Journal of Applied Phycology

, Volume 28, Issue 6, pp 3561–3573 | Cite as

Structural characterization and comparative biomedical properties of phloroglucinol from Indian brown seaweeds

  • Ramachandran Karthik
  • Venkatesan Manigandan
  • Ravi Sheeba
  • Ramachandran Saravanan
  • Pushpabai Rajaian Rajesh


In the present study, phloroglucinol, a phenolic derivative, was extracted from the brown seaweeds Sargassum wightii, Sargassum tenerrimum and Turbinaria conoides. The secondary metabolite purified by reversed phase-high-performance liquid chromatography (RP-HPLC) was characterized using Fourier transform infrared spectroscopy (FT-IR), fluorescence spectroscopy, matrix-assisted laser desorption/ionization-time of flight/mass spectrometry (MALDI-TOF/MS) and 1H nuclear magnetic resonance (NMR) spectroscopy. Phloroglucinol from S. tenerrimum exhibited higher total antioxidant (453.3 mg AscAE g−1), DPPH-scavenging (71.07 %), H2O2-scavenging (89.7 %) and metal chelating (14.28 %) activities. Anticoagulant activity was maximum in phloroglucinol from T. conoides (APTT 38.2 s, PT 22.7 s and FC 1.92 g dL−1). Phloroglucinol from S. wightii showed maximum lymphocyte migration inhibition (0.8 mm). Cytotoxicity and lactate dehydrogenase (LDH) leakage against MCF-7 cells was high in phloroglucinol from T. conoides (IC50 10.74 μg mL−1 and 56.17 %). These findings suggest that phloroglucinol from the selected brown seaweeds could be a rich functional food with appreciable biomedical properties.


Phaeophyta Phloroglucinol MALDI-TOF/MS Anti-oxidant Anti-coagulant Anti-proliferative 



The authors acknowledge the CARE fellowship provided by Chettinad Academy of Research and Education. The authors also gratefully acknowledge the Director, Faculty of Allied Health Sciences, CARE, for his valuable suggestions and guidance. The authors also acknowledge Prof. P. Gautam, Anna University, Chennai, for providing the HPLC facility.

Supplementary material

10811_2016_851_MOESM1_ESM.doc (545 kb)
ESM 1 Fig. S1 RP-HPLC chromatogram of phloroglucinol from selected brown seaweeds showing a retention time of 4.8 min. Fig. S2 (a) UV-visible spectrum of purified phloroglucinol fraction from selected brown seaweeds; S2 (b) Fluorescence spectrum of phloroglucinol from selected brown seaweeds. Fig. S3 FT-IR spectrum of standard phloroglucinol and purified phloroglucinol fraction from selected brown seaweeds. (DOC 545 kb)


  1. Abdullah ASH, Mohammed AS, Abdullah R, Mirghani MES, Qubaisi MA (2014) Cytotoxic effects of Mangifera indica L. kernel extract on human breast cancer (MCF-7 and MDA-MB-231) cell lines and bioactive constituents in the crude extract. BMC Complement Altern Med 14:199CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aravindan S, Caroline RD, Somasundaram ST, Terence SH, Natarajan A (2013) Anti-pancreatic cancer deliverables from sea: first-hand evidence on the efficacy molecular targets and mode of action for multifarious polyphenols from five different brown-algae. PLoS One 8(4):e61977CrossRefPubMedPubMedCentralGoogle Scholar
  3. Audibert L, Fauchon M, Blanc N, Hauchard D, Gall EA (2009) Phenolic compounds in the brown seaweed Ascophyllum nodosum: distribution and radical-scavenging activities. Phytochem Anal 21:399–405CrossRefGoogle Scholar
  4. Budhiyanti SA, Raharjo S, Marseno DW, Lelana IYB (2012) Antioxidant activity of brown algae Sargassum species extract from the coastline of Java Island. Amer J Agricult Biol Sci 7:337–346CrossRefGoogle Scholar
  5. Burtin P (2003) Nutritional value of seaweeds. Elect J Environ Agricult Food Chem 2(4):498–503Google Scholar
  6. Caspi R, Altman T, Billington R, Dreher K, Foerster H, Fulcher CA, Holland TA, Keseler IM, Kothari A, Kubo A, Krummenacker M, Latendresse M, Mueller LA, Ong Q, Paley S, Subhraveti P, Weaver DS, Weerasinghe D, Zhang P, Karp PD (2014) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases. Nucleic Acids Res 42:D459–D471. MetaCyc Compound: monodehydroascorbate radical, MetaCyc.
  7. Chung IK, Beardall J, Mehta S, Sahoo S, Stojkovic S (2010) Using marine macroalgae for CO2 sequesteration: a critical appraisal. J Appl Phycol 23:877–886CrossRefGoogle Scholar
  8. Drynan JW, Clifford MN, Obuchowiczc J, Kuhnert N (2010) The chemistry of low molecular weight black tea polyphenols. Nat Prod Rep 27:417–462CrossRefPubMedGoogle Scholar
  9. Glombitza KW, Keusgen M (1995) Fuhalols and desoxyfuhalols from the brown alga Sargassum spinuligerum. Phytochem 38:987–995CrossRefGoogle Scholar
  10. Gouda S, Moharana RR, Das G, Patra JK (2013) Free radical scavenging potential of extracts of Gracilaria verrucosa (L) (Harvey): an economically important seaweed from Chilika Lake India. Int J Pharm Pharmaceut Sci 6:707–710Google Scholar
  11. Heffernan N, Smyth TJ, Soler-Villa A, Fitzgerald RJ, Brunton NP (2014) Phenolic content and antioxidant activity of fractions obtained from selected Irish macroalgae species (Laminaria digitata, Fucus serratus, Gracilaria gracilis and Codium fragile). J Appl Phycol 27:519–530CrossRefGoogle Scholar
  12. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  13. Huang S, Zhang CP, Li GQ, Sun YY, Wang K, Hu FL (2014) Identification phloroglucinol as a new marker for detecting propolis adulteration. Molecules 19:10208–10217CrossRefPubMedGoogle Scholar
  14. Jegou C, Kervarec N, Cerantola S, Bihannic I, Pouvreau VS (2015) NMR use to quantify phlorotannins: the case of Cystoseira tamariscifolia a phloroglucinol-producing brown macroalga in Brittany (France). Talanta 135:1–6CrossRefPubMedGoogle Scholar
  15. Kang KA, Lee KH, Chae S, Zhang R, Jung MS, Ham YM, Baik JS, Lee NH, Hyun JW (2006) Cytoprotective effect of phloroglucinol on oxidative stress induced cell damage via catalase activation. J Cell Biochem 97:609–620CrossRefPubMedGoogle Scholar
  16. Kim SK, Wijesekara I (2013) Marine derived nutraceuticals: trends and prospectives.In: S K Lin (ed) Mar Drugs. CRC Press, Boca Raton,pp 1-4.Google Scholar
  17. Koivikko R (2008) Brown algal phlorotannins Improving and applying chemical methods, Ph.D. thesis. University of Turku, Turku, FinlandGoogle Scholar
  18. Kumar P, Senthamilselvi S, Govindaraju M (2014) Phloroglucinol-encapsulated starch biopolymer: preparation antioxidant and cytotoxic effects on HepG2 liver cancer cell lines. RSC Adv 4:26787–26795CrossRefGoogle Scholar
  19. La Barre S, Potin P, Leblanc C, Delage L (2010) The halogenated metabolism of brown algae (Phaeophyta) its biological importance and its environmental significance. Mar Drugs 8:988–1010CrossRefPubMedPubMedCentralGoogle Scholar
  20. Larson RA (1997) Phenolic and enolic antioxidants. In: Larson RA (ed) Naturally occurring antioxidants. Lewis publishers, New York, pp 83–87Google Scholar
  21. Manzocco L, Anese M, Nicoli MC (1998) Antioxidants properties of green tea extracts as affected by processing. LWT–Food Sci Technol 31:694–698Google Scholar
  22. Mayer AMS, Glaser KB, Cuevas C, Jacobs RS, Kem W, Little RD, McIntosh JM, Newman DJ, Potts BC, Shuster DE (2010) The odyssey of marine pharmaceuticals: a current pipeline perspective. Trends Pharmacol Sci 31:255–265CrossRefPubMedGoogle Scholar
  23. Meenakshi S, Umayaparvathi S, Arumugam M, Balasubramanian T (2012) In vitro antioxidant properties and FT-IR analysis of two seaweeds of Gulf of Mannar. Asian Pac J Trop Biomed 1:66–70CrossRefGoogle Scholar
  24. Mendis E, Kim SK (2011) Present and future prospects of seaweeds in developing functional foods. Adv Food Nutr Res 64:1–15CrossRefPubMedGoogle Scholar
  25. Mhadhebi L, Laroche-Clary AA, Robert J, Bouraoui A (2011) Anti-inflammatory anti-proliferative and anti-oxidant activities of organic extracts from the Mediterranean seaweed Cystoseira crinita. Afr J Biotechnol 10:16682–16690Google Scholar
  26. Mole MN, Sabale A (2013) Antioxidant potential of seaweeds from Kunakeshwar coast along the West coast Maharashtra. Asian J Biomed Pharmaceut Sci 3:45–50Google Scholar
  27. Moura LA, Ramirez FO, Cavalcanti DN, Ribeiro SM, Muricy G, Teixeira VL (2011) Evaluation of marine brown algae and sponges from Brazil as anticoagulant and antiplatelet products. Mar Drugs 9:1346–1358CrossRefGoogle Scholar
  28. Mousseau Y, Leclers D, Durand KF, Moreau JC, Lia-Baldini AS, Rigaud M, Sturtz FG (2007) Improved agarose gel assay for quantification of growth factor-induced cell motility. Biotechniques 43:509–516CrossRefPubMedGoogle Scholar
  29. Nakai M, Kageyama N, Nakahara K, Miki W (2006) Phlorotannins as radical scavengers from the extract of Sargassum ringgoldianum. Mar Biotech 8:409–414CrossRefGoogle Scholar
  30. Namvar F, Mohamed S, Fard SG, Behravan J, Mustapha NM, Alitheen NBM, Othman F (2012) Polyphenol-rich seaweed (Eucheuma cottonii) extract suppresses breast tumour via hormone modulation and apoptosis induction. Food Chem 130:376–382CrossRefGoogle Scholar
  31. Namvar F, Mohamad R, Baharara J, Zafar-Balanejad S, Fargahi F, Rahman HS (2013) Antioxidant antiproliferative and antiangiogenesis effects of polyphenol-rich seaweed (Sargassum muticum). BioMed Res Int doi:  10.1155/2013/604787
  32. Narasimhan M, Pavithra SK, Krishnan V, Chandrasekaran M (2013) In vitro analysis of Antioxidant antimicrobial and antiproliferative activity of Enteromorpha antenna Enteromorpha linza and Gracilaria corticata extracts. Jundishapur J Nat Pharmaceut Prod 8:151–159CrossRefGoogle Scholar
  33. Ngonda F (2013) In- vitro anti-oxidant activity and free radical scavenging potential of roots of Malawian Trichodesma zeylanicumm (Burm). Asian J Biomed Pharmaceut Sci 3:21–25Google Scholar
  34. Ortiz-Ramirez FA, Cavalcanti DN, Villaca RC, de Paula JC, Valentin YY, Teixeira VL (2008) Chemical variations in the diterpenes from the Brazilian brown alga Dictyota menstrualis (Dictyotaceae Phaeophyta). Nat Prod Comm 11:1879–1884Google Scholar
  35. Pangestuti R, Kim SK (2015) Seaweeds-Derived bioactive materials for the Prevention and treatment of female’s cancer. In: Kim SK (ed) Handbook of anticancer drugs from marine origin. Springer International Publishing, Switzerland, pp 165–175Google Scholar
  36. Pasch H, Pizzi A, Rode K (2001) MALDI-TOF mass spectrometry of polyflavonoid tannins. Polymer 42:7531–7539CrossRefGoogle Scholar
  37. Paul JJP (2014) Histochemistry and fluorescence analysis of Turbinaria ornata (Turner) JAG—an important brown seaweed (Phaeophyceae). Indian J Plant Sci 3(1):40–44Google Scholar
  38. Plouguerne E, Lann KL, Connan S, Jechoux G, Deslandes E (2006) Spatial and seasonal variation in density reproductive status length and phenolic content of the invasive brown macroalga Sargassum muticum (Yendo) Fensholt along the coast of Western Brittany (France). Aquat Bot 85:337–344CrossRefGoogle Scholar
  39. Quéguineur B, Goya L, Ramos S, Martín MA, Mateos R, Guiry MD, Bravo L (2012) Effect of phlorotannin-rich extracts of Ascophyllum nodosum and Himanthalia elongata (Phaeophyceae) on cellular oxidative markers in human HepG2 cells. J Appl Phycol 25:1–11CrossRefGoogle Scholar
  40. Rodgers EH, Grant MH (1998) The effect of the flavonoids quercetin myricetin and epicatechin on the growth and enzyme activities of MCF-7 human breast cancer cells. Chem Biol Interact 116:213–228CrossRefPubMedGoogle Scholar
  41. Sathya R, Kanaga N, Sankar P, Jeeva S (2013) Antioxidant properties of phlorotannins from brown seaweed Cystoseira trinodis (Forsskal) C Agardh. Arabian J Chem doi:  10.1016/jarabjc201309039
  42. Shibata T, Ishimaru K, Kawaguchi S, Yoshikawa H, Hama Y (2008) Antioxidant activities of phlorotannins isolated from Japanese Laminariaceae. J Appl Phycol 20:705–711CrossRefGoogle Scholar
  43. Tanniou A, Vandanjon L, Incera M, Serrano Leon E, Husa V, Grand J, Nicolas J-L, Poupart N, Kervarec N, Engelen A, Walsh R, Guerard F, Bourgougnon N, Stiger-Pouvreau V (2013) Assessment of the spatial variability of phenolic contents and associated bioactivities in the invasive alga Sargassum muticum sampled along its European range from Norway to Portugal. J Appl Phycol 26:1215–1230Google Scholar
  44. Thomas NV, Kim SK (2013) Beneficial effects of marine algal compounds in cosmeceuticals. Mar Drugs 11:146–164CrossRefPubMedPubMedCentralGoogle Scholar
  45. Trono GC Jr (1999) Diversity of the seaweed flora of the Philippines and its utilization. Hydrobiologia 398/399:1–6CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Ramachandran Karthik
    • 1
  • Venkatesan Manigandan
    • 1
  • Ravi Sheeba
    • 1
  • Ramachandran Saravanan
    • 2
  • Pushpabai Rajaian Rajesh
    • 3
  1. 1.Department of Medical Biotechnology, Faculty of Allied Health SciencesChettinad Academy of Research and EducationKelambakkamIndia
  2. 2.Department of Marine Pharmacology, Faculty of Allied Health SciencesChettinad Academy of Research and EducationKelambakkamIndia
  3. 3.Molecular Biophysics Unit, Indian Institute of ScienceBangaloreIndia

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