Advertisement

Hydrobiologia

, Volume 687, Issue 1, pp 341–351 | Cite as

Deep sequencing reveals diversity and community structure of complex microbiota in five Mediterranean sponges

  • Susanne Schmitt
  • Ute Hentschel
  • Michael W. Taylor
SPONGE RESEARCH DEVELOPMENTS

Abstract

Marine sponges harbor dense microbial communities of exceptionally high diversity. Despite the complexity of sponge microbiota, microbial communities in different sponges seem to be remarkably similar. In this study, we used a subset of a previously established 454 amplicon pyrosequencing dataset (Schmitt and Taylor, unpublished data). Five Mediterranean sponges were chosen including the model sponge Aplysina aerophoba to determine the extent of uniformity by defining (i) the core microbial community, consisting of bacteria found in all sponges, (ii) the variable microbial community, consisting of bacteria found in 2–4 sponges, and (iii) the species-specific community, consisting of bacteria found in only one sponge. Using the enormous sequencing depth of pyrosequencing the diversity in each of the five sponges was extended to up to 15 different bacterial phyla per sponge with Proteobacteria and Chloroflexi being most diverse in each of the five sponges. Similarity comparison of bacteria on phylum and phylotype level revealed most similar communities in A. aerophoba and A. cavernicola and the most dissimilar community in Pseudocorticium jarrei. A surprising minimal core bacterial community was found when distribution of 97% operational taxonomic units (OTUs) was analyzed. Core, variable, and species-specific communities were comprised of 2, 26, and 72% of all OTUs, respectively. This indicates that each sponge contains a large set of unique bacteria and shares only few bacteria with other sponges. However, host species-specific bacteria are probably still closely related to each other explaining the observed similarity among bacterial communities in sponges.

Keywords

454 amplicon pyrosequencing Bacterial symbiont Core microbiota Microbial diversity Sponge Vertical transmission 

Notes

Acknowledgments

Research was supported by German Research Foundation (DFG) grants Schm2559/1-1 and 2-1 and a stipend in the program “Chancengleichheit” of the University of Wuerzburg to SS, DFG grant HE3299/1-3 to UH and University of Auckland FRDF grants 3609286 and 3622989 to MWT.

Supplementary material

10750_2011_799_MOESM1_ESM.xls (46 kb)
Supplementary material 1 (XLS 45 kb)

References

  1. Ahn, Y. B., S. K. Rhee, D. E. Fennell, L. J. Kerkhof, U. Hentschel & M. M. Haggblom, 2003. Reductive dehalogenation of brominated phenolic compounds by microorganisms associated with the marine sponge Aplysina aerophoba. Applied and Environmental Microbiology 69: 4159–4166.PubMedCrossRefGoogle Scholar
  2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers & D. J. Lipman, 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403–410.PubMedGoogle Scholar
  3. Anderson, S. A., P. T. Northcote & M. J. Page, 2010. Spatial and temporal variability of the bacterial community in different chemotypes of the New Zealand marine sponge Mycale hentscheli. FEMS Microbiology Ecology 72: 328–342.PubMedCrossRefGoogle Scholar
  4. Andersson, A. F., L. Riemann & S. Bertilsson, 2010. Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities. The ISME Journal 4: 171–181.PubMedCrossRefGoogle Scholar
  5. Bayer, K., S. Schmitt & U. Hentschel, 2008. Physiology, phylogeny and in situ evidence for bacterial and archaeal nitrifiers in the marine sponge Aplysina aerophoba. Environmental Microbiology 10: 2942–2955.PubMedCrossRefGoogle Scholar
  6. Chelossi, E., R. Pantile, R. Pronzato, M. Milanese & U. Hentschel, 2007. Bacteria with antimicrobial properties isolated from the Mediterranean sponges Chondrilla nucula and Petrosia ficiformis. Aquatic Microbial Ecology 49: 157–163.CrossRefGoogle Scholar
  7. Chou, H. H. & M. H. Holmes, 2001. DNA sequence quality trimming and vector removal. Bioinformatics 17: 1093–1104.PubMedCrossRefGoogle Scholar
  8. Chou, H. Y., N. Fierer, C. L. Lauber, J. G. Caporaso, R. Knight & P. Grogan, 2010. Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environmental Microbiology 12: 2998–3006.CrossRefGoogle Scholar
  9. De Rosa, S., M. Mitova & G. Tommonaro, 2003. Marine bacteria associated with sponge as source of cyclic peptides. Biomolecular Engineering 20: 311–316.PubMedCrossRefGoogle Scholar
  10. DeCaralt, S., M. J. Uriz & R. H. Wijffels, 2007. Vertical transmission and successive location of symbiotic bacteria during embryo development and larva formation in Corticium candelabrum (Porifera: Demospongiae). Journal of the Marine Biological Association of the United Kingdom 87: 1693–1699.CrossRefGoogle Scholar
  11. Enticknap, J. J., M. Kelly, O. Peraud & R. T. Hill, 2006. Characterization of a culturable alphaproteobacterial symbiont common to many marine sponges and evidence for vertical transmission via sponge larvae. Applied and Environmental Microbiology 72: 3724–3732.PubMedCrossRefGoogle Scholar
  12. Ereskovsky, A. V., E. Gonobobleva & A. Vishnyakov, 2005. Morphological evidence for vertical transmission of symbiotic bacteria in the viviparous sponge Halisarca dujardini Johnston (Porifera, Demospongiae, Halisarcida). Marine Biology 146: 869–875.CrossRefGoogle Scholar
  13. Fieseler, L., M. Horn, M. Wagner & U. Hentschel, 2004. Discovery of the novel candidate phylum “Poribacteria” in marine sponges. Applied and Environmental Microbiology 70: 3724–3732.PubMedCrossRefGoogle Scholar
  14. Friedrich, A. B., H. Merkert, T. Fendert, J. Hacker, P. Proksch & U. Hentschel, 1999. Microbial diversity in the marine sponge Aplysina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridization (FISH). Marine Biology 134: 461–470.CrossRefGoogle Scholar
  15. Friedrich, A. B., I. Fischer, P. Proksch, J. Hacker & U. Hentschel, 2001. Temporal variation of the microbial community associated with the mediterranean sponge Aplysina aerophoba. FEMS Microbiology Ecology 38: 105–113.CrossRefGoogle Scholar
  16. Galand, P. E., E. O. Casamayor, D. L. Kirchman & C. Lovejoy, 2009. Ecology of the rare microbial biosphere of the Arctic Ocean. Proceedings of the National Academy of Sciences of the United States of America 106: 22427–22432.PubMedCrossRefGoogle Scholar
  17. Gilbert, J. A., D. Field, P. Swift, L. Newbold, A. Oliver, T. Smyth, P. J. Somerfield, S. Huse & I. Joint, 2009. The seasonal structure of microbial communities in the Western English Channel. Environmental Microbiology 11: 3132–3139.PubMedCrossRefGoogle Scholar
  18. Hentschel, U., M. Schmid, M. Wagner, L. Fieseler, C. Gernert & J. Hacker, 2001. Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS Microbiology Ecology 35: 305–312.PubMedCrossRefGoogle Scholar
  19. Hentschel, U., J. Hopke, M. Horn, A. B. Friedrich, M. Wagner, J. Hacker & B. S. Moore, 2002. Molecular evidence for a uniform microbial community in sponges from different oceans. Applied and Environmental Microbiology 68: 4431–4440.PubMedCrossRefGoogle Scholar
  20. Hill, M., A. Hill, N. Lopez & O. Harriott, 2006. Sponge-specific bacterial symbionts in the Caribbean sponge, Chondrilla nucula (Demospongiae, Chondrosida). Marine Biology 148: 1221–1230.CrossRefGoogle Scholar
  21. Huse, S., D. B. M. Welch, H. G. Morrison & M. L. Sogin, 2010. Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environmental Microbiology 12: 1889–1898.PubMedCrossRefGoogle Scholar
  22. Joachimiak, M. P., J. L. Weisman & B. C. H. May, 2006. JColorGrid: software for the visualization of biological measurement. BMC Bioinformatics 27: 7–225.Google Scholar
  23. Kamke, J., M. W. Taylor & S. Schmitt, 2010. Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons. The ISME Journal 4: 498–508.PubMedCrossRefGoogle Scholar
  24. Kunin, V., A. Engelbrektson, H. Ochman & P. Hugenholtz, 2010. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environmental Microbiology 12: 118–123.PubMedCrossRefGoogle Scholar
  25. Lafi, F. F., J. A. Fuerst, L. Fieseler, C. Engels, W. W. L. Goh & U. Hentschel, 2009. Widespread distribution of Poribacteria in Demospongiae. Applied and Environmental Microbiology 75: 5695–5699.PubMedCrossRefGoogle Scholar
  26. Lee, O. O., P. Y. Chui, Y. H. Wong, J. R. Pawlik & P. Y. Qian, 2009. Evidence for vertical transmission of bacterial symbionts from adult to embryo in the Caribbean sponge Svenzea zeai. Applied and Environmental Microbiology 75: 6147–6156.PubMedCrossRefGoogle Scholar
  27. Lee, O. O., Y. Wang, J. Yang, F. F. Lafi, A. Al-Suwailem & P.-Y. Qian, 2010. Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. The ISME Journal, epub ahead of print, doi: 10.1038/ismej.2010.165.
  28. Maldonado, M., 2007. Intergenerational transmission of symbiotic bacteria in oviparous and viviparous demosponges, with emphasis on intracytoplasmically-compartmented bacterial types. Journal of the Marine Biological Association of the United Kingdom 87: 1701–1713.CrossRefGoogle 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. Biological Journal of the Linnean Society 97: 427–447.CrossRefGoogle Scholar
  30. Maldonado, M. & A. Riesgo, 2009. Gametogenesis, embryogenesis, and larval features of the oviparous sponge Petrosia ficiformis (Haplosclerida, Demospongiae). Marine Biology 156: 2181–2197.CrossRefGoogle Scholar
  31. Metzger, M. L., 2010. Sequencing technologies—the next generation. Nature Reviews Genetics 11: 31–46.CrossRefGoogle Scholar
  32. Mohamed, N. M., V. Rao, M. T. Hamann, M. Kelly & R. T. Hill, 2008. Monitoring bacterial diversity of the marine sponge Ircinia strobilina upon transfer into aquaculture. Applied and Environmental Microbiology 74: 4133–4143.PubMedCrossRefGoogle Scholar
  33. Muscholl-Silberhorn, A., V. Thiel & J. F. Imhoff, 2008. Abundance and bioactivity of cultured sponge-associated bacteria from the Mediterranean sea. Microbial Ecology 55: 94–106.PubMedCrossRefGoogle Scholar
  34. Olson, J. B. & P. J. McCarthy, 2005. Associated bacterial communities of two deep-water sponges. Aquatic Microbial Ecology 39: 47–55.CrossRefGoogle Scholar
  35. Oren, M., L. Steindler & M. Ilan, 2005. Transmission, plasticity and the molecular identification of cyanobacterial symbionts in the Red Sea sponge Diacarnus erythraenus. Marine Biology 148: 35–41.CrossRefGoogle Scholar
  36. Pabel, C. T., J. Vater, C. Wilde, P. Franke, J. Hofemeister, B. Adler, G. Bringmann, J. Hacker & U. Hentschel, 2003. Antimicrobial activities and matrix-assisted laser desorption/ionization mass spectrometry of Bacillus isolates from the marine sponge Aplysina aerophoba. Marine Biotechnology 5: 424–434.PubMedCrossRefGoogle Scholar
  37. Pimentel-Elardo, S., M. Wehrl, A. B. Friedrich, P. R. Jensen & U. Hentschel, 2003. Isolation of planctomycetes from Aplysina sponges. Aquatic Microbial Ecology 33: 239–245.CrossRefGoogle Scholar
  38. Quince, C., A. Lanzen, T. P. Curtis, R. J. Davenport, N. Hall, I. M. Head, L. F. Read & W. T. Sloan, 2009. Accurate determination of microbial diversity from 454 pyrosequencing data. Nature Methods 6: 639–641.PubMedCrossRefGoogle Scholar
  39. Redford, A. J., R. M. Bowers, R. Knight, Y. Linhart & N. Fierer, 2010. The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environmental Microbiology 12: 2885–2893.PubMedCrossRefGoogle Scholar
  40. Reeder, J. & R. Knight, 2009. The ‘rare biosphere’: a reality check. Nature Methods 6: 636–637.PubMedCrossRefGoogle Scholar
  41. Roesch, L. F., R. R. Fulthorpe, A. Riva, G. Casella, A. K. M. Hadwin, A. D. Kent, S. H. Daroub, F. A. O. Camargo, W. G. Farmerie & E. W. Triplett, 2007. Pyrosequencing enumerates and contrasts soil microbial diversity. The ISME Journal 1: 283–290.PubMedGoogle Scholar
  42. Schirmer, A., R. Gadkari, C. D. Reeves, F. Ibrahim, E. F. DeLong & C. R. Hutchinson, 2005. Metagenomic analysis reveals diverse polyketide synthase gene clusters in microorganisms associated with the marine sponge Discodermia dissoluta. Applied and Environmental Microbiology 71: 4840–4849.PubMedCrossRefGoogle Scholar
  43. Schlappy, M. L., S. I. Schottner, G. Lavik, M. M. M. Kuypers, D. de Beer & F. Hoffmann, 2010. Evidence of nitrification and denitrification in high and low microbial abundance sponges. Marine Biology 157: 593–602.CrossRefGoogle Scholar
  44. Schloss, P. D., S. L. Westcott, T. Ryabin, J. R. Hall, M. Hartmann, E. B. Hollister, R. A. Lesniewski, B. B. Oakley, D. H. Parks, C. J. Robinson, J. W. Sahl, B. Stres, G. G. Thallinger, D. J. Van Horn & C. F. Weber, 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75: 7537–7541.PubMedCrossRefGoogle Scholar
  45. Schmitt, S., M. Wehrl, N. Lindquist, J. B. Weisz & U. Hentschel, 2007a. Morphological and molecular analyses of microorganisms in Caribbean reef adult sponges and in corresponding reproductive material. In Porifera Research: Biodiversity, Innovation & Sustainability. Rio de Janeiro Museu Nacional, Buzios, Brazil: 561–568.Google Scholar
  46. Schmitt, S., J. B. Weisz, N. Lindquist & U. Hentschel, 2007b. Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Applied and Environmental Microbiology 73: 2067–2078.PubMedCrossRefGoogle Scholar
  47. Schmitt, S., H. Angermeier, R. Schiller, N. Lindquist & U. Hentschel, 2008. Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Applied and Environmental Microbiology 74: 7694–7708.PubMedCrossRefGoogle Scholar
  48. Sharp, K. H., B. Eam, D. J. Faulkner & M. G. Haygood, 2007. Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Applied and Environmental Microbiology 73: 622–629.PubMedCrossRefGoogle Scholar
  49. Siegl, A. & U. Hentschel, 2010. PKS and NRPS gene clusters from microbial symbiont cells of marine sponges by whole genome amplification. Environmental Microbiology Reports 2: 507–513.CrossRefGoogle Scholar
  50. Sogin, M. L., H. G. Morrison, J. A. Huber, D. Mark Welch, S. M. Huse, P. R. Neal, J. M. Arrieta & G. J. Herndl, 2006. Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proceedings of the National Academy of Sciences of the United States of America 103: 12115–12120.PubMedCrossRefGoogle Scholar
  51. Steger, D., P. Ettinger-Epstein, S. Whalan, U. Hentschel, R. de Nys, M. Wagner & M. W. Taylor, 2008. Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environmental Microbiology 10: 1087–1094.PubMedCrossRefGoogle Scholar
  52. Taylor, M. W., R. Radax, D. Steger & M. Wagner, 2007. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiology and Molecular Biology Reviews 71: 295–347.PubMedCrossRefGoogle Scholar
  53. Thiel, V., S. Leininger, R. Schmaljohann, F. Brummer & J. F. Imhoff, 2007. Sponge-specific bacterial associations of the Mediterranean sponge Chondrilla nucula (Demospongiae, Tetractinomorpha). Microbial Ecology 54: 101–111.PubMedCrossRefGoogle Scholar
  54. Thoms, C., M. Horn, M. Wagner, U. Hentschel & P. Proksch, 2003. Monitoring microbial diversity and natural product profiles of the sponge Aplysina cavernicola following transplantation. Marine Biology 142: 685–692.Google Scholar
  55. Turnbaugh, P. J., M. Hamady, T. Yatsunenko, B. L. Cantarel, A. Duncan, R. E. Ley, M. L. Sogin, W. J. Jones, B. A. Roe, J. P. Affourtit, M. Egholm, B. Henrissat, A. C. Heath, R. Knight & J. I. Gordon, 2009. A core gut microbiome in obese and lean twins. Nature 457: 480–487.PubMedCrossRefGoogle Scholar
  56. Usher, K. M., 2008. The ecology and phylogeny of cyanobacterial symbionts in sponges. Marine Ecology and Evolutionary Perspective 29: 178–192.CrossRefGoogle Scholar
  57. Usher, K. M., J. Kuo, J. Fromont & D. C. Sutton, 2001. Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461: 15–23.CrossRefGoogle Scholar
  58. Usher, K. M., J. Fromont, D. C. Sutton & S. Toze, 2004. The biogeography and phylogeny of unicellular cyanobacterial symbionts in sponges from Australia and the Mediterranean. Microbial Ecology 48: 167–177.PubMedCrossRefGoogle Scholar
  59. Vacelet, J., 1975. Etude en microscopie electronique de l’association entre bacteries et spongiaires du genre Verongia (Dictyoceratida). Journal De Microscopie 23: 271–288.Google Scholar
  60. Vacelet, J. & C. Donadey, 1977. Electron-microscope study of association between some sponges and bacteria. Journal of Experimental Marine Biology and Ecology 30: 301–314.CrossRefGoogle Scholar
  61. Wagner, M. & M. Horn, 2006. The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Current Opinion in Biotechnology 17: 241–249.PubMedCrossRefGoogle Scholar
  62. Webster, N. S., J. R. Xavier, M. Freckelton, C. A. Motti & R. Cobb, 2008. Shifts in microbial and chemical patterns within the marine sponge Aplysina aerophoba during a disease outbreak. Environmental Microbiology 10: 3366–3376.PubMedCrossRefGoogle Scholar
  63. Webster, N. S., M. W. Taylor, F. Behnam, S. Luecker, T. Rattei, S. Whalan, M. Horn & M. Wagner, 2010. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environmental Microbiology 12: 2070–2082.PubMedGoogle Scholar
  64. Wilkinson, C. R. & J. Vacelet, 1979. Transplantation of marine sponges to different conditions of light and current. Journal of Experimental Marine Biology and Ecology 37: 91–104.CrossRefGoogle Scholar
  65. Zhu, P., Q. Z. Li & G. Y. Wang, 2008. Unique microbial signatures of the alien Hawaiian marine sponge Suberites zeteki. Microbial Ecology 55: 406–414.PubMedCrossRefGoogle Scholar
  66. Zientz, E., T. Dandekar & R. Gross, 2004. Metabolic interdependence of obligate intracellular bacteria and their insect hosts. Microbiology and Molecular Biology Reviews 68: 745–770.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Susanne Schmitt
    • 1
    • 2
  • Ute Hentschel
    • 1
  • Michael W. Taylor
    • 2
  1. 1.Julius-von-Sachs Institute for Biological SciencesUniversity of WuerzburgWuerzburgGermany
  2. 2.Centre for Microbial Innovation, School of Biological SciencesUniversity of AucklandAucklandNew Zealand

Personalised recommendations