Marine Biology

, Volume 152, Issue 2, pp 475–483 | Cite as

Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges

  • Jeremy B. WeiszEmail author
  • Ute Hentschel
  • Niels Lindquist
  • Christopher S. Martens
Research Article


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.


Sponge Particulate Organic Matter Sponge Species Sponge Cell Sponge Tissue 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



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.


  1. 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 69:4159–4166CrossRefPubMedCentralGoogle Scholar
  2. 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 130:529–536CrossRefGoogle Scholar
  3. 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 25:3389–3402CrossRefPubMedCentralGoogle Scholar
  4. Arillo A, Bavestrello G, Burlando B, Sara M (1993) Metabolic integration between symbiotic cyanobacteria and sponges—a possible mechanism. Mar Biol 117:159–162CrossRefGoogle Scholar
  5. Bewley CA, Holland ND, Faulkner DJ (1996) Two classes of metabolites from Theonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia 52:716–722CrossRefPubMedCentralGoogle Scholar
  6. Corredor JE, Wilkinson CR, Vicente VP, Morell JM, Otero E (1988) Nitrate release by Caribbean reef sponges. Limnol Oceanogr 33:114–120CrossRefGoogle Scholar
  7. Diaz MC, Ward BB (1997) Sponge-mediated nitrification in tropical benthic communities. Mar Ecol Prog Ser 156:97–107CrossRefGoogle Scholar
  8. Feldmann J (1933) Sur quelques cyanophycées vivant dans le tissue des ésponges de Banyuls. Arch Zool Expérimentale et Générale 75:381–404Google Scholar
  9. Fieseler L, Horn M, Wagner M, Hentschel U (2004) Discovery of the novel candidate phylum “Poribacteria” in marine sponges. Appl Environ Microbiol 70:3724–3732CrossRefPubMedCentralGoogle Scholar
  10. Fogel ML, Cifuentes LA (1993) Isotope fractionation during primary production. In: Engel MH, Macko SA (eds) Organic geochemistry, Springer, New York, pp 73–100Google Scholar
  11. 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 134:461–470CrossRefGoogle Scholar
  12. 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 38:105–113CrossRefGoogle Scholar
  13. 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 44:193–203Google Scholar
  14. Gilbert JJ, Allen HL (1973) Chlorophyll and primary productivy of some green freshwater sponges. Int Rev Gesamten Hydrobiol 58:633–658CrossRefGoogle Scholar
  15. Haygood MG, Schmidt EW, Davidson SK, Faulkner DJ (1999) Microbial symbionts of marine invertebrates: opportunities for microbial biotechnology. J Mol Microbiol Biotech 1:33–43Google Scholar
  16. 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 68:4431–4440CrossRefPubMedCentralGoogle Scholar
  17. Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177CrossRefPubMedCentralGoogle Scholar
  18. 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 UniversityGoogle Scholar
  19. Hoffmann F, Larsen O, Thiel V, Rapp HT, Pape T, Michaelis W, Reitner J (2005) An anaerobic world in sponges. Geomicrobiol J 22:1–10CrossRefGoogle Scholar
  20. 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 104:1354–1365CrossRefGoogle Scholar
  21. Leichter JJ, Stewart HL, Miller SL (2003) Episodic nutrient transport to Florida coral reefs. Limnol Oceanogr 48:1394–1407CrossRefGoogle Scholar
  22. Magnino G, Sara A, Lancioni T, Gaino E (1999) Endobionts of the coral reef sponge Theonella swinhoei (Porifera, Demospongiae). Invertebr Biol 118:213–220CrossRefGoogle Scholar
  23. 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 430:1027–1031CrossRefPubMedCentralGoogle Scholar
  24. Moore BS (1999) Biosynthesis of marine natural products: microorganisms and macroalgae. Nat Prod Rep 16:653–674CrossRefPubMedCentralGoogle Scholar
  25. Pawlik JR, Chanas B, Toonen RJ, Fenical W (1995) Defenses of Caribbean sponges against predatory reef fish: I. Chemical deterrency. Mar Ecol Prog Ser 127:183–194CrossRefGoogle Scholar
  26. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320CrossRefGoogle Scholar
  27. Piel J (2004) Metabolites from symbiotic bacteria. Nat Prod Rep 21:519–538CrossRefPubMedCentralGoogle Scholar
  28. 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 1403–1410Google Scholar
  29. Pile AJ (1999) Resource partitioning by Caribbean coral reef sponges: is there enough food for everyone? Mem Queensl Mus 44:457–461Google Scholar
  30. 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 93:6241–6246CrossRefPubMedCentralGoogle Scholar
  31. Reiswig HM (1971a) Particle feeding in natural populations of three marine demosponges. Biol Bull 141:568–591CrossRefGoogle Scholar
  32. Reiswig HM (1971b) In-situ pumping activities of tropical demospongiae. Mar Biol 9:38–50CrossRefGoogle Scholar
  33. Reiswig HM (1974) Water transport, respiration and energetics of three tropical marine sponges. J Exp Mar Biol Ecol 14:231–249CrossRefGoogle Scholar
  34. Reiswig HM (1975) The aquiferous systems of 3 marine demospongiae. J Morphol 145:493–502CrossRefGoogle Scholar
  35. 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 455–466Google Scholar
  36. Santavy DL, Willenz P, Colwell RR (1990) Phenotypic study of bacteria associated with the Caribbean sclerosponge, Ceratoporella nicholsoni. Appl Environ Microbiol 56:1750–1762PubMedPubMedCentralGoogle Scholar
  37. Sara M (1971) Ultrastructural aspects of symbiosis between 2 species of genus Aphanocapsa (Cyanophyceae) and Ircinia variabilis (Demospongiae). Mar Biol 11:214–221CrossRefGoogle Scholar
  38. Sara M, Liaci L (1964) Symbiotic associations between zooxanthellae and two marine sponges of the genus Cliona. Nature 203:321–323CrossRefGoogle Scholar
  39. 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 136:969–977CrossRefGoogle Scholar
  40. 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 73:2067–2078CrossRefPubMedCentralGoogle Scholar
  41. Southwell MW (2007) Sponge impacts on coral reef N cycling, Florida Keys, USA. Ph.D. Thesis, University of North Carolina at Chapel HillGoogle Scholar
  42. 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 6:121–130CrossRefPubMedCentralGoogle Scholar
  43. Thacker RW (2005) Impacts of shading on sponge-Cyanobacteria symbioses: a comparison between host-specific and generalist associations. Integr Comp Biol 45:369–376CrossRefPubMedCentralGoogle Scholar
  44. 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 142:685–692CrossRefGoogle Scholar
  45. Turon X, Galera J, Uriz MJ (1997) Clearance rates and aquiferous systems in two sponges with contrasting life-history strategies. J Exp Zool 278:22–36CrossRefGoogle Scholar
  46. 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 119:1–11CrossRefGoogle Scholar
  47. Vacelet J, Donadey C (1977) Electron microscope study of the association between some sponges and bacteria. J Exp Mar Biol Ecol 30:301–314CrossRefGoogle Scholar
  48. Vacelet J, Boury-Esnault N, Fiala-Medioni A, Fisher CR (1995) A methanotrophic carnivorous sponge. Nature 377:296CrossRefGoogle Scholar
  49. 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 145:77–85CrossRefGoogle Scholar
  50. Valley JW, Cole DR (2001) Stable isotope geochemistry. Mineralogical Society of America, Washington, DCGoogle Scholar
  51. 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 2:428–435CrossRefPubMedCentralGoogle Scholar
  52. Vincente VP (1990) Response of sponges with autotrophic endosymbionts during the coral-bleaching episode in Puerto Rico. Coral Reefs 8:199–202CrossRefGoogle Scholar
  53. Webb VL, Maas EW (2002) Sequence analysis of 16S rRNA gene of cyanobacteria associated with the marine sponge Mycale (Carmia) hentscheli. FEMS Microbiol Lett 207:43–47CrossRefPubMedCentralGoogle Scholar
  54. 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 138:843–851CrossRefGoogle Scholar
  55. Webster NS, Wilson KJ, Blackall LL, Hill RT (2001) Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol 67:434–444CrossRefPubMedCentralGoogle Scholar
  56. Webster NS, Negri AP, Munro M, Battershill CN (2004) Diverse microbial communities inhabit Antarctic sponges. Environ Microbiol 6:288–300CrossRefPubMedCentralGoogle Scholar
  57. 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 HillGoogle Scholar
  58. Wilkinson CR (1978a) Microbial associations in sponges. 1. Ecology, physiology and microbial populations of coral reef sponges. Mar Biol 49:161–167CrossRefGoogle Scholar
  59. Wilkinson CR (1978b) Microbial association in sponges. 2. Numerical analysis of sponge and water bacterial populations. Mar Biol 49:169–176CrossRefGoogle Scholar
  60. Wilkinson CR (1978c) Microbial associations in sponges. 3. Ultrastructure of the in situ associations in coral reef sponges. Mar Biol 49:177–185CrossRefGoogle Scholar
  61. Wilkinson CR (1983) Net primary productivity in coral reef sponges. Science 219:410–412CrossRefPubMedCentralGoogle Scholar
  62. Wilkinson CR (1984) Immunological evidence for the Precambrian origin of bacterial symbioses in marine sponges. Proc R Soc Lond 220:509–517CrossRefGoogle Scholar
  63. Wilkinson CR (1992) Symbiotic interactions between marine sponges and algae. In: Reisser W (ed) Algae and symbioses. Biopress, Bristol, UK, pp 112–151Google Scholar
  64. Wilkinson CR, Nowak M, Austin B, Colwell RR (1981) Specificity of bacterial symbionts in Mediterranean and great barrier reef sponges. Microbiol Ecol 7:13–21CrossRefGoogle Scholar
  65. Wilkinson CR, Summons RE, Evans E (1999) Nitrogen fixation in symbiotic marine sponges: ecological significance and difficulties in detection. Mem Queensl Mus 44:667–673Google Scholar
  66. Zehr JP, Ward BB (2002) Nitrogen cycling in the ocean: new perspectives on processes and paradigms. Appl Environ Microbiol 68:1015–1024CrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Jeremy B. Weisz
    • 1
    • 4
    Email author
  • Ute Hentschel
    • 2
  • Niels Lindquist
    • 1
  • Christopher S. Martens
    • 3
  1. 1.Institute of Marine SciencesUniversity of North Carolina at Chapel HillMorehead CityUSA
  2. 2.Research Center for Infectious DiseasesUniversity of WürzburgWürzburgGermany
  3. 3.Department of Marine SciencesUniversity of North Carolina at Chapel HillChapel HillUSA
  4. 4.Department of Biological SciencesOld Dominion UniversityNorfolkUSA

Personalised recommendations