Skip to content
naulon

No retraction, correction or concern found when last checked on Nov 1, 2026.

Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts

Nicole S. Webster, Michael W. Taylor, Faris Behnam and 5 more

Environmental Microbiology · 2010

doi:10.1111/j.1462-2920.2009.02065.x

Abstract

Summary Marine sponges contain complex bacterial communities of considerable ecological and biotechnological importance, with many of these organisms postulated to be specific to sponge hosts. Testing this hypothesis in light of the recent discovery of the rare microbial biosphere, we investigated three Australian sponges by massively parallel 16S rRNA gene tag pyrosequencing. Here we show bacterial diversity that is unparalleled in an invertebrate host, with more than 250 000 sponge‐derived sequence tags being assigned to 23 bacterial phyla and revealing up to 2996 operational taxonomic units (95% sequence similarity) per sponge species. Of the 33 previously described ‘sponge‐specific’ clusters that were detected in this study, 48% were found exclusively in adults and larvae – implying vertical transmission of these groups. The remaining taxa, including ‘ Poribacteria ’, were also found at very low abundance among the 135 000 tags retrieved from surrounding seawater. Thus, members of the rare seawater biosphere may serve as seed organisms for widely occurring symbiont populations in sponges and their host association might have evolved much more recently than previously thought.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 56

  1. 1.

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

    Not in our library10.1016/s0022-2836(05)80360-2

  2. 2.

    Amann RI, Krumholz L, Stahl DA. Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol. 1990;172:762-770.

    Not in our library10.1128/jb.172.2.762-770.1990

  3. 3.

    Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol. 2005;71:7724-7736.

    Not in our library10.1128/aem.71.12.7724-7736.2005

  4. 4.

    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. 2008;10:2942-2955.

    Not in our library10.1111/j.1462-2920.2008.01582.x

  5. 5.

    Bock E, Wagner M, Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E. Oxidation of inorganic nitrogen compounds as an energy source. The Prokaryotes, Volume 2: Ecophysiology and Biochemistry. 2007;457-495.

    Not in our library

  6. 6.

    Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrell DM, et al. The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res. 2007;35:D169-D172.

    Not in our library10.1093/nar/gkl889

  7. 7.

    Daims H, Brühl A, Amann R, Schleifer K-H, Wagner M. The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol. 1999;22:434-444.

    Not in our library10.1016/s0723-2020(99)80053-8

  8. 8.

    Daims H, Nielsen JL, Nielsen PH, Schleifer KH, Wagner M. In situ characterization of Nitrospira-like nitrite-oxidizing bacteria active in wastewater treatment plants. Appl Environ Microbiol. 2001;67:5273-5284.

    Not in our library10.1128/aem.67.11.5273-5284.2001

  9. 9.
  10. 10.

    Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635-1638.

    Not in our library10.1126/science.1110591

  11. 11.

    Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792-1797.

    Not in our library10.1093/nar/gkh340

  12. 12.

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

    Not in our library10.1128/aem.72.5.3724-3732.2006

  13. 13.

    Felsenstein J. PHYLIP – Phylogeny Inference Package (Version 3.2). Cladistics. 1989;5:164-166.

    Not in our library

  14. 14.

    Fieseler L, Horn M, Wagner M, Hentschel U. Discovery of the novel candidate phylum ‘Poribacteria’ in marine sponges. Appl Environ Microbiol. 2004;70:3724-3732.

    Not in our library10.1128/aem.70.6.3724-3732.2004

  15. 15.
  16. 16.

    Hardoim CC, Costa R, Araujo FV, Hajdu E, Peixoto R, Lins U, et al. Diversity of bacteria in the marine sponge Aplysina fulva. Brazilian coastal waters. Appl Environ Microbiol. 2009;75:3331-3343.

    Not in our library10.1128/aem.02101-08

  17. 17.

    Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J, Moore BS. Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol. 2002;68:4431-4440.

    Not in our library10.1128/aem.68.9.4431-4440.2002

  18. 18.

    Hentschel U, Usher KM, Taylor MW. Marine sponges as microbial fermenters. FEMS Microbiol Ecol. 2006;55:167-177.

    Not in our library10.1111/j.1574-6941.2005.00046.x

  19. 19.

    Hoffmann F, Radax R, Woebken D, Holtappels M, Lavik G, Rapp HT, et al. Complex nitrogen cycling in the sponge Geodia barretti. Environ Microbiol. 2009;11:2228-2243.

    Not in our library10.1111/j.1462-2920.2009.01944.x

  20. 20.

    Hongoh Y, Deevong P, Inoue T, Moriya S, Trakulnaleamsai S, Ohkuma M, et al. Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl Environ Microbiol. 2005;71:6590-6599.

    Not in our library10.1128/aem.71.11.6590-6599.2005

  21. 21.

    Huber JA, Mark Welch DB, Morrison HG, Huse SM, Neal PR, Butterfield DA, Sogin ML. Microbial population structures in the deep marine biosphere. Science. 2007;318:97-100.

    Not in our library10.1126/science.1146689

  22. 22.

    Hugenholtz P, Pitulle C, Hershberger KL, Pace NR. Novel division level bacterial diversity in a yellowstone hot spring. J Bacteriol. 1998;180:366-376.

    Not in our library10.1128/jb.180.2.366-376.1998

  23. 23.

    Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJ. Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microbiol. 2001;67:4399-4406.

    Not in our library10.1128/aem.67.10.4399-4406.2001

  24. 24.
  25. 25.
  26. 26.

    Juretschko S, Timmermann G, Schmid M, Schleifer KH, Pommerening-Roser A, Koops HP, Wagner M. Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl Environ Microbiol. 1998;64:3042-3051.

    Not in our library10.1128/aem.64.8.3042-3051.1998

  27. 27.

    Kubota N, Kanemori M, Sasayama Y, Aida M, Fukumori Y. Identification of endosymbionts in Oligobrachia mashikoi (Siboglinidae, Annelida). Microbes Environ. 2007;22:136-144.

    Not in our library

  28. 28.

    Meyer B, Kuever J. Phylogenetic diversity and spatial distribution of the microbial community associated with the Caribbean deep-water sponge Polymastia cf. corticata by 16S rRNA, aprA, and amoA gene analysis. Microb Ecol. 2008;56:306-321.

    Not in our library10.1007/s00248-007-9348-5

  29. 29.

    Mohamed NM, Enticknap JJ, Lohr JE, McIntosh SM, Hill RT. Changes in bacterial communities of the marine sponge Mycale laxissima on transfer into aquaculture. Appl Environ Microbiol. 2008;74:1209-1222.

    Not in our library10.1128/aem.02047-07

  30. 30.

    Nyholm SV, McFall-Ngai MJ. The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol. 2004;2:632-642.

    Not in our library10.1038/nrmicro957

  31. 31.

    Peterson DA, Frank DN, Pace NR, Gordon JI. Metagenomic approaches for defining the pathogenesis of inflammatory bowel diseases. Cell Host Microbe. 2008;3:417-427.

    Not in our library10.1016/j.chom.2008.05.001

  32. 32.

    Pham VD, Konstantinidis KT, Palden T, DeLong EF. Phylogenetic analyses of ribosomal DNA-containing bacterioplankton genome fragments from a 4000 m vertical profile in the North Pacific Subtropical Gyre. Environ Microbiol. 2008;10:2313-2330.

    Not in our library10.1111/j.1462-2920.2008.01657.x

  33. 33.

    Pisera A. Palaeontology of sponges – a review. Can J Zool. 2006;84:242-261.

    Not in our library

  34. 34.

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

    Not in our library10.1093/nar/gkm864

  35. 35.

    Robidart JC, Bench SR, Feldman RA, Novoradovsky A, Podell SB, Gaasterland T, et al. Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ Microbiol. 2008;10:727-737.

    Not in our library10.1111/j.1462-2920.2007.01496.x

  36. 36.

    Santavy DL, Colwell RR. Comparison of bacterial communities associated with the Caribbean sclerosponge Ceratoporella nicholsoni and ambient seawater. Mar Ecol Prog Ser. 1990;67:73-82.

    Not in our library

  37. 37.

    Schloss PD, Handelsman J. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol. 2005;71:1501-1506.

    Not in our library10.1128/aem.71.3.1501-1506.2005

  38. 38.

    Schmitt S, Weisz J, Lindquist N, Hentschel U. Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Appl Environ Microbiol. 2007;73:2067-2078.

    Not in our library10.1128/aem.01944-06

  39. 39.

    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. 2008;74:7694-7708.

    Not in our library10.1128/aem.00878-08

  40. 40.

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

    Not in our library10.1128/aem.01493-06

All 56 references

Cited by papers we hold 12

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.