Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges

Abstract

Sponges are an important source of secondary metabolites showing a great diversity of structures and biological activities. Secondary metabolites can display specificity on different taxonomic levels, from species to phylum, which can make them good taxonomic biomarkers. However, the knowledge available on the metabolome of non-model organisms is often poor. In this study, we demonstrate that sponge chemical diversity may be useful for fundamental issues in systematics or evolutionary biology, by using metabolic fingerprints as indicators of metabolomic diversity in order to assess interspecific relationships. The sponge clade Homoscleromorpha is particularly challenging because its chemistry has been little studied and its phylogeny is still debated. Identification at species level is often troublesome, especially for the highly diversified Oscarella genus which lacks the fundamental characters of sponge taxonomy. An HPLC–DAD–ELSD–MS metabolic fingerprinting approach was developed and applied to 10 Mediterranean Homoscleromorpha species as a rapid assessment of their chemical diversity. A first validation of our approach was to measure intraspecific variability, which was found significantly lower than interspecific variability obtained between two Oscarella sister-species. Interspecific relationships among Homoscleromorpha species were then inferred from the alignment of their metabolic fingerprints. The resulting classification is congruent with phylogenetic trees obtained for a DNA marker (mitochondrial COI) and demonstrates the existence of two distinct groups within Homoscleromorpha. Metabolic fingerprinting proves a useful complementary tool in sponge systematics. Our case study calls for a revision of Homoscleromorpha with further phylogenetic studies and identification of additional chemical synapomorphic characters.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. Aiello, A., Fattorusso, E., Magno, S., & Menna, M. (1991). Isolation of 5 new 5-alpha-hydroxy-6-keto-delta-7 sterols from the marine sponge Oscarella lobularis. Steroids, 56, 337–340.

    PubMed  Article  CAS  Google Scholar 

  2. Allwood, J. W., Ellis, D. I., & Goodacre, R. (2008). Metabolomic technologies and their application to the study of plants and plant-host interactions. Physiologia Plantarum, 132, 117–135.

    PubMed  CAS  Google Scholar 

  3. Aoki, S., Watanabe, Y., Sanagawa, M., Setiawan, A., Kotoku, N., & Kobayashi, M. (2006). Cortistatins A, B, C, and D, anti-angiogenic steroidal alkaloids, from the marine sponge Corticium simplex. Journal of the American Chemical Society, 128, 3148–3149.

    PubMed  Article  CAS  Google Scholar 

  4. Aoki, S., Watanabe, Y., Tanabe, D., Setiawan, A., Arai, M., & Kobayashi, M. (2007). Cortistatins J, K, L, novel abeo-9(10–19)-androstane-type steroidal alkaloids with isoquinoline unit, from marine sponge Corticium simplex. Tetrahedron Letters, 48, 4485–4488.

    Article  CAS  Google Scholar 

  5. Ayanoglu, E., Li, H., Djerassi, C., & Duzgunes, N. (1988). Phospholipid studies of marine organisms. 17. Unusual sponge phospholipids and their analogs––synthesis and interactions with conventional phospholipids and cholesterol in model membranes. Chemistry and Physics of Lipids, 47, 165–175.

    Article  CAS  Google Scholar 

  6. Becerro, M. A., Uriz, M. J., & Turon, X. (1997). Chemically-mediated interactions in benthic organisms: The chemical ecology of Crambe crambe (Porifera, Poecilosclerida). Hydrobiologia, 355, 77–89.

    Article  CAS  Google Scholar 

  7. Bergquist, P. R., Lavis, A., & Cambie, R. C. (1986). Sterol composition and classification of the porifera. Biochemical Systematics and Ecology, 14, 105–112.

    Article  CAS  Google Scholar 

  8. Bergquist, P. R., & Wells, R. J. (1983). Chemotaxonomy of the Porifera: The development and current status of the field. In P. J. Scheuer (Ed.), Marine natural products: Chemical and biological perspectives (pp. 1–50). London: Academic Press.

    Google Scholar 

  9. Bewley, C. A., Holland, N. D., & Faulkner, D. J. (1996). Two classes of metabolites from Theonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia, 52, 716–722.

    PubMed  Article  CAS  Google Scholar 

  10. Blumenberg, M. (2003). Biomarker aus Kaltwasser- und Tiefsee-Kieselschwämmen: Phylogenie, Chemotaxonomie und Chemische Ökologie der Demospongiae und der Hexactinellida, PhD Thesis, Universität Hamburg.

  11. Borbone, N., De Marino, S., Iorizzi, M., Zollo, F. O., Debitus, C., Esposito, G., et al. (2002). Minor steroidal alkaloids from the marine sponge Corticium sp. Journal of Natural Products, 65, 1206–1209.

    PubMed  Article  CAS  Google Scholar 

  12. Borchiellini, C., Chombard, C., Manuel, M., Alivon, E., Vacelet, J., & Boury-Esnault, N. (2004). Molecular phylogeny of Demospongiae: Implications for classification and scenarios of character evolution. Molecular Phylogenetics and Evolution, 32, 823–837.

    PubMed  Article  CAS  Google Scholar 

  13. Boury-Esnault, N., Muricy, G., Gallissian, M. F., & Vacelet, J. (1995). Sponges without skeleton––a new mediterranean genus of Homoscleromorpha (Porifera, Demospongiae). Ophelia, 43, 25–43.

    Google Scholar 

  14. Boury-Esnault, N., Solecava, A. M., & Thorpe, J. P. (1992). Genetic and cytological divergence between color morphs of the Mediterranean sponge Oscarella lobularis schmidt (Porifera, Demospongiae, Oscarellidae). Journal of Natural History, 26, 271–284.

    Article  Google Scholar 

  15. Bultel-Ponce, V., Berge, J. P., Debitus, C., Nicolas, J. L., & Guyot, M. (1999). Metabolites from the sponge-associated bacterium Pseudomonas species. Marine Biotechnology, 1, 384–390.

    PubMed  Article  CAS  Google Scholar 

  16. Bultel-Ponce, V., Debitus, C., Berge, J. P., Cerceau, C., & Guyot, M. (1998). Metabolites from the sponge-associated bacterium Micrococcus luteus. Journal of Marine Biotechnology, 6, 233–236.

    PubMed  Google Scholar 

  17. Bundy, G. J., Davey, P. M., & Viant, R. M. (2009). Environmental metabolomics: A critical review and future perspectives. Metabolomics, 5, 3–21.

    Article  CAS  Google Scholar 

  18. Cimino, G., Destefano, S., & Minale, L. (1975). Long alkyl chains 3-substituted pyrrole-2-aldehyde (-2-carboxylic acid and methyl-ester) from marine sponge Oscarella lobularis. Experientia, 31, 1387–1389.

    Article  CAS  Google Scholar 

  19. De Caralt, S. (2007). Sponge culture: Learning from biology and ecology. PhD Thesis, Wageningen University.

  20. De Marino, S., Iorizzi, M., Zollo, F., Roussakis, C., & Debitus, C. (1999). Plakinamines C and D and three other new steroidal alkaloids from the sponge Corticium sp. European Journal of Organic Chemistry, 697–701.

  21. Djerassi, C., & Silva, C. J. (1991). Sponge sterols––origin and biosynthesis. Accounts of Chemical Research, 24, 371–378.

    Article  CAS  Google Scholar 

  22. Dunstan, G. A., Brown, M. R., & Volkman, J. K. (2005). Cryptophyceae and Rhodophyceae; chemotaxonomy, phylogeny, and application. Phytochemistry, 66, 2557–2570.

    PubMed  Article  CAS  Google Scholar 

  23. Ellis, D. I., Dunn, W. B., Griffin, J. L., Allwood, J. W., & Goodacre, R. (2007). Metabolic fingerprinting as a diagnostic tool. Pharmacogenomics, 8, 1243–1266.

    PubMed  Article  CAS  Google Scholar 

  24. Ereskovsky, A. V., Borchiellini, C., Gazave, E., Ivanisevic, J., Lapebie, P., Perez, T., et al. (2009a). The Homoscleromorph sponge Oscarella lobularis, a promising sponge model in evolutionary and developmental biology. Bioessays, 31, 89–97.

    PubMed  Article  Google Scholar 

  25. Ereskovsky, A. V., Ivanisevic, J., & Pérez, T. (2009b). Overview on the Homoscleromorpha sponges diversity in the Mediterranean, RAC/SPA, Okianos, Tabarka, Tunisia (pp. 88–96).

  26. Erpenbeck, D., Breeuwer, J., van der Velde, H., & van Soest, R. (2002). Unravelling host and symbiont phylogenies of halichondrid sponges (Demospongiae, Porifera) using a mitochondrial marker. Marine Biology, 141, 377–386.

    Article  Google Scholar 

  27. Erpenbeck, D., & van Soest, R. W. M. (2005). A survey for biochemical synapomorphies to reveal phylogenetic relationships of halichondrid demosponges (Metazoa: Porifera). Biochemical Systematics and Ecology, 33, 585–616.

    Article  CAS  Google Scholar 

  28. Erpenbeck, D., & van Soest, R. W. M. (2007). Status and perspective of sponge chemosystematics. Marine Biotechnology, 9, 2–19.

    PubMed  Article  CAS  Google Scholar 

  29. Fiehn, O. (2002). Metabolomics––the link between genotypes and phenotypes. Plant Molecular Biology, 48, 155–171.

    PubMed  Article  CAS  Google Scholar 

  30. Flowers, A. E., Garson, M. J., Webb, R. I., Dumdei, E. J., & Charan, R. D. (1998). Cellular origin of chlorinated diketopiperazines in the dictyoceratid sponge Dysidea herbacea (Keller). Cell and Tissue Research, 292, 597–607.

    PubMed  Article  CAS  Google Scholar 

  31. Fu, C. M., Lu, G. H., Schmitz, O. J., Li, Z. W., & Leung, K. S. Y. (2009). Improved chromatographic fingerprints for facile differentiation of two Ganoderma spp. Biomedical Chromatography, 23, 280–288.

    PubMed  Article  CAS  Google Scholar 

  32. Gazave, E. (2010). Etude de gène et voie de signalisation impliqués dans les processus morphogénétiques chez Oscarella lobularis: Implications potentielles sur la compréhension de l’origine du système nerveux, PhD Thesis, Université de la Méditérranée, Marseille.

  33. Ge, G. B., Zhang, Y. Y., Hao, D. C., Hu, Y., Luan, H. W., Liu, X. B., et al. (2008). Chemotaxonomic study of medicinal Taxus species with fingerprint and multivariate analysis. Planta Medica, 74, 773–779.

    PubMed  Article  CAS  Google Scholar 

  34. Griffiths, W. (2007). Metabolomics, metabonomics and metabolite profiling. Cambridge: Royal Society of Chemistry.

    Google Scholar 

  35. Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.

    PubMed  Article  Google Scholar 

  36. Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    CAS  Google Scholar 

  37. Han, C., Shen, Y., Chen, J. H., Lee, F. S. C., & Wang, X. R. (2008). HPLC fingerprinting and LC-TOF-MS analysis of the extract of Pseudostellaria heterophylla (Miq.) Pax root. Journal of Chromatography B, 862, 125–131.

    Article  CAS  Google Scholar 

  38. Jurek, J., Scheuer, P. J., & Kellyborges, M. (1994). Two steroidal alkaloids from a sponge Corticium sp. Journal of Natural Products, 57, 1004–1007.

    PubMed  Article  CAS  Google Scholar 

  39. Katajamaa, M., Miettinen, J., & Oresic, M. (2006). MZmine: Toolbox for processing and visualization of mass spectrometry based molecular profile data. Bioinformatics, 22, 634–636.

    PubMed  Article  CAS  Google Scholar 

  40. Kornprobst, J. M. (2005). Chimie des substances naturelles marines: Originalité, diversité, répartition. In J. M. Kornprobst (Ed.), Substances naturelles d’origine marine: Chimiodiversité, pharmacodiversité, biotechnologie (p. 601). Paris: Lavoisier.

    Google Scholar 

  41. Laroche, M., Imperatore, C., Grozdanov, L., Costantino, V., Mangoni, A., Hentschel, U., et al. (2007). Cellular localisation of secondary metabolites isolated from the Caribbean sponge Plakortis simplex. Marine Biology, 151, 1365–1373.

    Article  CAS  Google Scholar 

  42. Lee, H. S., Seo, Y., Rho, J. R., Shin, J., & Paul, V. J. (2001). New steroidal alkaloids from an undescribed sponge of the genus Corticium. Journal of Natural Products, 64, 1474–1476.

    PubMed  Article  CAS  Google Scholar 

  43. Lee, O. O., Yang, L. H., Li, X. C., Pawlik, J. R., & Qian, P. Y. (2007). Surface bacterial community, fatty acid profile, and antifouling activity of two congeneric sponges from Hong Kong and the Bahamas. Marine Ecology-Progress Series, 339, 25–40.

    Article  CAS  Google Scholar 

  44. Lopez-Legentil, S., Bontemps-Subielos, N., Turon, X., & Banaigs, B. (2006). Temporal variation in the production of four secondary metabolites in a colonial ascidian. Journal of Chemical Ecology, 32, 2079–2084.

    PubMed  Article  CAS  Google Scholar 

  45. Lopez-Legentil, S., & Turon, X. (2005). How do morphotypes and chemotypes relate to genotypes? The colonial ascidian Cystodytes (Polycitoridae). Zoologica Scripta, 34, 3–14.

    Article  Google Scholar 

  46. Loukaci, A., Muricy, G., Brouard, J.-P., Guyot, M., Vacelet, J., & Boury-Esnault, N. (2004). Chemical divergence between two sibling species of Oscarella (Porifera) from the Mediterranean Sea. Biochemical Systematics and Ecology, 32, 893–899.

    Article  CAS  Google Scholar 

  47. Marti, R., Fontana, A., Uriz, M. J., & Cimino, G. (2003). Quantitative assessment of natural toxicity in sponges: Toxicity bioassay versus compound quantification. Journal of Chemical Ecology, 29, 1307–1318.

    PubMed  Article  CAS  Google Scholar 

  48. McCarthy, P. J., Pitts, T. P., Gunawardana, G. P., Kellyborges, M., & Pomponi, S. A. (1992). Antifungal activity of meridine, a natural product from the marine sponge Corticium sp. Journal of Natural Products, 55, 1664–1668.

    PubMed  Article  CAS  Google Scholar 

  49. Molinski, T. F. (1993). Marine pyridoacridine alkaloids––structure, synthesis and biological chemistry. Chemical Reviews, 93, 1825–1838.

    Article  CAS  Google Scholar 

  50. Mooney, B. D., Nichols, P. D., de Salas, M. F., & Hallegraeff, G. M. (2007). Lipid, fatty acid, and sterol composition of eight species of Kareniaceae (Dinophyta): Chemotaxonomy and putative lipid phycotoxins. Journal of Phycology, 43, 101–111.

    Article  CAS  Google Scholar 

  51. Muricy, G. (1999). An evaluation of morphological and cytological data sets for the phylogeny of Homosclerophorida (Porifera: Demospongiae). Memoirs of the Queensland Museum, 44, 399.

    Google Scholar 

  52. Muricy, G., Bezac, C., Gallissian, M. F., & Boury-Esnault, N. (1999). Anatomy, cytology and symbiotic bacteria of four Mediterranean species of Plakina Schulze, 1880 (Demospongiae, Homosclerophorida). Journal of Natural History, 33, 159–176.

    Article  Google Scholar 

  53. Muricy, G., Boury-Esnault, N., Bezac, C., & Vacelet, J. (1996). Cytological evidence for cryptic speciation in Mediterranean Oscarella species (Porifera, Homoscleromorpha). Canadian Journal of Zoology, 74, 881–896.

    Article  Google Scholar 

  54. Muricy, G., Boury-Esnault, N., Bezac, C., & Vacelet, J. (1998). Taxonomic revision of the Mediterranean Plakina Schulze (Porifera, Demospongiae, Homoscleromorpha). Zoological Journal of the Linnean Society, 124, 169–203.

    Article  Google Scholar 

  55. Muricy, G., & Díaz, M. C. (2002). Order Homosclerophorida Dendy, 1905, Family Plakinidae Schilze, 1880. In J. N. A. Hooper & R. W. M. Van Soest (Eds.), Systema porifera a guide to the classification of sponges (p. 71). New York: Kluwer Academic/Plenum Publishers.

    Google Scholar 

  56. Nichols, S. A. (2005). An evaluation of support for order-level monophyly and interrelationships within the class Demospongiae using partial data from the large subunit rDNA and cytochrome oxidase subunit I. Molecular Phylogenetics and Evolution, 34, 81–96.

    PubMed  Article  CAS  Google Scholar 

  57. Nobeli, I., & Thornton, J. M. (2006). A bioinformatician’s view of the metabolome. Bioessays, 28, 534–545.

    PubMed  Article  CAS  Google Scholar 

  58. Paul, V. J., Arthur, K. E., Ritson-Williams, R., Ross, C., & Sharp, K. (2007). Chemical defenses: From compounds to communities. Biological Bulletin, 213, 226–251.

    PubMed  Article  CAS  Google Scholar 

  59. Paul, V. J., & Puglisi, M. P. (2004). Chemical mediation of interactions among marine organisms. Natural Product Reports, 21, 189–209.

    PubMed  Article  CAS  Google Scholar 

  60. Philippe, H., Derelle, R., Lopez, P., Pick, K., Borchiellini, C., Boury-Esnault, N., et al. (2009). Phylogenomics revives traditional views on deep animal relationships. Current Biology, 19, 706–712.

    PubMed  Article  CAS  Google Scholar 

  61. Pierens, G. K., Palframan, M. E., Tranter, C. J., Carroll, A. R., & Quinn, R. J. (2005). A robust clustering approach for NMR spectra of natural product extracts. Magnetic Resonance in Chemistry, 43, 359–365.

    PubMed  Article  CAS  Google Scholar 

  62. Plouguerne, E., Ioannou, E., Georgantea, P., Vagias, C., Roussis, V., Hellio, C., et al. (2010). Anti-microfouling activity of lipidic metabolites from the invasive brown alga Sargassum muticum (Yendo) Fensholt. Marine Biotechnology, 12, 52–61.

    PubMed  Article  CAS  Google Scholar 

  63. Posada, D. (2003). Using Modeltest and PAUP* to select a model of nucleotide substitution. In A. D. Baxevanis, D. B. Davison, & R. D. M. Page (Eds.), Current protocols in bioinformatics (pp. 6.5.1–6.5.14). New York: John Wiley & Sons.

    Google Scholar 

  64. Posada, D. (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.

    PubMed  Article  CAS  Google Scholar 

  65. Regalado, E. L., Mendiola, J., Laguna, A., Nogueiras, C., & Thomas, O. P. (2010) Polar alkaloids from the Caribbean marine sponge Niphates digitalis. Natural Product Communications. In press.

  66. Ridley, C. P., & Faulkner, D. J. (2003). New cytotoxic steroidal alkaloids from the Philippine sponge Corticium niger. Journal of Natural Products, 66, 1536–1539.

    PubMed  Article  CAS  Google Scholar 

  67. Rosenthal, G. A., & Berenbaum, M. R. (1992). Herbivores: Their interactions with plant secondary metabolites, ecological and evolutionary processes. San Diego, CA: Academic Press.

    Google Scholar 

  68. Rosser, R. M., & Faulkner, D. J. (1984). Two steroidal alkaloids from a marine sponge Plakina sp. Journal of Organic Chemistry, 49, 5157–5160.

    Article  CAS  Google Scholar 

  69. Shulaev, V., Cortes, D., Miller, G., & Mittler, R. (2008). Metabolomics for plant stress response. Physiologia Plantarum, 132, 199–208.

    PubMed  Article  CAS  Google Scholar 

  70. Sieber, S. A., & Marahiel, M. A. (2005). Molecular mechanisms underlying nonribosomal peptide synthesis: Approaches to new antibiotics. Chemical Reviews, 105, 715–738.

    PubMed  Article  CAS  Google Scholar 

  71. Solé-Cava, A. M., Bourt-Esnault, N., Vacelet, J., & Thorpe, J. P. (1992). Biochemical genetic divergence and systematics in sponges of the genera Corticium and Oscarella (Demospongiae: Homoscleromorpha) in the Mediterranean Sea. Marine Biology, 113, 299.

    Google Scholar 

  72. Swofford, D. L. (2002). PAUP*: Phylogenetic analysis using parsimony (*and other methods). Version 4. Sunderland, MA: Sinauer Associates Inc.

    Google Scholar 

  73. Taylor, M. W., Radax, R., Steger, D., & Wagner, M. (2007). Sponge-associated microorganisms: Evolution, ecology, and biotechnological potential. Microbiology and Molecular Biology Reviews, 71, 295–303.

    PubMed  Article  CAS  Google Scholar 

  74. Thiel, V., Blumenberg, M., Hefter, J., Pape, T., Pomponi, S., Reed, J., et al. (2002). A chemical view of the most ancient metazoa––biomarker chemotaxonomy of hexactinellid sponges. Naturwissenschaften, 89, 60.

    PubMed  Article  CAS  Google Scholar 

  75. Uriz, M. J., Becerro, M. A., Tur, J. M., & Turon, X. (1996). Location of toxicity within the Mediterranean sponge Crambe crambe (Demospongiae: Poecilosclerida). Marine Biology, 124, 583–590.

    Article  CAS  Google Scholar 

  76. Van Soest, R. W. M., & Braekman, J. C. (1999). Chemosystematics of Porifera: A review. Memoirs of the Queensland Museum, 44, 569.

    Google Scholar 

  77. Varmuza, K., & Filzmoser, P. (2009). Introduction to multivariate statistical analysis in chemometrics. New York: CRC Press, Taylor & Francis Group.

    Google Scholar 

  78. Vishnyakov, A., & Ereskovsky, A. (2009). Bacterial symbionts as an additional cytological marker for identification of sponges without a skeleton. Marine Biology, 156, 1625–1632.

    Article  Google Scholar 

  79. Wang, X. J., & Lavrov, D. V. (2007). Mitochondrial genome of the homoscleromorph Oscarella carmela (Porifera, Demospongiae) reveals unexpected complexity in the common ancestor of sponges and other animals. Molecular Biology and Evolution, 24, 363–373.

    PubMed  Article  Google Scholar 

  80. Watanabe, Y., Aoki, S., Tanabe, D., Setiawan, A., & Kobayashi, M. (2007). Cortistatins E, F, G, and H, four novel steroidal alkaloids from marine sponge Corticium simplex. Tetrahedron, 63, 4074–4079.

    Article  CAS  Google Scholar 

  81. Weckwerth, W., & Morgenthal, K. (2005). Metabolomics: From pattern recognition to biological interpretation. Drug Discovery Today, 10, 1551–1558.

    PubMed  Article  CAS  Google Scholar 

  82. Wolfender, J. L., Glauser, G., Boccard, J., & Rudaz, S. (2009). MS-based plant metabolomic approaches for biomarker discovery. Natural Product Communications, 4, 1417–1430.

    PubMed  CAS  Google Scholar 

  83. Xie, G. X., Ni, Y., Su, M. M., Zhang, Y. Y., Zhao, A. H., Gao, X. F., et al. (2008). Application of ultra-performance LC-TOF MS metabolite profiling techniques to the analysis of medicinal Panax herbs. Metabolomics, 4, 248–260.

    Article  CAS  Google Scholar 

  84. Yang, J., Chen, L. H., Zhang, Q., Lai, M. X., & Wang, Q. (2007). Quality assessment of Cortex cinnamomi by HPLC chemical fingerprint, principle component analysis and cluster analysis. Journal of Separation Science, 30, 1276–1283.

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

We sincerely thank to N. Penez and G. Culioli (Université du Sud Toulon-Var, France) for their assistance in HPLC–MS analyses and Daria Tokina (Zoological Institute of RAS, St. Petersburg, Russia) for technical assistance. We gratefully acknowledge the scientific help of J. Vacelet, N. Boury-Esnault, C. Borchiellini, A. Ereskovsky, (Centre d’Océanologie de Marseille, France), B. Banaigs (Université de Perpignan Via Domitia, France), M. Mehiri and D. Cabrol-Bass (Université de Nice Sophia Antipolis, France). We are also grateful to R. Graille and B. DeLigondes for diving and sampling assistance. This work was funded by the ECIMAR program (ANR-06-BDIV-001) of the French National Agency for Research.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Thierry Pérez.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Ivanišević, J., Thomas, O.P., Lejeusne, C. et al. Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges. Metabolomics 7, 289–304 (2011). https://doi.org/10.1007/s11306-010-0239-2

Download citation

Keywords

  • Metabolic fingerprinting
  • Porifera
  • Homoscleromorpha
  • Secondary metabolism
  • Sponge systematics