Abstract
Many sponge species contain large and diverse communities of microorganisms. Some of these microbes are suggested to be in a mutualistic interaction with their host sponges, but there is little evidence to support these hypotheses. Stable nitrogen isotope ratios of sponges in the Key Largo, Florida (USA) area grouped sponges into species with relatively low δ15N ratios and species with relatively high δ15N ratios. Using samples collected in June 2002 from Three Sisters Reef and Conch Reef in the Key Largo, Florida area, transmission electron microscopy (TEM) and denaturing gradient gel electrophoresis were performed on tissues of the sponges Ircinia felix and Aplysina cauliformis, which are in the low δ15N group, and on tissue of the sponge Niphates erecta, which is in the high δ15N group. Results showed that I. felix and A. cauliformis have large and diverse microbial communities, while N. erecta has a low biomass of one bacterial strain. As the low δ15N ratios indicated a microbial input of nitrogen, these results suggested that I. felix and A. cauliformis were receiving nitrogen from their associated microbial community, while N. erecta was obtaining nitrogen solely from external sources. Sequence analysis of the microbial communities showed a diversity of metabolic capabilities among the microbes of the low δ15N group, which are lacking in the high δ15N group, further supporting metabolic differences between the two groups. This research provides support for hypotheses of mutualisms between sponges and their associated microbial communities.
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References
Ahn Y-B, Rhee S-K, Fennell DE, Kerkhof LJ, Hentschel U, Häggblom MM (2003) Reductive dehalogenation of brominated phenolic compounds by microorganisms associated with the marine sponge Aplysina aerophoba. Appl Environ Microbiol 69:4159–4166
Althoff KC, Schutt C, Steffen R, Batel R, Muller WEG (1998) Evidence for a symbiosis between bacteria of the genus Rhodobacter and the marine sponge Halichondria panicea: harbor also for putatively toxic bacteria? Mar Biol 130:529–536
Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Arillo A, Bavestrello G, Burlando B, Sara M (1993) Metabolic integration between symbiotic cyanobacteria and sponges—a possible mechanism. Mar Biol 117:159–162
Bewley CA, Holland ND, Faulkner DJ (1996) Two classes of metabolites from Theonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia 52:716–722
Corredor JE, Wilkinson CR, Vicente VP, Morell JM, Otero E (1988) Nitrate release by Caribbean reef sponges. Limnol Oceanogr 33:114–120
Diaz MC, Ward BB (1997) Sponge-mediated nitrification in tropical benthic communities. Mar Ecol Prog Ser 156:97–107
Feldmann J (1933) Sur quelques cyanophycées vivant dans le tissue des ésponges de Banyuls. Arch Zool Expérimentale et Générale 75:381–404
Fieseler L, Horn M, Wagner M, Hentschel U (2004) Discovery of the novel candidate phylum “Poribacteria” in marine sponges. Appl Environ Microbiol 70:3724–3732
Fogel ML, Cifuentes LA (1993) Isotope fractionation during primary production. In: Engel MH, Macko SA (eds) Organic geochemistry, Springer, New York, pp 73–100
Friedrich AB, Merkert H, Fendert T, Hacker J, Proksch P, Hentschel U (1999) Microbial diversity in the marine sponge Aplysina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridization (FISH). Mar Biol 134:461–470
Friedrich AB, Fischer I, Proksch P, Hacker J, Hentschel U (2001) Temporal variation of the microbial community associated with the Mediterranean sponge Aplysina aerophoba. FEMS Microbiol Ecol 38:105–113
Fuerst JA, Webb RI, Garson MJ, Hardy L, Reiswig HM (1999) Membrane-bounded nuclear bodies in a diverse range of microbial symbionts of Great Barrier Reef sponges. Mem Queensl Mus 44:193–203
Gilbert JJ, Allen HL (1973) Chlorophyll and primary productivy of some green freshwater sponges. Int Rev Gesamten Hydrobiol 58:633–658
Haygood MG, Schmidt EW, Davidson SK, Faulkner DJ (1999) Microbial symbionts of marine invertebrates: opportunities for microbial biotechnology. J Mol Microbiol Biotech 1:33–43
Hentschel U, Hopke J, Friedrich AB, Wagner M, Hacker J, Moore BS (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68:4431–4440
Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177
Hoffmann F (2003) Microbial sulfate reduction in the tissue of the cold-water sponge Geodia barretti (Tetractinellida, Demospongiae). Ph.D. thesis, Department of Geosciences, Göttingen University
Hoffmann F, Larsen O, Thiel V, Rapp HT, Pape T, Michaelis W, Reitner J (2005) An anaerobic world in sponges. Geomicrobiol J 22:1–10
Holler U, Wright AD, Matthee GF, Koenig GM, Draeger S, Aust HJ, Schulz B (2000) Fungi from marine sponges: diversity, biological activity and secondary metabolites. Mycol Res 104:1354–1365
Leichter JJ, Stewart HL, Miller SL (2003) Episodic nutrient transport to Florida coral reefs. Limnol Oceanogr 48:1394–1407
Magnino G, Sara A, Lancioni T, Gaino E (1999) Endobionts of the coral reef sponge Theonella swinhoei (Porifera, Demospongiae). Invertebr Biol 118:213–220
Montoya JP, Holl CM, Zehr JP, Hansen A, Villareal TA, Capone DG (2004) High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 430:1027–1031
Moore BS (1999) Biosynthesis of marine natural products: microorganisms and macroalgae. Nat Prod Rep 16:653–674
Pawlik JR, Chanas B, Toonen RJ, Fenical W (1995) Defenses of Caribbean sponges against predatory reef fish: I. Chemical deterrency. Mar Ecol Prog Ser 127:183–194
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320
Piel J (2004) Metabolites from symbiotic bacteria. Nat Prod Rep 21:519–538
Pile AJ (1997) Finding Reiswig’s missing carbon: quantification of sponge feeding using dual-beam flow cytometry, vol 2. In: Proceedings of the 8th international coral reef symposium, Panama, pp 1403–1410
Pile AJ (1999) Resource partitioning by Caribbean coral reef sponges: is there enough food for everyone? Mem Queensl Mus 44:457–461
Preston CM, Wu KY, Molinski TF, DeLong EF (1996) A psychrophilic crenarchaeon inhabits a marine sponge: Crenarchaeum symbiosum gen. nov., sp. nov. Proc Natl Acad Sci USA 93:6241–6246
Reiswig HM (1971a) Particle feeding in natural populations of three marine demosponges. Biol Bull 141:568–591
Reiswig HM (1971b) In-situ pumping activities of tropical demospongiae. Mar Biol 9:38–50
Reiswig HM (1974) Water transport, respiration and energetics of three tropical marine sponges. J Exp Mar Biol Ecol 14:231–249
Reiswig HM (1975) The aquiferous systems of 3 marine demospongiae. J Morphol 145:493–502
Rützler K (1990) Associations between Caribbean sponges and photosynthetic organisms. In: Rützler K (ed) New perspectives in sponge biology. Smithsonian Institution Press, Washington, DC, pp 455–466
Santavy DL, Willenz P, Colwell RR (1990) Phenotypic study of bacteria associated with the Caribbean sclerosponge, Ceratoporella nicholsoni. Appl Environ Microbiol 56:1750–1762
Sara M (1971) Ultrastructural aspects of symbiosis between 2 species of genus Aphanocapsa (Cyanophyceae) and Ircinia variabilis (Demospongiae). Mar Biol 11:214–221
Sara M, Liaci L (1964) Symbiotic associations between zooxanthellae and two marine sponges of the genus Cliona. Nature 203:321–323
Schmidt EW, Obraztova AY, Davidson SK, Faulkner DJ, Haygood MG (2000) Identification of the antifungal peptide-containing symbiont of the marine sponge Theonella swinhoei as a novel Delta-Proteobacterium Candidatus Entotheonella palauensis. Mar Biol 136:969–977
Schmitt S, Weisz J, Lindquist N, Hentschel U (2007) Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Appl Environ Microbiol 73:2067–2078
Southwell MW (2007) Sponge impacts on coral reef N cycling, Florida Keys, USA. Ph.D. Thesis, University of North Carolina at Chapel Hill
Taylor MW, Schupp PJ, Dahllof I, Kjelleberg S, Steinberg PD (2004) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6:121–130
Thacker RW (2005) Impacts of shading on sponge-Cyanobacteria symbioses: a comparison between host-specific and generalist associations. Integr Comp Biol 45:369–376
Thoms C, Horn M, Wagner M, Hentschel U, Proksch P (2003) Monitoring microbial diversity and natural product profiles of the sponge Aplysina cavernicola following transplantation. Mar Biol 142:685–692
Turon X, Galera J, Uriz MJ (1997) Clearance rates and aquiferous systems in two sponges with contrasting life-history strategies. J Exp Zool 278:22–36
Unson MD, Holland ND, Faulkner DJ (1994) 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
Vacelet J, Donadey C (1977) Electron microscope study of the association between some sponges and bacteria. J Exp Mar Biol Ecol 30:301–314
Vacelet J, Boury-Esnault N, Fiala-Medioni A, Fisher CR (1995) A methanotrophic carnivorous sponge. Nature 377:296
Vacelet J, Fiala-Medioni A, Fisher CR, Boury-Esnault N (1996) Symbiosis between methane-oxidizing bacteria and a deep-sea carnivorous cladorhizid sponge. Mar Ecol Prog Ser 145:77–85
Valley JW, Cole DR (2001) Stable isotope geochemistry. Mineralogical Society of America, Washington, DC
van der Meer MTJ, Schouten S, de Leeuw JW, Ward DM (2000) Autotrophy of green non-sulphur bacteria in hot spring microbial mats: biological explanations for isotopically heavy organic carbon in the geological record. Environ Microbiol 2:428–435
Vincente VP (1990) Response of sponges with autotrophic endosymbionts during the coral-bleaching episode in Puerto Rico. Coral Reefs 8:199–202
Webb VL, Maas EW (2002) Sequence analysis of 16S rRNA gene of cyanobacteria associated with the marine sponge Mycale (Carmia) hentscheli. FEMS Microbiol Lett 207:43–47
Webster NS, Hill RT (2001) The culturable microbial community of the Great Barrier reef sponge Rhopaloeides odorabile is dominated by an α-proteobacterium. Mar Biol 138:843–851
Webster NS, Wilson KJ, Blackall LL, Hill RT (2001) Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol 67:434–444
Webster NS, Negri AP, Munro M, Battershill CN (2004) Diverse microbial communities inhabit Antarctic sponges. Environ Microbiol 6:288–300
Weisz JB (2006) Measuring impacts of associated microbial communities on Caribbean reef sponges: searching for symbiosis. Ph.D. Thesis, University of North Carolina at Chapel Hill
Wilkinson CR (1978a) Microbial associations in sponges. 1. Ecology, physiology and microbial populations of coral reef sponges. Mar Biol 49:161–167
Wilkinson CR (1978b) Microbial association in sponges. 2. Numerical analysis of sponge and water bacterial populations. Mar Biol 49:169–176
Wilkinson CR (1978c) Microbial associations in sponges. 3. Ultrastructure of the in situ associations in coral reef sponges. Mar Biol 49:177–185
Wilkinson CR (1983) Net primary productivity in coral reef sponges. Science 219:410–412
Wilkinson CR (1984) Immunological evidence for the Precambrian origin of bacterial symbioses in marine sponges. Proc R Soc Lond 220:509–517
Wilkinson CR (1992) Symbiotic interactions between marine sponges and algae. In: Reisser W (ed) Algae and symbioses. Biopress, Bristol, UK, pp 112–151
Wilkinson CR, Nowak M, Austin B, Colwell RR (1981) Specificity of bacterial symbionts in Mediterranean and great barrier reef sponges. Microbiol Ecol 7:13–21
Wilkinson CR, Summons RE, Evans E (1999) Nitrogen fixation in symbiotic marine sponges: ecological significance and difficulties in detection. Mem Queensl Mus 44:667–673
Zehr JP, Ward BB (2002) Nitrogen cycling in the ocean: new perspectives on processes and paradigms. Appl Environ Microbiol 68:1015–1024
Acknowledgments
We thank the staff of the UNCW-NURC Center for exceptional logistical support that greatly facilitated the research. Financial support was provided by grants from NOAA’s National Undersea Research Center at the University of North Carolina at Wilmington to CSM and NL (NA03OAR4300088); the NSF Chemical Oceanography Program to CSM and NL (OCE 0351893 & OCE 0531422); a NSF Graduate Research Fellowship and Gussenhoven Student Fund in UNC Marine Sciences travel grant to JBW; UNC-Chapel Hill seed grants to CSM and to NL; and SFB567 (TPC3) grant to UH. We are grateful to Christine Gernert for help with sequencing and Susanne Schmitt for interesting discussions (both University of Wuerzburg). Three anonymous referees provided valuable comments on the manuscript. This study was conducted under permits from the Florida Keys National Marine Sanctuary and complied with the legal requirements in the United States of America.
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Communicated by J.P. Grassle.
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Weisz, J.B., Hentschel, U., Lindquist, N. et al. Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Mar Biol 152, 475–483 (2007). https://doi.org/10.1007/s00227-007-0708-y
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DOI: https://doi.org/10.1007/s00227-007-0708-y