Skip to main content

Advertisement

SpringerLink
Log in

Metabolome variability for two Mediterranean sponge species of the genus Haliclona: specificity, time, and space

  • Original Article
  • Published:
Metabolomics Aims and scope Submit manuscript

Abstract

Introduction

The study of natural variation of metabolites brings valuable information on the physiological state of the organisms as well as their phenotypic traits. In marine organisms, metabolome variability has mostly been addressed through targeted studies on metabolites of ecological or pharmaceutical interest. However, comparative metabolomics has demonstrated its potential to address the overall and complex metabolic variability of organisms.

Objectives

In this study, the intraspecific (temporal and spatial) variability of two Mediterranean Haliclona sponges (H. fulva and H. mucosa) was investigated through an untargeted and then targeted metabolomics approach and further compared to their interspecific variability.

Methods

Samples of both species were collected monthly during 1 year in the coralligenous habitat of the Northwestern Mediterranean sae at Marseille and Nice. Their metabolomic profiles were obtained by UHPLC-QqToF analyses.

Results

Marked variations were noticed in April and May for both species including a decrease in Shannon’s diversity and concentration in specialized metabolites together with an increase in fatty acids and lyso-PAF like molecules. Spatial variations across different sampling sites could also be observed for both species, however in a lesser extent.

Conclusions

Synchronous metabolic changes possibly triggered by physiological factors like reproduction and/or environmental factors like an increase in the water temperature were highlighted for both Mediterranean Haliclona species inhabiting close habitats but displaying different biosynthetic pathways. Despite significative intraspecific variations, metabolomic variability remains minor when compared to interspecific variations for these congenerous species, therefore suggesting the predominance of genetic information of the holobiont in the observed metabolome.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Abdo, D. A., Motti, C. A., Battershill, C. N., & Harvey, E. S. (2007). Temperature and spatiotemporal variability of salicylihalamide a in the sponge Haliclona sp. Journal of Chemical Ecology, 33, 1635–1645.

    Article  CAS  PubMed  Google Scholar 

  • Agrawal, A. A., Hastings, A. P., Johnson, M. T. J., Maron, J. L., & Salminen, J.-P. (2012). Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science, 338, 113–116.

    Article  CAS  PubMed  Google Scholar 

  • Alam, N., Bae, B. H., Hong, J., Lee, C.-O., Shin, B. A., Im, K. S., & Jung, J. H. (2001). Additional bioactive lyso-PAF congeners from the sponge Spirastrella abata. Journal of Natural Products, 64, 533–535.

    Article  CAS  PubMed  Google Scholar 

  • Alarif Walied, M., Abdel-Lateff, A., Al-Lihaibi Sultan, S., Seif-Eldin, A., N. & Badria Farid, A. (2013). A new cytotoxic brominated acetylenic hydrocarbon from the marine sponge Haliclona sp. with a selective effect against human breast cancer. Zeitschrift für Naturforschung C, 68, 70–75.

    Article  CAS  Google Scholar 

  • Aoki, N., Yamamoto, K., Ogawa, T., Ohta, E., Ikeuchi, T., Kamemura, K., Ikegami, S., & Ohta, S. (2013). Bromotheoynic acid, a brominated acetylenic acid from the marine sponge Theonella swinhoei. Natural Product Research, 27, 117–122.

    Article  CAS  PubMed  Google Scholar 

  • Aratake, S., Trianto, A., Hanif, N., De Voogd, N. J., & Tanaka, J. (2009). A new polyunsaturated brominated fatty acid from a Haliclona sponge. Marine Drugs, 7, 523–527.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergquist, P. R., & Hartman, W. D. (1969). Free amino acid patterns and the classification of the demospongiae. Marine Biology, 3, 247–268.

    Article  CAS  Google Scholar 

  • Blunt, J. W., Copp, B. R., Keyzers, R. A., Munro, M. H. G., & Prinsep, M. R. (2017). Marine natural products. Natural Product Reports, 34, 235–294.

    Article  CAS  PubMed  Google Scholar 

  • Borchert, E., Jackson, S. A., O’gara, F., & Dobson, A. D. W. (2016). Diversity of natural product biosynthetic genes in the microbiome of the deep sea sponges Inflatella pellicula, Poecillastra compressa, and Stelletta normani. Frontiers in Microbiology, 7, 1027.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bornancin, L., Bonnard, I., Mills, S. C., & Banaigs, B. (2017). Chemical mediation as a structuring element in marine gastropod predator-prey interactions. Natural Product Reports, 34, 644–676.

    Article  CAS  PubMed  Google Scholar 

  • Boury-Esnault, N., Lavrov, D. V., Ruiz, C. A., & Pérez, T. (2013). The integrative taxonomic approach applied to porifera: A case study of the homoscleromorpha. Integrative and Comparative Biology, 53, 416–427.

    Article  PubMed  Google Scholar 

  • Butler, A. J., Van Altena, I. A., & Dunne, S. J. (1996). Antifouling activity oflyso-platelet-activating factor extracted from australian sponge Crella incrustans. Journal of Chemical Ecology, 22, 2041–2061.

    Article  CAS  PubMed  Google Scholar 

  • Casapullo, A., Minale, L., & Zollo, F. (1993). Paniceins and related sesquiterpenoids from the Mediterranean sponge Reniera fulva. Journal of Natural Products, 56, 527–533.

    Article  CAS  PubMed  Google Scholar 

  • Casapullo, A., Scognamiglio, G., & Cimino, G. (1997). Mucosin: A new bicyclic eicosanoid from the Mediterranean sponge Reniera mucosa. Tetrahedron Letters, 38, 3643–3646.

    Article  CAS  Google Scholar 

  • Cimino, G., & De Stefano, S. (1977). New acetylenic compounds from the sponge Reniera fulva. Tetrahedron Letters, 18, 1325–1328.

    Article  Google Scholar 

  • Costa-Lotufo, L. V., Carnevale-Neto, F., Trindade-Silva, A. E., Silva, R. R., Silva, G. G. Z., Wilke, D. V., Pinto, F. C. L., Sahm, B. D. B., Jimenez, P. C., Mendonca, J. N., Lotufo, T. M. C., Pessoa, O. D. L., & Lopes, N. P. (2018). Chemical profiling of two congeneric sea mat corals along the Brazilian coast: Adaptive and functional patterns. Chemical Communications, 54, 1952–1955.

    Article  CAS  PubMed  Google Scholar 

  • De Caralt, S., Bry, D., Bontemps, N., Turon, X., Uriz, M.-J., & Banaigs, B. (2013). Sources of secondary metabolite variation in dysidea avara (Porifera: Demospongiae): The importance of having good neighbors. Marine Drugs, 11, 489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Goeij, J. M., Van Oevelen, D., Vermeij, M. J. A., Osinga, R., Middelburg, J. J., De Goeij, A. F. P. M., & Admiraal, W. (2013). Surviving in a marine desert: The sponge loop retains resources within coral reefs. Science, 342, 108–110.

    Article  CAS  PubMed  Google Scholar 

  • De’ath, G. (2002). Multivariate regression trees: A new technique for modeling species-environment relationships. Ecology, 83, 1105–1117.

    Google Scholar 

  • Dembitsky, V. M., Rezanka, T., & Srebnik, M. (2003). Lipid compounds of freshwater sponges: Family Spongillidae, class Demospongiae. Chemistry and Physics of Lipids, 123, 117–155.

    Article  CAS  PubMed  Google Scholar 

  • Duckworth, A. R., West, L., Vansach, T., Stubler, A., & Hardt, M. (2012). Effects of water temperature and pH on growth and metabolite biosynthesis of coral reef sponges. Marine Ecology Progress Series, 462, 67–77.

    Article  Google Scholar 

  • Ereskovsky, A. V., Geronimo, A., & Pérez, T. (2017). Asexual and puzzling sexual reproduction of the Mediterranean sponge Haliclona fulva (Demospongiae): Life cycle and cytological structures. Invertebrate Biology, 136, 403–421.

    Article  Google Scholar 

  • Erpenbeck, D., & Van Soest, R. W. M. (2006). Status and perspective of sponge chemosystematics. Marine Biotechnology, 9, 2.

    Article  CAS  PubMed  Google Scholar 

  • Ferrer, R. P., & Zimmer, R. K. (2012). Community ecology and the evolution of molecules of keystone significance. The Biological Bulletin, 223, 167–177.

    Article  PubMed  Google Scholar 

  • Ferrer, R. P., & Zimmer, R. K. (2013). Molecules of keystone significancecrucial agents in ecology and resource management. BioScience, 63, 428–438.

    Article  Google Scholar 

  • Genta-Jouve, G., & Thomas, O. P. (2013). Absolute configuration of the New 3-epi-cladocroic acid from the Mediterranean sponge Haliclona Fulva. Metabolites, 3, 24–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glassmire, A. E., Jeffrey, C. S., Forister, M. L., Parchman, T. L., Nice, C. C., Jahner, J. P., Wilson, J. S., Walla, T. R., Richards, L. A., Smilanich, A. M., Leonard, M. D., Morrison, C. R., Simbaña, W., Salagaje, L. A., Dodson, C. D., Miller, J. S., Tepe, E. J., Villamarin-Cortez, S., & Dyer, L. A. (2016). Intraspecific phytochemical variation shapes community and population structure for specialist caterpillars. New Phytologist, 212, 208–219.

    Article  PubMed  Google Scholar 

  • Goulitquer, S., Potin, P., & Tonon, T. (2012). Mass spectrometry-based metabolomics to elucidate functions in marine organisms and ecosystems. Marine Drugs, 10, 849–880.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haas, A. F., Fairoz, M. F. M., Kelly, L. W., Nelson, C. E., Dinsdale, E. A., Edwards, R. A., Giles, S., Hatay, M., Hisakawa, N., Knowles, B., Lim, Y. W., Maughan, H., Pantos, O., Roach, T. N. F., Sanchez, S. E., Silveira, C. B., Sandin, S., Smith, J. E., & Rohwer, F. (2016). Global microbialization of coral reefs. Nature Microbiology, 1, 16042.

    Article  CAS  PubMed  Google Scholar 

  • Hay, M. E. (2009). Marine chemical ecology: Chemical signals and cues structure marine populations, communities, and ecosystems. Annual Review of Marine Science, 1, 193–212.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hay, M. E. (2014). Challenges and opportunities in marine chemical ecology. Journal of Chemical Ecology, 40, 216–217.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He, Q., Sun, R., Liu, H., Geng, Z., Chen, D., Li, Y., Han, J., Lin, W., Du, S., & Deng, Z. (2014). NMR-Based Metabolomic Analysis of Spatial Variation in Soft Corals. Marine Drugs, 12, 1876–1890.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ivanisevic, J., Thomas, O. P., Pedel, L., Pénez, N., Ereskovsky, A. V., Culioli, G., & Pérez, T. (2011). Biochemical trade-offs: Evidence for ecologically linked secondary metabolism of the sponge Oscarella balibaloi. PLoS ONE, 6, e28059.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ivanišević, J., Perez, T., Ereskovsky, A. V., Barnathan, G., & Thomas, O. P. (2011). Lysophospholipids in the Mediterranean sponge Oscarella tuberculata: Seasonal variability and putative biological role. Journal of Chemical Ecology, 37, 537–545.

    Article  CAS  PubMed  Google Scholar 

  • Kelman, D., Benayahu, Y., & Kashman, Y. (2000). Variation in secondary metabolite concentrations in yellow and grey morphs of the red sea soft coral Parerythropodium fulvum fulvum: Possible ecological implications. Journal of Chemical Ecology, 26, 1123–1133.

    Article  CAS  Google Scholar 

  • Kessner, D., Chambers, M., Burke, R., Agus, D., & Mallick, P. (2008). ProteoWizard: Open source software for rapid proteomics tools development. Bioinformatics, 24, 2534–2536.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosmides, A. K., Kamisoglu, K., Calvano, S. E., Corbett, S. A., & Androulakis, I. P. (2013). Metabolomic fingerprinting: Challenges and opportunities. Critical Reviews in Biomedical Engineering, 41, 205–221.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuhlisch, C., & Pohnert, G. (2015). Metabolomics in chemical ecology. Natural Product Reports, 32, 937–955.

    Article  CAS  PubMed  Google Scholar 

  • Li, D., Baldwin, I. T., & Gaquerel, E. 2015. Navigating natural variation in herbivory-induced secondary metabolism in coyote tobacco populations using MS/MS structural analysis. Proceedings of the National Academy of Sciences, 112, E4147–E4155.

    Google Scholar 

  • Lin, K., Yang, P., Yang, H., Liu, A.-H., Yao, L.-G., Guo, Y.-W., & Mao, S.-C. (2015). Lysophospholipids from the Guangxi sponge Spirastrella purpurea. Lipids, 50, 697–703.

    Article  CAS  PubMed  Google Scholar 

  • Loh, T.-L., & Pawlik, J. R. (2014). Chemical defenses and resource trade-offs structure sponge communities on Caribbean coral reefs. Proceedings of the National Academy of Sciences of the United States of America, 111, 4151–4156.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López-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.

    Article  CAS  PubMed  Google Scholar 

  • López-Legentil, S., Bontemps-Subielos, N., Turon, X., & Banaigs, B. (2007). Secondary metabolite and inorganic contents in Cystodytes sp. (Ascidiacea): Temporal patterns and association with reproduction and growth. Marine Biology, 151, 293–299.

    Article  CAS  Google Scholar 

  • Moore, B. D., Andrew, R. L., Külheim, C., & Foley, W. J. (2014). Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytologist, 201, 733–750.

    Article  PubMed  Google Scholar 

  • Müller, W. E. G., Klemt, M., Thakur, N. L., Schröder, H. C., Aiello, A., D’esposito, M., Menna, M., & Fattorusso, E. (2004). Molecular/chemical ecology in sponges: Evidence for an adaptive antibacterial response in Suberites domuncula. Marine Biology, 144, 19–29.

    Article  CAS  Google Scholar 

  • Nishikawa, Y., Furukawa, A., Shiga, I., Muroi, Y., Ishii, T., Hongo, Y., Takahashi, S., Sugawara, T., Koshino, H., & Ohnishi, M. (2015). Cytoprotective effects of lysophospholipids from sea cucumber Holothuria atra. PLoS ONE, 10, e0135701.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noyer, C., & Becerro, M. A. (2012). Relationship between genetic, chemical, and bacterial diversity in the Atlanto-Mediterranean bath sponge Spongia lamella. Hydrobiologia, 687, 85–99.

    Article  Google Scholar 

  • Noyer, C., Thomas, O. P., & Becerro, M. A. (2011). Patterns of chemical diversity in the Mediterranean sponge Spongia lamella. PLoS ONE, 6, e20844.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nuzzo, G., Ciavatta, M. L., Villani, G., Manzo, E., Zanfardino, A., Varcamonti, M., & Gavagnin, M. (2012). Fulvynes, antimicrobial polyoxygenated acetylenes from the Mediterranean sponge Haliclona fulva. Tetrahedron, 68, 754–760.

    Article  CAS  Google Scholar 

  • Ohta, S., Ogawa, T., Ohta, E., Ikeuchi, T., Kamemura, K., & Ikegami, S. (2013). Petroacetylene, a new polyacetylene from the marine sponge Petrosiasolida that inhibits blastulation of starfish embryos. Natural Product Research, 27, 1842–1847.

    Article  CAS  PubMed  Google Scholar 

  • Ortega, M. J., Zubía, E., Carballo, J. L., & Salvá, J. (1996). Fulvinol, a new long-chain diacetylenic metabolite from the sponge Reniera fulva. Journal of Natural Products, 59, 1069–1071.

    Article  CAS  Google Scholar 

  • Page, M., West, L., Northcote, P., Battershill, C., & Kelly, M. (2005). Spatial and temporal variability of cytotoxic metabolites in populations of the New Zealand sponge Mycale hentscheli. Journal of Chemical Ecology, 31, 1161–1174.

    Article  CAS  PubMed  Google Scholar 

  • Patti, G. J., Tautenhahn, R., & Siuzdak, G. (2012). Meta-analysis of untargeted metabolomic data: Combining results from multiple profiling experiments. Nature Protocols, 7, 508–516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Paul, V. J., & Van Alstyne, K. L. (1992). Activation of chemical defenses in the tropical green algae Halimeda spp. Journal of Experimental Marine Biology and Ecology, 160, 191–203.

    Article  CAS  Google Scholar 

  • Payo, D. A., Colo, J., Calumpong, H., & De Clerck, O. (2011). Variability of non-polar secondary metabolites in the red alga Portieria. Marine Drugs, 9, 2438–2468.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters, L., Wright, A. D., Krick, A., & König, G. M. (2004). Variation of brominated indoles and terpenoids within single and different colonies of the marine bryozoan Flustra foliacea. Journal of Chemical Ecology, 30, 1165–1181.

    Article  CAS  PubMed  Google Scholar 

  • Pham, N. B., Butler, M. S., Hooper, J. N. A., Moni, R. W., & Quinn, R. J. (1999). Isolation of xestosterol esters of brominated acetylenic fatty acids from the marine sponge Xestospongia testudinaria. Journal of Natural Products, 62, 1439–1442.

    Article  CAS  PubMed  Google Scholar 

  • Pohnert, G. (2004). Chemical defense strategies of marine organisms. In S. SCHULZ (Ed.), The chemistry of pheromones and other semiochemicals I. Berlin: Springer.

    Google Scholar 

  • Proksch, P. (1994). Defensive roles for secondary metabolites from marine sponges and sponge-feeding nudibranchs. Toxicon, 32, 639–655.

    Article  CAS  PubMed  Google Scholar 

  • Redmond, N. E., Raleigh, J., Van Soest, R. W. M., Kelly, M., Travers, S. A. A., Bradshaw, B., Vartia, S., Stephens, K. M., & Mccormack, G. P. (2011). Phylogenetic relationships of the marine Haplosclerida (Phylum Porifera) employing ribosomal (28S rRNA) and mitochondrial (cox1, nad1) gene sequence data. PLoS ONE, 6, e24344.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reverter, M., Perez, T., Ereskovsky, A. V., & Banaigs, B. (2016). Secondary metabolome variability and inducible chemical defenses in the Mediterranean sponge Aplysina cavernicola. Journal of Chemical Ecology, 42, 60–70.

    Article  CAS  PubMed  Google Scholar 

  • Rhoades, D. F. (1985). Offensive-defensive interactions between herbivores and plants: Their relevance in herbivore population dynamics and ecological theory. The American Naturalist, 125, 205–238.

    Article  Google Scholar 

  • Routaboul, J.-M., Dubos, C., Beck, G., Marquis, C., Bidzinski, P., Loudet, O., & Lepiniec, L. (2012). Metabolite profiling and quantitative genetics of natural variation for flavonoids in Arabidopsis. Journal of Experimental Botany, 63, 3749–3764.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sacristan-Soriano, O., Banaigs, B., & Becerro, M. A. (2011). Relevant spatial scales of chemical variation in Aplysina aerophoba. Marine Drugs, 9, 2499–2513.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sacristán-Soriano, O., Banaigs, B., & Becerro, M. A. (2012). Temporal trends in the secondary metabolite production of the sponge Aplysina aerophoba. Marine Drugs, 10, 677–693.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santín, A., Grinyó, J., Ambroso, S., Uriz, M. J., Gori, A., Dominguez-Carrió, C., & Gili, J.-M. (2017). Sponge assemblages on the deep Mediterranean continental shelf and slope (Menorca Channel, Western Mediterranean Sea). Deep Sea Research Part I, 131, 75–86.

    Article  Google Scholar 

  • Schlick-Steiner, B. C., Steiner, F. M., Seifert, B., Stauffer, C., Christian, E., & Crozier, R. H. (2009). Integrative taxonomy: A multisource approach to exploring biodiversity. Annual Review of Entomology, 55, 421–438.

    Article  CAS  Google Scholar 

  • Schmitt, S., Tsai, P., Bell, J., Fromont, J., Ilan, M., Lindquist, N., Perez, T., Rodrigo, A., SCHUPP, P. J., Vacelet, J., Webster, N., Hentschel, U., & Taylor, M. W. (2012). Assessing the complex sponge microbiota: Core, variable and species-specific bacterial communities in marine sponges. The ISME Journal, 6, 564–576.

    Article  CAS  PubMed  Google Scholar 

  • Shin, B. A., Kim, Y. R., Lee, I.-S., Sung, C. K., Hong, J., Sim, C. J., Im, K. S., & Jung, J. H. (1999). Lyso-PAF analogues and lysophosphatidylcholines from the marine sponge Spirastrella abata as inhibitors of cholesterol biosynthesis. Journal of Natural Products, 62, 1554–1557.

    Article  CAS  PubMed  Google Scholar 

  • Soares, A. R., Duarte, H. M., Tinnoco, L. W., Pereira, R. C., & Teixeira, V. L. (2015). Intraspecific variation of meroditerpenoids in the brown alga Stypopodium zonale guiding the isolation of new compounds. Revista Brasileira de Farmacognosia, 25, 627–633.

    Article  CAS  Google Scholar 

  • Stanley, D. W. 2000. Eicosanoids in invertebrate signal transduction systems, Princeton: Princeton University Press.

    Google Scholar 

  • Sugiura, T., Fukuda, T., Miyamoto, T., & Waku, K. (1992). Distribution of alkyl and alkenyl ether-linked phospholipids and platelet-activating factor-like lipid in various species of invertebrates. Biochimica et Biophysica Acta (BBA), 1126, 298–308.

    Article  CAS  Google Scholar 

  • Ternon, E., Perino, E., Manconi, R., Pronzato, R., & THOMAS, O. P. (2017). How environmental factors affect the production of guanidine alkaloids by the Mediterranean sponge Crambe crambe. Marine Drugs, 15, 181.

    Article  PubMed Central  Google Scholar 

  • Tribalat, M.-A. 2016. Specialized metabolisms of Mediterranean sponges of genus Haliclona Grant, 1836. Nice: Université Côte d’Azur.

    Google Scholar 

  • Tribalat, M.-A., Marra, M. V., Mccormack, G. P., & Thomas, O. P. (2016). Does the chemical diversity of the order Haplosclerida (Phylum Porifera: Class Demospongia) fit with current taxonomic classification? Planta Medica, 82, 843–856.

    Article  CAS  PubMed  Google Scholar 

  • Vrablik, T. L., & Watts, J. L. (2013). Polyunsaturated fatty acid derived signaling in reproduction and development: Insights from Caenorhabditis elegans and Drosophila melanogaster. Molecular Reproduction and Development, 80, 244–259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, Q., Mansoor, T. A., Hong, J., Lee, C.-O., Im, K. S., Lee, D. S., & Jung, J. H. (2003). New lysophosphatidylcholines and monoglycerides from the marine sponge Stelletta sp. Journal of Natural Products, 66, 725–728.

    Article  CAS  PubMed  Google Scholar 

  • Zubía, E., Ortega, J., Luis Carballo, M., J. & Salvá, J. (1994). Sesquiterpene hydroquinones from the sponge Reniera mucosa. Tetrahedron, 50, 8153–8160.

    Article  Google Scholar 

Download references

Acknowledgements

This project (Grant-Aid Agreement No. PBA/MB/16/01) is carried out with the support of the Marine Institute and is funded under the Marine Research Programme by the Irish Government. M.-A.T. received a Ph.D. scholarship from the French Ministry for Higher education and Research. Metabolomic analyses were performed on the MALLABAR platform (Funded by the CNRS, the Provence Alpes Côte d’Azur Region and the Total Foundation). S. Greff (IMBE Marseille, France) is acknowledged for his help in recording and analysing the metabolomic data.

Funding

This project (Grant-Aid Agreement No. PBA/MB/16/01) is carried out with the support of the Marine Institute and is funded under the Marine Research Programme by the Irish Government. The Ph.D. scholarship of M.-A. Tribalat has been funded by the French “Ministère de lʼEnseignement supérieur, de la Recherche et de lʼInnovation”.

Author information

Authors and Affiliations

  1. Marine Biodiscovery, School of Chemistry and Ryan Institute, National University of Ireland Galway (NUI Galway), University Road, Galway, H91 TK33, Ireland

    Miriam Reverter & Olivier P. Thomas

  2. Geoazur, UMR Université Nice Sophia Antipolis-CNRS-IRD-OCA, 06560, Valbonne, France

    Marie-Aude Tribalat & Olivier P. Thomas

  3. Institut Méditerranéen de Biodiversité et d’Ecologie marine et continentale (IMBE), CNRS, IRD, Aix Marseille Université, Université Avignon, Station Marine d’Endoume, Rue de la Batterie des Lions, Marseille, France

    Thierry Pérez

Authors
  1. Miriam Reverter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie-Aude Tribalat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thierry Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Olivier P. Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Methodology and Formal Analysis, M.-A.T., T.P., M.R.; Validation, O.P.T.; Writing—Original Draft Preparation, M.R.; Writing—Review & Editing, O.P.T.; Supervision, T.P., O.P.T.; Project Administration, O.P.T.; Funding Acquisition, T.P., O.P.T.

Corresponding author

Correspondence to Olivier P. Thomas.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 320 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Reverter, M., Tribalat, MA., Pérez, T. et al. Metabolome variability for two Mediterranean sponge species of the genus Haliclona: specificity, time, and space. Metabolomics 14, 114 (2018). https://doi.org/10.1007/s11306-018-1401-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11306-018-1401-5

Keywords

Search

Navigation