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 In this study, we used a subset of a previously established 454 amplicon pyrosequencing dataset (Schmitt and Taylor, unpublished data).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.
Similar content being viewed by others
References
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.
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.
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.
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.
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.
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.
Chou, H. H. & M. H. Holmes, 2001. DNA sequence quality trimming and vector removal. Bioinformatics 17: 1093–1104.
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.
De Rosa, S., M. Mitova & G. Tommonaro, 2003. Marine bacteria associated with sponge as source of cyclic peptides. Biomolecular Engineering 20: 311–316.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Joachimiak, M. P., J. L. Weisman & B. C. H. May, 2006. JColorGrid: software for the visualization of biological measurement. BMC Bioinformatics 27: 7–225.
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.
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.
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.
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.
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.
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.
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.
Maldonado, M. & A. Riesgo, 2009. Gametogenesis, embryogenesis, and larval features of the oviparous sponge Petrosia ficiformis (Haplosclerida, Demospongiae). Marine Biology 156: 2181–2197.
Metzger, M. L., 2010. Sequencing technologies—the next generation. Nature Reviews Genetics 11: 31–46.
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.
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.
Olson, J. B. & P. J. McCarthy, 2005. Associated bacterial communities of two deep-water sponges. Aquatic Microbial Ecology 39: 47–55.
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.
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.
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.
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.
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.
Reeder, J. & R. Knight, 2009. The ‘rare biosphere’: a reality check. Nature Methods 6: 636–637.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Usher, K. M., 2008. The ecology and phylogeny of cyanobacterial symbionts in sponges. Marine Ecology and Evolutionary Perspective 29: 178–192.
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.
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.
Vacelet, J., 1975. Etude en microscopie electronique de l’association entre bacteries et spongiaires du genre Verongia (Dictyoceratida). Journal De Microscopie 23: 271–288.
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.
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.
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.
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.
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.
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.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Guest editors: M. Maldonado, X. Turon, M. A. Becerro & M. J. Uriz / Ancient animals, new challenges: developments in sponge research
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Schmitt, S., Hentschel, U. & Taylor, M.W. Deep sequencing reveals diversity and community structure of complex microbiota in five Mediterranean sponges. Hydrobiologia 687, 341–351 (2012). https://doi.org/10.1007/s10750-011-0799-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-011-0799-9