Deep sequencing reveals diversity and community structure of complex microbiota in five Mediterranean sponges
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 In this study, we used a subset of a previously established 454 amplicon pyrosequencing dataset (Schmitt and Taylor, unpublished data).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.
Keywords454 amplicon pyrosequencing Bacterial symbiont Core microbiota Microbial diversity Sponge Vertical transmission
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.
- 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
- 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
- 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
- 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
- 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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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