Google Scholar 

  87. Mittl, P. R. & Schneider-Brachert, W. Sel1-like repeat proteins in signal transduction. Cell. Signal. 19, 20–31 (2007).

    Article  CAS  PubMed  Google Scholar 

  88. Kataeva, I. A. et al. The fibronectin type 3-like repeat from the Clostridium thermocellum cellobiohydrolase CbhA promotes hydrolysis of cellulose by modifying its surface. Appl. Environ. Microbiol. 68, 4292–4300 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Exposito, J. Y. et al. Demosponge and sea anemone fibrillar collagen diversity reveals the early emergence of A/C clades and the maintenance of the modular structure of type V/XI collagens from sponge to human. J. Biol. Chem. 283, 28226–28235 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Har-el, R. & Tanzer, M. L. Extracellular matrix. 3: evolution of the extracellular matrix in invertebrates. FASEB J. 7, 1115–1123 (1993).

    Article  CAS  PubMed  Google Scholar 

  91. Ozbek, S., Balasubramanian, P. G., Chiquet-Ehrismann, R., Tucker, R. P. & Adams, J. C. The evolution of extracellular matrix. Mol. Biol. Cell 21, 4300–4305 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  92. Fuqua, C. & Greenberg, E. P. Listening in on bacteria: acyl-homoserine lactone signalling. Nature Rev. Mol. Cell Biol. 3, 685–695 (2002).

    Article  CAS  Google Scholar 

  93. Mohamed, N. M. et al. Diversity and quorum-sensing signal production of Proteobacteria associated with marine sponges. Environ. Microbiol. 10, 75–86 (2008).

    Article  CAS  PubMed  Google Scholar 

  94. Zan, J., Fricke, W. F., Fuqua, C., Ravel, J. & Hill, R. T. Genome sequence of Ruegeria sp. strain KLH11, an N-acylhomoserine lactone-producing bacterium isolated from the marine sponge Mycale laxissima. J. Bacteriol. 193, 5011–5012 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Zan, J., Fuqua, C. & Hill, R. T. Diversity and functional analysis of luxS genes in vibrios from marine sponges Mycale laxissima and Ircinia strobilina. ISME J. 5, 1505–1516 (2011). A report on quorum sensing, the presence of luxS genes and autoinducer 2 activity in sponge-associated bacterial communities.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Taylor, M. W. et al. Evidence for acyl homoserine lactone signal production in bacteria associated with marine sponges. Appl. Environ. Microbiol. 70, 4387–4389 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Hughes, D. T. & Sperandio, V. Inter-kingdom signalling: communication between bacteria and their hosts. Nature Rev. Microbiol. 6, 111–120 (2008). A summary of recently acquired evidence that bacterial quorum sensing signalling can also be used in crosstalk between microorganisms and their hosts.

    Article  CAS  Google Scholar 

  98. Webster, N. S. Sponge disease: a global threat? Environ. Microbiol. 9, 1363–1375 (2007).

    Article  CAS  PubMed  Google Scholar 

  99. Wilson, H. V. On some phenomena of coalescence and regeneration in sponges. J. Exp. Zool. 5, 245–258 (1907).

    Article  Google Scholar 

  100. Gordon, S. Pattern recognition receptors: doubling up for the innate immune response. Cell 111, 927–930 (2002).

    Article  CAS  PubMed  Google Scholar 

  101. Janeway, C. A. & Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 20, 197–216 (2002).

    Article  CAS  PubMed  Google Scholar 

  102. Liu, L. et al. Structural basis of toll-like receptor 3 signaling with double-stranded RNA. Science 320, 379–381 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Dunne, A. & O'Neill, L. A. The Interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense. Sci. STKE 2003, re3 (2003).

  104. Påisson-McDermott, E. M. & O'Neill, L. A. J. Building an immune system from nine domains. Biochem. Soc. Trans. 35, 1437–1444 (2007).

    Article  Google Scholar 

  105. Bosch, T. C. G. et al. Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence. Dev. Comp. Immunol. 33, 559–569 (2009).

    Article  CAS  PubMed  Google Scholar 

  106. Franchi, L., Eigenbrod, T., Munoz-Planillo, R. & Nunez, G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nature Immunol. 10, 241–247 (2009).

    Article  CAS  Google Scholar 

  107. Elinav, E., Strowig, T., Henao-Mejia, J. & Flavell, R. A. Regulation of the antimicrobial response by NLR proteins. Immunity 34, 665–679 (2011).

    Article  CAS  PubMed  Google Scholar 

  108. Monie, T. P., C. E., B. & Gay, N. J. Activating immunity: lessons from the TLRs and NLRs. Trends Biochem. Sci. 34, 553–561 (2009).

    Article  CAS  PubMed  Google Scholar 

  109. Seong, S. & Matzinger, P. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nature Rev. Immunol. 4, 469–478 (2004).

    Article  CAS  Google Scholar 

  110. Sarrias, M. R. et al. The Scavenger Receptor Cysteine-Rich (SRCR) domain: an ancient and highly conserved protein module of the innate immune system. Crit. Rev. Immunol. 24, 1–37 (2004).

    Article  CAS  PubMed  Google Scholar 

  111. Plüddemann, A. et al. SR-A, MARCO and TLRs differentially recognise selected surface proteins from Neisseria meningitidis: an example of fine specificity in microbial ligand recognition by innate immune receptors. Innate Immun. 1, 153–163 (2009).

    Article  CAS  Google Scholar 

  112. Pahler, S., Blumbach, B., Muller, I. & Muller, W. E. Putative multiadhesive protein from the marine sponge Geodia cydonium: cloning of the cDNA encoding a fibronectin-, an SRCR-, and a complement control protein module. J. Exp. Zool. 282, 332–343 (1998).

    Article  CAS  PubMed  Google Scholar 

  113. Pancer, Z., Münker, J., Müller, I. M. & Müller, W. E. G. A novel member of an ancient superfamily: sponge (Geodia cydonium, Porifera) putative protein that features scavenger receptor cysteine-rich repeats. Gene 193, 211–218 (1997).

    Article  CAS  PubMed  Google Scholar 

  114. Steindler, L. et al. Differential gene expression in a marine sponge in relation to its symbiotic state. Mar. Biotechnol. 9, 543–549 (2007).

    Article  CAS  Google Scholar 

  115. Huyck, T. K., Gradishar, W., Manuguid, F. & Kirkpatrick, P. Eribulin mesylate. Nature Rev. Drug Discov. 10, 173–174 (2011).

    Article  CAS  Google Scholar 

  116. Aicher, T. D. et al. Total synthesis of halichondrin B and norhalichondrin B. J. Am. Chem. Soc. 114, 3162–3164 (1992).

    Article  CAS  Google Scholar 

  117. Munro, M. G. H. et al. The discovery and development of marine compounds with pharmaceutical potential. J. Biotechnol. 70, 15–25 (1999).

    Article  CAS  PubMed  Google Scholar 

  118. Bewley, C. A. & Faulkner, D. J. Lithistid sponges: star performers or hosts to the stars. Angew. Chem. Int. Ed. Engl. 37, 2163–2178 (1998).

    Article  CAS  Google Scholar 

  119. Faulkner, D. J., Unson, M. D. & Bewley, C. A. The chemistry of some sponges and their symbionts. Pure Appl. Chem. 66, 1983–1990 (1994).

    Article  CAS  Google Scholar 

  120. Unson, M. D. & Faulkner, D. J. Cyanobacterial symbiont biosynthesis of chlorinated metabolites from Dysidea herbacea (Porifera). Experientia 49, 349–353 (1993). The first convincing experimental evidence that sponge-derived natural products can be of bacterial origin.

    Article  CAS  Google Scholar 

  121. Unson, M. D., Holland, N. D. & Faulkner, D. J. A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue. Mar. Biol. 119, 1–11 (1994).

    Article  CAS  Google Scholar 

  122. Schmidt, E. W., Obraztsova, A. Y., Davidson, S. K., Faulkner, D. J. & Haygood, M. G. Identification of the antifungal peptide-containing symbiont of the marine sponge Theonella swinhoei as a novel δ-proteobacterium, “Candidatus Entotheonella palauensis”. Mar. Biol. 136, 969–977 (2000).

    Article  CAS  Google Scholar 

  123. Bewley, C. A., Holland, N. D. & Faulkner, D. J. Two classes of metabolites from Theonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia 52, 716–722 (1996).

    Article  CAS  PubMed  Google Scholar 

  124. Gillor, O., Carmeli, S., Rahamim, Y., Fishelson, Z. & Ilan, M. Immunolocalization of the toxin latrunculin B within the Red Sea sponge Negombata magnifica (Demospongiae, Latrunculiidae). Mar. Biotechnol. 2, 213–223 (2000).

    Article  CAS  Google Scholar 

  125. Fischbach, M. A. & Walsh, C. T. Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic, machinery, and mechanisms. Chem. Rev. 106, 3468–3496 (2006).

    Article  CAS  PubMed  Google Scholar 

  126. Fisch, K. M. et al. Polyketide assembly lines of uncultivated sponge symbionts from structure-based gene targeting. Nature Chem. Biol. 5, 494–501 (2009). A report of a strategy that allows the identification of biosynthetic-gene clusters from microbial metagenomes on the basis of chemical moieties in the compounds produced by the microbial community. Using this strategy, the complete pathway for psymberin is recovered from the sponge P. bulbosa.

    Article  CAS  Google Scholar 

  127. Piel, J. et al. Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei. Proc. Natl Acad. Sci. USA 101, 16222–16227 (2004). An investigation that provides unambiguous evidence for the bacterial production of a potent antitumor compound from the sponge T. swinhoei.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Piel, J. Biosynthesis of polyketides by trans-AT polyketide synthases. Nat. Prod. Rep. 27, 996–1047 (2010).

    Article  CAS  PubMed  Google Scholar 

  129. Piel, J. A polyketide synthase-peptide synthetase gene cluster from an uncultured bacterial symbiont of Paederus beetles. Proc. Natl Acad. Sci. USA 99, 14002–14007 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Sudek, S. et al. Identification of the putative bryostatin polyketide synthase gene cluster from “Candidatus Endobugula sertula”, the uncultivated microbial symbiont of the marine bryozoan Bugula neritina. J. Nat. Prod. 70, 67–74 (2007).

    Article  CAS  PubMed  Google Scholar 

  131. Partida-Martinez, L. P. & Hertweck, C. Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437, 884–888 (2005).

    Article  CAS  PubMed  Google Scholar 

  132. Partida-Martinez, L. P. & Hertweck, C. A gene cluster encoding rhizoxin biosynthesis in “Burkholderia rhizoxina”, the bacterial endosymbiont of the fungus Rhizopus microsporus. Chembiochem 8, 41–45 (2007).

    Article  CAS  PubMed  Google Scholar 

  133. Donia, M. S. et al. Complex microbiome underlying secondary and primary metabolism in the tunicate- Prochloron symbiosis. Proc. Natl Acad. Sci. USA 108, e1423–e1432 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  134. Nguyen, T. et al. Exploiting the mosaic structure of trans-acyltransferase polyketide synthases for natural product discovery and pathway dissection. Nature Biotech. 26, 225–233 (2008).

    Article  CAS  Google Scholar 

  135. Flatt, P. M. et al. Identification of the cellular site of polychlorinated peptide biosynthesis in the marine sponge Dysidea (Lamellodysidea) herbacea and symbiotic cyanobacterium Oscillatoria spongeliae by CARD-FISH analysis. Mar. Biol. 147, 761–774 (2005).

    Article  CAS  Google Scholar 

  136. Lasken, R. S. Single-cell genomic sequencing using multiple displacement amplification. Curr. Opin. Microbiol. 10, 510–516 (2007).

    Article  CAS  PubMed  Google Scholar 

  137. Wang, D. J. & Bodovitz, S. Single cell analysis: the new frontier in 'omics'. Trends Biotechnol. 28, 281–290 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Siegl, A. & Hentschel, U. PKS and NRPS gene clusters from microbial symbiont cells of marine sponges by whole genome amplification. Environ. Microbiol. Rep. 2, 507–513 (2010).

    Article  CAS  PubMed  Google Scholar 

  139. Grindberg, R. V. et al. Single cell genome amplification accelerates identification of the apratoxin biosynthetic pathway from a complex microbial assemblage. PLoS ONE 6, e18565 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Engene, N. et al. Underestimated biodiversity as a major explanation for the perceived rich secondary metabolite capacity of the cyanobacterial genus Lyngbya. Environ. Microbiol. 13, 1601–1610 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Intergovernmental Panel on Climate Change. Fourth Assessment Report of the Intergovernmental Panel on Climate Change (Geneva, 2007).

  142. Lemoine, N., Buell, N., Hill, A. & Hill, M. in Porifera Research: Biodiversity, Innovation and Sustainability (eds M.R. Custódio, G. Lôbo-Hajdu, E. Hajdu, & G. Muricy) 419–425 (Série Livros, 2007).

    Google Scholar 

  143. Webster, N. S., Cobb, R. E. & Negri, A. P. Temperature thresholds for bacterial symbiosis with a sponge. ISME J. 2, 830–842 (2008).

    Article  CAS  PubMed  Google Scholar 

  144. Lopez-Legentil, S., Song, B., McMurray, S. E. & Pawlik, J. R. Bleaching and stress in coral reef ecosystems: hsp70 expression by the giant barrel sponge Xestospongia muta. Mol. Ecol. 17, 1840–1849 (2008).

    Article  CAS  PubMed  Google Scholar 

  145. Pantile, R. & Webster, N. Strict thermal threshold identified by quantitative PCR in the sponge Rhopaloeides odorabile. Mar. Ecol. Prog. Ser. 431, 97–105 (2011).

    Article  CAS  Google Scholar 

  146. Luter, H. M., Whalan, S. & Webster, N. S. Exploring the role of microorganisms in the disease-like syndrome affecting the sponge Ianthella basta. Appl. Environ. Microbiol. 76, 5736–5744 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Angermeier, H. et al. The pathology of sponge orange band disease affecting the Caribbean barrel sponge Xestospongia muta. FEMS Microb. Ecol. 75, 218–230 (2011).

    Article  CAS  Google Scholar 

  148. Webster, N. S., Negri, A. P., Webb, R. I. & Hill, R. T. A spongin-boring α-proteobacterium is the etiological agent of disease in the Great Barrier Reef sponge, Rhopaloeides odorabile. Mar. Ecol. Prog. Ser. 232, 305–309 (2002).

    Article  Google Scholar 

  149. Reiswig, H. M. Particle feeding in natural populations of three marine demosponges. Biol. Bull. 141, 568–591 (1971).

    Article  Google Scholar 

  150. Reiswig, H. M. Bacteria as food for temperate-water marine sponges. Can. J. Zool. 53, 582–589 (1975).

    Article  Google Scholar 

  151. Pile, A. J., Patterson, M. R. & Witman, J. D. In situ grazing on plankton <10μm by the boreal sponge Mycale lingua. Mar. Ecol. Prog. Ser. 141, 95–102 (1996).

    Article  Google Scholar 

  152. Hadas, E., Marie, D., Shpigel, M. & Ilan, M. Virus predation by sponges is a new nutrient-flow pathway in coral reef food webs. Limnol. Oceanogr. 51, 1548–1550 (2006).

    Article  Google Scholar 

  153. Maritz, K., Calcino, A., Fahey, B., Degnan, B. & Degnan, S. M. Remarkable consistency of larval supply in the spermcast-mating demosponge Amphimedon queenslandica (Hooper and van Soest). Open Mar. Biol. J. 4, 57–64 (2010).

    Article  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the valuable contributions of all current and past members of their respective research groups. They are grateful to the participants of the First International Symposium on Sponge Microbiology (Würzburg, Germany, March 2011), for inspiring discussions and insights into many aspects of sponge microbiology. The pioneering efforts of early sponge microbiologists such as H. Reiswig, J. Vacelet and C. Wilkinson are also acknowledged. Funding for sponge and microbiology research in the authors' laboratories was provided by the German Research Foundation (DFG) grants SFB567/TPC3 and SFB630/TPA5 (to U.H.); by the DFG, the German Federal Ministry of Education and Research (BMBF), the Japan Society for the Promotion of Sciences, the German Academic Exchange Service (DAAD), the Human Frontier Science Program, the Max Planck Society (MPG) and the German Alexander von Humboldt Foundation (to J.P.); by the Australian Research Council and the University of Queensland (to S.M.D.); and by the University of Auckland (to M.W.T.).

Author information

Authors and Affiliations

  1. Julius-von-Sachs-Institute for Biological Sciences, University of Würzburg, Julius-von-Sachs Platz 3, Würzburg, 97082, Germany

    Ute Hentschel

  2. Kekulé Institute of Organic Chemistry and Biochemistry, University of Bonn, Gerhard-Domagk Straße 1, Bonn, 53121, Germany

    Jörn Piel

  3. School of Biological Sciences, University of Queensland, Brisbane, 4072, Queensland, Australia

    Sandie M. Degnan

  4. Centre for Microbial Innovation, School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand

    Michael W. Taylor

Authors
  1. Ute Hentschel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jörn Piel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sandie M. Degnan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael W. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ute Hentschel.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Ute Hentschel's homepage

Glossary

Benthic

Pertaining to organisms: living in or on the sea floor.

Slime capsules

Extracellular masking layers that encapsulate bacterial cells, putatively shielding the cells from detection by a host (in the context of this Review, the sponge).

Biologically active

Exhibiting activity in a biological assay (for example, a screen for antitumour agents).

Aposymbiotic

Pertaining to an organism: lacking its symbionts.

16S rRNA gene library

A vector library created by the amplification and cloning of the 16S rRNA genes in a population. The library can be used for subsequent sequencing and phylogenetic analysis, as a method of describing the composition of a microbial community.

Pyrosequencing

A next-generation sequencing method based on the detection of pyrophosphate release on nucleotide incorporation. The technique allows thousands or millions of sequences to be obtained from a given sample.

Rare biosphere

The low-abundance microorganisms that are found in a microbial community.

Operational taxonomic units

(OTUs). An arbitrary definition for a specific taxonomic grouping; for example, 97% 16S rRNA sequence similarity is frequently used to approximate a bacterial species.

Phylotype

A sequence type; analogous to an operational taxonomic unit.

Holobiont

A host animal and all of its associated microorganisms.

CRISPRs

(Clustered regularly interspaced short palindromic repeats). Short repeats that are found in the genomes of many bacteria and archaea, and provide resistance to genetic elements such as viruses and plasmids.

Heterotrophic

Pertaining to an organism: requiring dissolved organic matter for its carbon and energy sources.

Autotrophic

Pertaining to an organism: growing on carbon dioxide as the sole carbon source.

Ankyrin repeats

(ANKs). Common eukaryotic structural protein motifs that occur in functionally diverse proteins and mediate protein–protein interactions.

Tetratrico peptide repeats

Common structural protein motifs that mediate protein–protein interactions and are frequently involved in the assembly of multiprotein complexes.

Leucine-rich repeats

Structural protein motifs that are unusually rich in the hydrophobic amino acid leucine and are involved in the formation of protein–protein interactions.

Quorum sensing

A chemical language by which bacteria communicate in and across populations through the use of small diffusible molecules. Bacterial production of quorum sensing molecules, as well as the bacterial response to these molecules, is correlated with population density.

Lipopolysaccharide

A large endotoxic molecule consisting of a lipid and a polysaccharide; the major component of the outer membrane of Gram-negative bacteria. LPS induces a strong immune response in animals.

Eumetazoans

The 'true' animals, as defined by having a nervous system and true tissues; this group includes cnidarians, ctenophores and bilaterians.

Bilaterian

An animal that has three germ layers (endoderm, mesoderm and ectoderm) and bilateral symmetry; this group includes all animals except for sponges, ctenophores and cnidarians.

Danger-associated molecular patterns

(DAMPS). Molecules that are released by stressed or damaged cells and act as endogenous signals to initiate a non-infectious repair (or inflammatory) response. Also called damage-associated molecular patterns.

Complement system

The part of the vertebrate innate immune system that complements the activity of antibodies by opsonizing bacteria and inducing inflammatory responses which help to fight infection. Several complement-like components have also been identified in many invertebrates.

Secondary metabolites

Metabolites that are not essential for the survival of the organism in which they are found (unlike primary metabolites, such as fatty acids, amino acids, and so on, which are essential).

Epibionts

Organisms that live on the surface of another living organism.

Polyketides

Secondary metabolites that are biosynthesized from short acyl-CoA units and often exhibit potent bioactivities. Examples are erythromycin and tetracycline.

Non-ribosomal peptides

Peptides that are assembled by large multifunctional enzymes (termed non-ribosomal-peptide synthetases) and often contain non-proteinogenic amino acids. Many of these compounds (for example, cyclosporine and daptomycin) are of biomedical relevance.

CARD–FISH

(Catalysed reporter deposition–fluorescence in situ hybridization). A technique that uses horseradish peroxidase-labelled oligonucleotide probes to obtain signals in samples with low-abundance targets. The signal is generated after incubation with fluorescently labelled tyramine, which is deposited at the labelling site by enzymatic polymerization.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hentschel, U., Piel, J., Degnan, S. et al. Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10, 641–654 (2012). https://doi.org/10.1038/nrmicro2839

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro2839

This article is cited by

Search

Advanced search

Quick links

Nature Briefing: Translational Research

Sign up for the Nature Briefing: Translational Research newsletter — top stories in biotechnology, drug discovery and pharma.

Get what matters in translational research, free to your inbox weekly. Sign up for Nature Briefing: Translational Research