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Metabolomic fingerprinting of Brazilian marine sponges: a case study of Plakinidae species from Fernando de Noronha Archipelago

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Abstract

Marine sponges from the Plakinidae family are well known for hosting cytotoxic secondary metabolites and the Brazilian Atlantic coast and its oceanic islands have been considered as a hotspot for the discovery of new Plakinidae species. Herein, we report the chemical profile among cytotoxic extracts obtained from four species of Plakinidae, collected in Fernando de Noronha Archipelago (PE, Northeastern Brazil). Crude organic extracts of Plakinastrella microspiculifera, Plakortis angulospiculatus, Plakortis insularis, and Plakortis petrupaulensis showed strong antiproliferative effects against two different cancer cell lines (HCT-116: 86.7–100%; MCF-7: 74.9–89.5%) at 50 μg/mL, by the MTT assay. However, at a lower concentration (5 μg/mL), high variability in inhibition of cell growth was observed (HCT-116: 17.3–68.7%; MCF-7: 0.00–55.5%), even within two samples of Plakortis insularis which were collected in the west and east sides of the Archipelago. To discriminate the chemical profile, the samples were investigated by UHPLC-HRMS under positive ionization mode. The produced data was uploaded to the Global Natural Products Social Molecular Networking and organized based on spectral similarities for purposes of comparison and annotation. Compounds such as dipeptides, nucleosides and derivatives, polyketides, and thiazine alkaloids were annotated and metabolomic differences were perceived among the species. To the best of our knowledge, this is the first assessment for cytotoxic activity and chemical profiling for Plakinastrella microspiculifera, Plakortis insularis and Plakortis petrupaulensis, revealing other biotechnologically relevant members of the Plakinidae family.

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References

  1. Carroll AR, Copp BR, Davis RA, Keyzers RA, Prinsep MR. Marine natural products. Nat Prod Rep. 2020;37:175–223.

    Article  Google Scholar 

  2. Thompson F, Krüger R, Thompson CC, Berlinck RGS, Coutinho R, Landell MF, et al. Marine biotechnology in Brazil: recent developments and its potential for innovation. Front Mar Sci. 2018;5:1–8.

    Article  Google Scholar 

  3. Ioca LP, Nicacio KJ, Berlinck RGS. Natural products from marine invertebrates and microorganisms in Brazil between 2004 and 2017: still the challenges, more rewards. J Braz Chem Soc. 2018;29(5):998–1031.

    CAS  Google Scholar 

  4. Wilke DV, Jimenez PC, Branco PC, Rezende-Teixeira P, Trindade-Silva AE, Bauermeister A, et al. Anticancer potential of compounds from the Brazilian Blue Amazon. Planta Med. 2020;87(01/02):49–70.

  5. Domingos C, Moraes F, Muricy G. Four new species of Plakinidae (Porifera: Homoscleromorpha) from Brazil. Zootaxa. 2013;6:530–44.

    Article  Google Scholar 

  6. Santos EA, Quintela AL, Ferreira EG, Sousa TS, Pinto FCL, Hajdu E, et al. Cytotoxic plakortides from the Brazilian marine sponge Plakortis angulospiculatus. J Nat Prod. 2015;78:996–1004.

    Article  CAS  Google Scholar 

  7. Norris MD, Perkins MV. Structural diversity and chemical synthesis of peroxide and peroxide-derived polyketide metabolites from marine sponges. Nat Prod Rep. 2016;33(7):861–80.

    Article  CAS  Google Scholar 

  8. Domingos C, Lage A, Muricy G. Overview of the biodiversity and distribution of the Class Homoscleromorpha in the tropical Western Atlantic. J Mar Biol Assoc U K. 2016;96(2):379–89.

    Article  Google Scholar 

  9. Epifanio RA, Pinheiro LS, Alves NC. Polyketides from the marine sponge Plakortis angulospiculatus. J Braz Chem Soc. 2005;16:1367–71.

    Article  CAS  Google Scholar 

  10. Costa-Lotufo LV, Carnevale-Neto F, Trindade-Silva AE, Silva RR, Silva GGZ, Wilke DV, et al. Chemical profiling of two congeneric sea mat corals along the Brazilian coast: adaptive and functional patterns. Chem Commun. 2018;54:1952–5.

    Article  CAS  Google Scholar 

  11. Bauermeister A, Velasco-Alzate K, Jimenez PC, Costa-Lotufo LV, Lopes NP, Dias T, et al. Metabolomic fingerprinting of Salinispora from Atlantic Oceanic islands. Front Microbiol. 2018;9:3021.

    Article  Google Scholar 

  12. Reverter M, Rohde S, Parchemin C, Tapissier-Bontempsand N, Schupp PJ. Metabolomics and marine biotechnology: coupling metabolite profiling and organism biology for the discovery of new compounds. Front Mar Sci. 2020;7:1–8.

    Article  Google Scholar 

  13. Ivanisevic J, Thomas OP, Lejeusne C, Chevaldonné P, Pérez T. Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges. Metabolomics. 2011;7:289–304.

    Article  CAS  Google Scholar 

  14. Mansur AA, Brown MT, Billington RA. The cytotoxic activity of extracts of the brown alga Cystoseira tamariscifolia (Hudson) Papenfuss, against cancer cell lines changes seasonally. J Appl Phycol. 2020;32(4):2419–29.

    Article  Google Scholar 

  15. Reverter M, Tribalat MA, Perez T, Thomas OP. Metabolome variability for two Mediterranean sponge species of the genus Haliclona: specificity, time, and space. Metabolomics. 2018;14(9):1–12/114.

  16. Machado FLS, Duarte HM, Gestinari LMS, Cassano V, Kaiser CR, Soares AR. Geographic distribution of natural products produced by the red alga Laurencia dendroidea J. AGARDH. Chem Biodivers. 2016;13:845–51.

    Article  CAS  Google Scholar 

  17. Puyana M, Pawlik J, Blum J, Fehical W. Metabolite variability Caribbean sponges of the genus Aplysina. Braz J Pharmacogn. 2015;25(6):592–9.

    Article  CAS  Google Scholar 

  18. Wang M, Carver JJ, Phelan VV, Sanchez LM, Garg N, Peng Y, et al. Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nat Biotechnol. 2016;34(8):828–37.

    Article  CAS  Google Scholar 

  19. Chong J, Xia J, Wishart DS. Using MetaboAnalyst 4.0 for comprehensive and integrative metabolomics data analysis. Curr Protoc Bioinformatics. 2019;68:1–128.

    Article  Google Scholar 

  20. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1–2):55–63.

    Article  CAS  Google Scholar 

  21. De Caralt S, Bry D, Bontemps N, Turon X, Uriz MJ, Banaigs B. Sources of secondary metabolite variation in Dysidea avara (Porifera: Demospongiae): the importance of having good neighbors. Mar Drugs. 2013;11(2):489–503.

    Article  Google Scholar 

  22. Gazave E, Lapébie P, Ereskovsky AV, Vacelet J, Renard E, Cárdenas P, et al. No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera. Hydrobiologia. 2012;687:3–10.

    Article  Google Scholar 

  23. Guo Y-C, Cao S-X, Zong X-K, Liao X-C, Zhao Y-F. ESI-MSn study on the fragmentation of protonated cyclic-dipeptides. Spectroscopy. 2009;23:131–9.

    Article  CAS  Google Scholar 

  24. Takeara R, Jimenez PC, Costa-Lotufo LV, Lopes JLC, Lopes NP. Sample optimization for rapid identification of nucleosides and bases from ascidian extracts using ESI-MS/MS. J Braz Chem Soc. 2007;18(5):1054–60.

    Article  CAS  Google Scholar 

  25. Huang R-M, Chen Y-N, Zeng Z, Gao C-H, Su X, Peng Y. Marine nucleosides: structure, bioactivity, synthesis and biosynthesis. Mar Drugs. 2014;12:5817–38.

    Article  CAS  Google Scholar 

  26. Festa C, De Marino S, D'Auria MV, Taglialatela-Scafati O, Deharo E, Petek S, et al. New antimalarial polyketide endoperoxides from the marine sponge Plakinastrella mamillaris collected at Fiji Islands. Tetrahedron. 2013;69(18):3706–13.

    Article  CAS  Google Scholar 

  27. Berrue F, Thomas OP, Funel-Le Bon C, Reyes F, Amade P. New bioactive cyclic peroxides from the Caribbean marine sponge Plakortis zyggompha. Tetrahedron. 2005;61:11843–9.

    Article  CAS  Google Scholar 

  28. Campagnuolo C, Fattorusso E, Taglialatela-Scafati O, Ianaro A, Pisano B. Plakortethers A-G: a new class of cytotoxic plakortin-derived metabolites. Eur J Org Chem. 2002;1:61–9.

    Article  Google Scholar 

  29. Davis RA, Duffy S, Fletcher S, Avery VM, Quinn RJ, Thiaplakortones A-D. Antimalarial thiazine alkaloids from the Australian marine sponge Plakortis lita. J Organomet Chem. 2013;78(19):9608–13.

    Article  CAS  Google Scholar 

  30. Zhang J, Tang X, Li J, Li P, de Voogd NJ, Ni X, et al. Cytotoxic polyketide derivatives from the South China Sea sponge Plakortis simplex. J Nat Prod. 2013;76(4):600–6.

    Article  CAS  Google Scholar 

  31. Hashemi M, Karami-Tehrani F, Ghavami S, Maddika S, Los M. Adenosine and deoxyadenosine induces apoptosis in oestrogen receptor-positive and -negative human breast cancer cells via the intrinsic pathway. Cell Prolif. 2005;38(5):269–85.

    Article  CAS  Google Scholar 

  32. Lockshin A, Mendoza JT, Giovanella BC, Stehlin JS Jr. Cytotoxic and biochemical effects of thymidine and 3-deazauridine on human tumor cells. Cancer Res. 1984;44(6):2534–9.

    CAS  PubMed  Google Scholar 

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Acknowledgements

We are forever grateful to Prof. Dr. Rosângela de Almeida Epifanio (in memoriam) for her dedication to the research in Brazilian marine natural products. She collected, kept, and cared for the biological material we assessed in this study, and her provision is the essential feature of all the work carried out until this day by our research group.

Funding

The authors thank Coordination for the Improvement of Higher Education Personnel (CAPES, Finance Code 001), Council for Technological and Scientific Development (CNPq) (grant number 406064/2018-0) CNPq, FAPERJ and São Paulo Research Foundation (FAPESP) [grant number 2014/50244-6; 2015/17177-6] for financial support.

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Correspondence to Alessandra Leda Valverde.

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Fagundes, T.d.S.F., da Silva, L.R.G., Brito, M.d.F. et al. Metabolomic fingerprinting of Brazilian marine sponges: a case study of Plakinidae species from Fernando de Noronha Archipelago. Anal Bioanal Chem 413, 4301–4310 (2021). https://doi.org/10.1007/s00216-021-03385-6

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