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Metabolomics

, 14:114 | Cite as

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

  • Miriam Reverter
  • Marie-Aude Tribalat
  • Thierry Pérez
  • Olivier P. ThomasEmail author
Original Article

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.

Keywords

Marine environment Sponges Haliclona Spatio-temporal variability Interspecific variability Specialized metabolites 

Notes

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.

Author contribution

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.

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”.

Compliance with ethical standards

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.

Supplementary material

11306_2018_1401_MOESM1_ESM.docx (320 kb)
Supplementary material 1 (DOCX 320 KB)

References

  1. 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.CrossRefPubMedGoogle Scholar
  2. 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.CrossRefPubMedGoogle Scholar
  3. 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.CrossRefPubMedGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.CrossRefPubMedGoogle Scholar
  6. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bergquist, P. R., & Hartman, W. D. (1969). Free amino acid patterns and the classification of the demospongiae. Marine Biology, 3, 247–268.CrossRefGoogle Scholar
  8. 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.CrossRefPubMedGoogle Scholar
  9. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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.CrossRefPubMedGoogle Scholar
  11. 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.CrossRefPubMedGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. Casapullo, A., Minale, L., & Zollo, F. (1993). Paniceins and related sesquiterpenoids from the Mediterranean sponge Reniera fulva. Journal of Natural Products, 56, 527–533.CrossRefPubMedGoogle Scholar
  14. Casapullo, A., Scognamiglio, G., & Cimino, G. (1997). Mucosin: A new bicyclic eicosanoid from the Mediterranean sponge Reniera mucosa. Tetrahedron Letters, 38, 3643–3646.CrossRefGoogle Scholar
  15. Cimino, G., & De Stefano, S. (1977). New acetylenic compounds from the sponge Reniera fulva. Tetrahedron Letters, 18, 1325–1328.CrossRefGoogle Scholar
  16. 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.CrossRefPubMedGoogle Scholar
  17. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 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.CrossRefPubMedGoogle Scholar
  19. De’ath, G. (2002). Multivariate regression trees: A new technique for modeling species-environment relationships. Ecology, 83, 1105–1117.Google Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. Erpenbeck, D., & Van Soest, R. W. M. (2006). Status and perspective of sponge chemosystematics. Marine Biotechnology, 9, 2.CrossRefPubMedGoogle Scholar
  24. Ferrer, R. P., & Zimmer, R. K. (2012). Community ecology and the evolution of molecules of keystone significance. The Biological Bulletin, 223, 167–177.CrossRefPubMedGoogle Scholar
  25. Ferrer, R. P., & Zimmer, R. K. (2013). Molecules of keystone significancecrucial agents in ecology and resource management. BioScience, 63, 428–438.CrossRefGoogle Scholar
  26. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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.CrossRefPubMedGoogle Scholar
  28. Goulitquer, S., Potin, P., & Tonon, T. (2012). Mass spectrometry-based metabolomics to elucidate functions in marine organisms and ecosystems. Marine Drugs, 10, 849–880.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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.CrossRefPubMedGoogle Scholar
  30. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hay, M. E. (2014). Challenges and opportunities in marine chemical ecology. Journal of Chemical Ecology, 40, 216–217.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. Kessner, D., Chambers, M., Burke, R., Agus, D., & Mallick, P. (2008). ProteoWizard: Open source software for rapid proteomics tools development. Bioinformatics, 24, 2534–2536.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kuhlisch, C., & Pohnert, G. (2015). Metabolomics in chemical ecology. Natural Product Reports, 32, 937–955.CrossRefPubMedGoogle Scholar
  39. 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
  40. 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.CrossRefPubMedGoogle Scholar
  41. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 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.CrossRefPubMedGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. 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.CrossRefPubMedGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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.CrossRefGoogle Scholar
  48. Noyer, C., Thomas, O. P., & Becerro, M. A. (2011). Patterns of chemical diversity in the Mediterranean sponge Spongia lamella. PLoS ONE, 6, e20844.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. 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.CrossRefPubMedGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. 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.CrossRefPubMedGoogle Scholar
  53. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 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.CrossRefPubMedGoogle Scholar
  55. 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.CrossRefGoogle Scholar
  56. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 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.CrossRefPubMedGoogle Scholar
  58. 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.CrossRefPubMedGoogle Scholar
  59. 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
  60. Proksch, P. (1994). Defensive roles for secondary metabolites from marine sponges and sponge-feeding nudibranchs. Toxicon, 32, 639–655.CrossRefPubMedGoogle Scholar
  61. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 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.CrossRefPubMedGoogle Scholar
  63. 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.CrossRefGoogle Scholar
  64. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Sacristan-Soriano, O., Banaigs, B., & Becerro, M. A. (2011). Relevant spatial scales of chemical variation in Aplysina aerophoba. Marine Drugs, 9, 2499–2513.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 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.CrossRefGoogle Scholar
  68. 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.CrossRefGoogle Scholar
  69. 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.CrossRefPubMedGoogle Scholar
  70. 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.CrossRefPubMedGoogle Scholar
  71. 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.CrossRefGoogle Scholar
  72. Stanley, D. W. 2000. Eicosanoids in invertebrate signal transduction systems, Princeton: Princeton University Press.Google Scholar
  73. 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.CrossRefGoogle Scholar
  74. 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.CrossRefPubMedCentralGoogle Scholar
  75. Tribalat, M.-A. 2016. Specialized metabolisms of Mediterranean sponges of genus Haliclona Grant, 1836. Nice: Université Côte d’Azur.Google Scholar
  76. 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.CrossRefPubMedGoogle Scholar
  77. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 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.CrossRefPubMedGoogle Scholar
  79. Zubía, E., Ortega, J., Luis Carballo, M., J. & Salvá, J. (1994). Sesquiterpene hydroquinones from the sponge Reniera mucosa. Tetrahedron, 50, 8153–8160.CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Marine Biodiscovery, School of Chemistry and Ryan InstituteNational University of Ireland Galway (NUI Galway)GalwayIreland
  2. 2.Geoazur, UMR Université Nice Sophia Antipolis-CNRS-IRD-OCAValbonneFrance
  3. 3.Institut Méditerranéen de Biodiversité et d’Ecologie marine et continentale (IMBE), CNRS, IRD, Aix Marseille Université, Université AvignonMarseilleFrance

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