Assessment of mutagenic activity of phlorotannin-enriched extracts of three brown algal species

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

BACKGROUND: Phlorotannins are unique phenolic compounds produced by brown algae. Due to their considerable biological activity these metabolites are extensively studied in the context of medicinal applications. However, to date, no studies addressed potential genotoxicity of phlorotannins.

AIM: The objective of this research is an assessment of mutagenic activity of intracellular and cell wall (CW) bound phlorotannins of three brown algal species.

MATERIALS AND METHODS: Mutagenicity of phlorotannin extracts of Desmarestia aculeata, Fucus serratus, and Ectocarpus siliculosus was assessed by the Ames test, carried out using three tester strains of Salmonella typhimurium (TA97, TA98, and TA100) with and without metabolic activation.

RESULTS: Intracellular phlorotannin extracts of all tested algae showed relatively low values of minimum inhibitory concentration against S. typhimurium (20–30 μg/ml), with extract of D. aculeata being the most toxic. Intracellular phlorotannins of F. serratus and CW-bound polyphenols of E. siliculosus demonstrated moderate mutagenic activity in the Ames test inducing frameshift mutations with the number of His+ revertants more than twice higher compared to the control. The phlorotannin extracts of D. aculeata showed no mutagenic activity.

CONCLUSIONS: The brown alga D. aculeata may be regarded as a promising source of phlorotannins for medical applications, as its phlorotannin-enriched extracts have high antibiotic activity and are not mutagenic.

About the authors

Elena R. Tarakhovskaya

Saint Petersburg State University; Vavilov Institute of General Genetics, Russian Academy of Science, Saint Petersburg Branch

Author for correspondence.
Email: elena.tarakhovskaya@gmail.com
ORCID iD: 0000-0002-5341-2813
SPIN-code: 1710-9200

Cand. Sci. (Biol.), associate professor, Department of plant physiology and biochemistry

Russian Federation, Saint Petersburg; Saint Petersburg

Renata T. Islamova

Saint Petersburg State University

Email: renata.tag.isl@gmail.com
SPIN-code: 6559-9398

student

Russian Federation, Saint Petersburg

Elizaveta B. Zamyatkina

Saint Petersburg State University

Email: lizatekna@mail.ru
SPIN-code: 1986-2385

student

Russian Federation, Saint Petersburg

Elena I. Stepchenkova

Saint Petersburg State University; Vavilov Institute of General Genetics, Russian Academy of Science, Saint Petersburg Branch

Email: stepchenkova@gmail.com
ORCID iD: 0000-0002-5854-8701
SPIN-code: 9121-7483

Cand. Sci. (Biol.), head of laboratory of mutagenesis and genetic toxicology; assistant professor, Department of genetics and biotechnology

Russian Federation, Saint Petersburg; Saint Petersburg

References

  1. Shannon E, Abu-Ghannam N. Antibacterial derivatives of marine algae: An overview of pharmacological mechanisms and applications. Marine Drugs. 2016;14(8):81. doi: 10.3390/md14040081
  2. Papon N, Copp BR, Courdavault V. Marine drugs: Biology, pipelines, current and future prospects for production. Biotechnol Adv. 2022;54:107871. doi: 10.1016/j.biotechadv.2021.107871
  3. Isaza Martinez JH, Torres Castaneda HG. Preparation and chromatographic analysis of phlorotannins. J Chromatogr Sci. 2013;51(8):825–838. doi: 10.1093/chromsci/bmt045
  4. Shrestha S, Zhang W, Smid SD. Phlorotannins: A review on biosynthesis, chemistry and bioactivity. Food Biosci. 2021;39:100832. doi: 10.1016/j.fbio.2020.100832
  5. Steevensz AJ, Mackinnon SL, Hankinson R, et al. Profiling phlorotannins in brown macroalgae by liquid chromatography-high resolution mass spectrometry. Phytochem Anal. 2012;23(5):547–553. doi: 10.1002/pca.2354
  6. Birkemeyer C, Lemesheva V, Billig S, et al. Composition of intracellular and cell wall-bound phlorotannin fractions in fucoid algae indicates specific functions of these metabolites dependent on the chemical structure. Metabolites. 2020;10(9):369. doi: 10.3390/metabo10090369
  7. Generalić Mekinić I, Skroza D, Šimat V, et al. Phenolic content of brown algae (Pheophyceae) species: Extraction, identification, and quantification. Biomolecules. 2019;9(6):244. doi: 10.3390/biom9060244
  8. Lemesheva V, Islamova R, Stepchenkova E, et al. Antibacterial, antifungal and algicidal activity of phlorotannins, as principal biologically active components of ten species of brown algae. Plants. 2023;12(4):821. doi: 10.3390/plants12040821
  9. Schoenwaelder MEA, Clayton MN. The presence of phenolic compounds in isolated cell walls of brown algae. Phycologia. 1999;38(3):161–166. doi: 10.2216/i0031-8884-38-3-161.1
  10. Schoenwaelder MEA. The occurrence and cellular significance of physodes in brown algae. Phycologia. 2002;41(2):125–139. doi: 10.2216/i0031-8884-41-2-125.1
  11. Catarino MD, Silva AMS, Cardoso SM. Fucaceae: a source of bioactive phlorotannins. Int J Mol Sci. 2017;18(6):1327. doi: 10.3390/ijms18061327
  12. Hagerman AE, Riedl KM, Jones GA, et al. High molecular weight plant polyphenolics (tannins) as biological antioxidants. J Agric Food Chem. 1998;46(5):1887–1892. doi: 10.1021/jf970975b
  13. Ferreres F, Lopes G, Gil-Izquierdo A, et al. Phlorotannin extracts from Fucales characterized by HPLC-DAD-ESI-MSn: approaches to hyaluronidase inhibitory capacity and antioxidant properties. Marine Drugs. 2012;10(12):2766–2781. doi: 10.3390/md10122766
  14. Wang T, Jónsdóttir R, Liu H, et al. Antioxidant capacities of phlorotannins extracted from the brown algae Fucus vesiculosus. J Agric Food Chem. 2012;60(23):5874–5883. doi: 10.1021/jf3003653
  15. Liu X, Yuan W, Sharma-Shivappa R, van Zanten J. Antioxidant activity of phlorotannins from brown algae. Int J Agric Biol Eng. 2017;10(6):184–191. doi: 10.25165/j.ijabe.20171006.2854
  16. Kim A-R, Shin T-S, Lee M-S, et al. Isolation and identification of phlorotannins from Ecklonia stolonifera with antioxidant and anti-inflammatory properties. J Agric Food Chem. 2009;57(9):3483–3489. doi: 10.1021/jf900820x
  17. Quéguineur B, Goya L, Ramos S, et al. Effect of phlorotannin-rich extracts of Ascophyllum nodosum and Himanthalia elongata (Phaeophyceae) on cellular oxidative markers in human HepG2 cells. J Appl Phycol. 2013;25:1–11. doi: 10.1007/s10811-012-9832-2
  18. Kang M-C, Cha SH, Wijesinghe WAJP, et al. Protective effect of marine algae phlorotannins against AAPH-induced oxidative stress in zebrafish embryo. Food Chem. 2013;138(2–3):950–955. doi: 10.1016/j.foodchem.2012.11.005
  19. Eom S-H, Kim Y-M, Kim S-K. Antimicrobial effect of phlorotannins from marine brown algae. Food Chem Toxicol. 2012;50(9): 3251–3255. doi: 10.1016/j.fct.2012.06.028
  20. Lopes G, Pinto E, Andrade PB, Valentaõ P. Antifungal activity of phlorotannins against dermatophytes and yeasts: Approaches to the mechanism of action and influence on Candida albicans virulence factor. PLoS ONE. 2013;8: e72203. doi: 10.1371/journal.pone.0072203
  21. Eom S-H, Kang M-S, Kim Y-M. Antibacterial activity of the Phaeophyta Ecklonia stolonifera on methicillin-resistant Staphylococcus aureus. Fish Aquatic Sci. 2008;11(1):1–6. doi: 10.5657/FAS.2008.11.1.001
  22. Kim H-J, Dasagrandhi C, Kim S-H, et al. In vitro antibacterial activity of phlorotannins from edible brown algae, Eisenia bicyclis against streptomycin-resistant Listeria monocytogenes. Ind J Microbiol. 2018;58:105–108. doi: 10.1007/s12088-017-0693-x
  23. Dutot M, Fagon R, Hemon M, Rat P. Antioxidant, anti-inflammatory, and anti-senescence activities of a phlorotannin-rich natural extract from brown seaweed Ascophyllum nodosum. Appl Biochem Biotechnol. 2012;167:2234–2240. doi: 10.1007/s12010-012-9761-1
  24. Geisen U, Zenthoefer M, Peipp M, et al. Molecular mechanisms by which a Fucus vesiculosus extract mediates cell cycle inhibition and cell death in pancreatic cancer cells. Marine Drugs. 2015;13(7): 4470–4491. doi: 10.3390/md13074470
  25. Zenthoefer M, Geisen U, Hofmann-Peiker K, et al. Isolation of polyphenols with anticancer activity from the Baltic Sea brown seaweed Fucus vesiculosus using bioassay-guided fractionation. J Appl Phycol. 2017;29:2021–2037. doi: 10.1007/s10811-017-1080-z
  26. Liu H, Gu L. Phlorotannins from brown algae (Fucus vesiculosus) inhibited the formation of advanced glycation endproducts by scavenging reactive carbonyls. J Agric Food Chem. 2012;60(5):1326–1334. doi: 10.1021/jf204112f
  27. Meshalkina D, Tsvetkova E, Orlova A, et al. First insight into the neuroprotective and antibacterial effects of phlorotannins isolated from the cell walls of brown algae Fucus vesiculosus and Pelvetia canaliculata. Antioxidants. 2023;12(3):696. doi: 10.3390/antiox12030696
  28. AlgaeBase [Internet]. World-wide electronic publication, National University of Ireland, Galway [cited 2023 Sep 20]. Available at: https://www.algaebase.org
  29. Koivikko R, Loponen J, Pihlaja K, Jormalainen V. High-performance liquid chromatographic analysis of phlorotannins from the brown alga Fucus vesiculosus. Phytochem Anal. 2007;18(4):326–332. doi: 10.1002/pca.986
  30. Maron DM, Ames BN. Revised methods for the Salmonella mutagenicity test. Mutat Res Environ Mutagen Relat Subj. 1983;113(3–4): 173–215. doi: 10.1016/0165-1161(83)90010-9
  31. Andrews JM. Determination of minimum inhibitory concentrations. J Antimicrob Chemother. 2001;48(S1):5–16. doi: 10.1093/jac/48.suppl_1.5
  32. Mortelmans K, Zeiger E. The Ames Salmonella/microsome mutagenicity assay. Mutat Res Fund Mol Mech Mutag. 2000;455(1–2): 29–60. doi: 10.1016/s0027-5107(00)00064-6
  33. Wang Y, Xu Z, Bach SJ, McAllister TA. Sensitivity of Escherichia coli to seaweed (Ascophyllum nodosum) phlorotannins and terrestrial tannins. Asian-Australas. J Anim Sci. 2009;22(2):238–245. doi: 10.5713/ajas.2009.80213
  34. Iken K, Amsler CD, Amsler MO, et al. Field studies on deterrent properties of phlorotannins in Antarctic brown algae. Bot Mar. 2009;52(6):547–557. doi: 10.1515/BOT.2009.071
  35. Deniaud-Bouët E, Kervarec N, Michel G, et al. Chemical and enzymatic fractionation of cell walls from Fucales: insights into the structure of the extracellular matrix of brown algae. Ann Bot. 2014;114(6):1203–1216. doi: 10.1093/aob/mcu096
  36. Lemesheva V, Tarakhovskaya E. Physiological functions of phlorotannins. Biol Comm. 2018;63(1):70–76. doi: 10.21638/spbu03.2018.108
  37. www.ema.europa.eu [Internet]. ICH guideline S2 (R1) on genotoxicity testing and data interpretation for pharmaceuticals intended for human use — Scientific guideline [cited 2023 Sep 20]. Available at: https://www.ema.europa.eu/en/ich-s2-r1-genotoxicity-testing-data-interpretation-pharmaceuticals-intended-human-use
  38. Patrineli A, Clifford MN, Ioannides C. Contribution of phenols, quinones and reactive oxygen species to the mutagenicity of white grape juice in the Ames test. Food Chem Toxicol. 1996;34(9):869–872. doi: 10.1016/s0278-6915(96)00048-8
  39. Calvo TR, Demarco D, Santos FV, et al. Phenolic compounds in leaves of Alchornea triplinervia: anatomical localization, mutagenicity, and antibacterial activity. Nat Prod Commun. 2010;5(8): 1225–1532. doi: 10.1177/1934578X1000500816
  40. de Mejía EG, Castaño-Tostado E, Loarca-Piña G. Antimutagenic effects of natural phenolic compounds in beans. Mutat Res Genet Toxicol Environ Mutag. 1999;441(1):1–9. doi: 10.1016/s1383-5718(99)00040-6
  41. Bouguellid G, Russo C, Lavorgna M, et al. Antimutagenic, antigenotoxic and antiproliferative activities of Fraxinus angustifolia Vahl. leaves and stem bark extracts and their phytochemical composition. PLoS One. 2020;15: e0230690. doi: 10.1371/journal.pone.0230690
  42. Reid TM, Wang CY, King CM, Morton KC. Mutagenicity of some benzidine congeners and their N-acetylated and N, N’-diacetylated derivatives in different strains of Salmonella typhimurium. Environ Mutag. 1984;6(2):145–151. doi: 10.1002/em.2860060205
  43. Fragopoulou E, Nomikos T, Karantonis HC, et al. Biological activity of acetylated phenolic compounds. J Agric Food Chem. 2007;55(1):80–89. doi: 10.1021/jf0627221

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Figure. Representatives of major phlorotannin classes: fucols (1), phlorethols (2), fuhalols (3), eckols (4), and carmalols (5) [3]

Download (92KB)

Copyright (c) 2023 Eco-Vector

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
 


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies