Improving potential strategies for biological activities of phlorotannins derived from seaweeds

Figures & data

Figure 1. The example structures of phlorotannins, divided by their linkages and functional groups.

Figure 2. Potential biosynthesis pathway of phlorotannin in brown seaweed cells (Gómez and Huovinen 2020; Phang et al. 2023). PKS: polyketide synthase; CoA: coenzyme A.

Table 1. Phlorotannin content among different seaweed species by different determination methods.

Seaweed species	Collection spots	Collection time	Extraction method	Contents (mg PGE/g DW)	References
Spectrophotometry assays
Folin–Ciocalteu assay
Fucus vesiculosus L.	Oskar Bay, Zelenetskaya Gulf, Barents Sea, Russia	August 2017	Extracted by NADES, dissolved (50–70%) in H2O and solvents of various polarities that were used to extract the phenolic compounds (40 and 96% ethanol, Me2CO, 70% aqueous Me2CO) for 2 h at 50 °C	8.7–61.2	(Obluchinskaya et al. 2019)
Ascophyllum nodosum (L.) Le Jolis				7.8–50.3
F. vesiculosus	Donegal, Ireland	(Not Specified)	30%, 50%, 70% ethanol with a sample-to-solvent ratio of 1:10 (w/v) for 4 h at 20 °C with pretreated by 0, 35 and 130 kHz ultrasonic for 10 and 30 min	382.1–568.9	(Ummat et al. 2020)
F. vesiculosus	Coastal zone of the Artic: Irminger Sea, Norwegian Sea, Barents Sea, and White Sea	Fertile and sterile phases in 2019	60% methanol with a sample-to-solvent ratio of 1:25 (w/v) for 24 h at 200 rpm	72.4–158.1	(Obluchinskaya et al. 2022)
F. vesiculosus	Donegal, Ireland	November 2017	Applied UAE, MAE, UMAE, HAE and HPAE with 50% ethanol at a sample/solvent ratio of 1:10 (w/v) by with post-treatment of 0 h and 24 h	238.7–362.9	(Garcia-Vaquero et al. 2021)
Pelvetia canaliculata				128.3–203.9
Polycladia myrica	Hurghada, Red Sea	Winter 2020	Pre-removed lipids by adding hexane with a sample-to-solvent ratio of 1:5 (w/v), and add 50 mL of 70% acetone containing 0.3% w/v ascorbic acid to the sample for 1 h	57.52 ± 1.2	(Ismail et al. 2023)
Sirophysalis trinodis				55.58 ± 1.6
Dictyota spiralis				48.75 ± 2.1
Sargassum euryphyllum				56.13 ± 1.4
Turbinaria decurrens				43.75 ± 1.2
2,4-Dimethoxybenzaldehyde assay
Phyllospora comosa	Queenscliff Harbor, Victoria, Australia	February (summer)	Conventional extracted and using UAE with 70% methanol, 70% ethanol, 70% acetone, and absolute ethyl acetate	0.33–6.65	(Subbiah, Ebrahimi, et al. 2023)
Ecklonia radiata				0.59–8.29
Durvillaea sp.				0.29–8.22
Sargassum sp.				0.54–6.32
Cystophora sp.				1.02–4.15
P. comosa	Queenscliff Harbor, Victoria, Australia	February 2022	70% ethanol (1:20, w/v) for 16 h at 120 rpm at 10 °C	0.03–0.38	(Subbiah, Duan, et al. 2023)
E. radiata				0.18–0.65
Durvillaea sp.				0.04–0.40
Sargassum sp.				0.11–0.46
Cystophora sp.				0.63–2.86
Sargassum vulgare	Stora, Skikda, northeastern Algeria	February 2018	70% acetone solution (1:70, w/v) for 3 h at room temperature	0.4–9.4	(Chouh et al. 2022)
P. myrica	Hurghada, Red Sea	Winter 2020	Pre-removed lipids by adding hexane with a sample-to-solvent ratio of 1:5 (w/v), and add 50 mL of 70% acetone containing 0.3% w/v ascorbic acid to the sample for 1 h	13.44 ± 0.4	(Ismail et al. 2023)
S. trinodis				11.22 ± 0.6
D. spiralis				9.05 ± 0.3
S. euryphyllum				10.92 ± 0.2
T. decurrens				9.94 ± 0.4
C. compressa	Cleopatra coast, Marsa Matruh city, Mediterranean Sea, Egypt	April 2017	Pre-removed lipids by adding hexane with a sample-to-solvent ratio of 1:5 (w/v), and add 50 mL of 70% acetone containing 0.3% w/v ascorbic acid to the sample for 1 h	140.5	(Gheda et al. 2021)
Prussian blue assay
P. comosa	Queenscliff Harbor, Victoria, Australia	February (summer)	70% methanol, 70% ethanol, 70% acetone, and absolute ethyl acetate by conventional extraction and UAE	0.13–12.62	(Subbiah, Ebrahimi, et al. 2023)
E. radiata				0.46–8.00
Durvillaea sp.				0.48–6.63
Sargassum sp.				0.12–7.77
Cystophora sp.				0.48–8.61
P. comosa	Queenscliff Harbor, Victoria, Australia	February 2022	70% ethanol (1:20, w/v) for 16 h at 120 rpm at 10 °C	0.17–25.35	(Subbiah, Duan, et al. 2023)
E. radiata				0.06–3.33
Durvillaea sp.				0.20–5.31
Sargassum sp.				0.34–6.01
Cystophora sp.				0.56–28.77
Nuclear magnetic resonance (NMR)
Cystoseira tamariscifolia	Penmarc’h, Brittany, France	From February 2009 to July 2010	50% methanol at 40 °C	0.07%–0.46% DW	(Jégou et al. 2015)
Laminaria digitata	Scotland	2015	80% methanol for 1.5 h under 20 °C	4.3% DW	(Vissers et al. 2017)
Laminaria hyperborea	Haugesund, Norway	March 2020, September 2020, and August 2021	50% ethanol for 30 min with pretreated by 35 kHz ultrasonic for 30 min	4.08–6.17	(Wekre, Hellesen Brunvoll, and Jordheim 2022)
L. digitata	Southern Australian coast, Melbourne, Victoria, Australia	August 2019		5.09 ± 0.01
F. vesiculosus	Storåkervika, Bergen, Norway	August 2019		11.0 ± 0.0
Saccharina latissima	Trollsøy, Vestland	June 2021		12.4 ± 0.0
A. nodosum	Eidsvåg, Bergen	September 2017		8.57 ± 0.0
High-performance liquid chromatographic (HPLC)
F. vesiculosus	Archipelago Sea, SW Finland	(Not Specified)	Soluble fraction: 70% acetone (1:50, w/v) for 1 h; Insoluble fraction: soluble fractions was further suspended in 8 mL of 1M NaOH solution (80 °C) and stirred for 2.5 h at room temperature	6.01–7.47	(Koivikko et al. 2008)
Ecklonia cava	Aewol-eup, Jeju-island, South Korea	(Not Specified)	50% ethanol (1:10, w/v) for 6 h at 60 °C	48.08 ± 0.67 mg dieckol/g	(Petchidurai et al. 2019)
E. cava Kjellman	Busan, South Korea	2009	Methanol (1:4, w/v) for 2 h at room temperature	7.25–24.15 µg dieckol/mL 5.82–19.41 µg phlorofucofuroeckol-A/mL	(Chowdhury et al. 2011)

Note: NADES: natural deep eutectic solvents; PGE: phloroglucinol equivalents; DW: dry weight of seaweed biomass; UAE: ultrasound-assisted extraction; MAE: microwave-assisted extraction; UMAE: ultrasound–microwave-assisted extraction; HAE: hydrothermal-assisted extraction; HPAE: high-pressure-assisted extraction.

Table 2. A brief summary of phlorotannin biological activities.

Bioactivities	Seaweeds	Phlorotannins	Models	Outcomes	References
Antioxidant	Undaria pinnatifida sporophyll (China)	Crude extracts	(Not Specified)	Approximately 40 µg/mL of phlorotannin extract showed similar antioxidant capacity to positive control (80 µg/mL of epigallocatechin gallate.	(Dong et al. 2019)
	Sargassum vulgare (Algeria)	Crude extracts and liquid-liquid purification fractions	(Not Specified)	DPPH: IC50 values ranged from 6.14 to 97.41 µg/mL. ABTS: IC50 values ranged from 1.29 to 93.76 µg/mL.	(Chouh et al. 2022)
	Fucus vesiculosus (Denmark)	Phlorotannin-rich extracts	(Not Specified)	EC50 of DPPH: 16.3–76.3 µg/mL.	(Hermund et al. 2022)
Anti-inflammatory	Ascophyllum nodosum (France)	Phlorotannin-rich extracts	Human epithelial cells (ARPE-19 and WKD cell lines)	A concentration of 0.2% effectively prevent the overproduction of ROS. A concentration of 0.05%, it reduced TNF-α release. A concentration of 0.2%, it reduced TNF-α and IL-6 release.	(Dutot et al. 2012)
	U. pinnatifida Sporophyll (China)	Phlorotannin-rich extracts	RAW 264.7 Macrophages	More efficient than epigallocatechin gallate at decreasing NO production.	(Dong et al. 2019)
	F. vesiculosus (Portugal)	Crude extracts & ethanolic extracts	RAW 264.7 Macrophages	Inhibit the NO production in a dose-dependent manner, decreasing to 14.08 ± 3.68 and 16.80 ± 6.32% in 100 µg/mL crude and ethanolic extract, respectively. However, at 200 µg/mL a decrease in cell viability indicates a cytotoxic effect. Down-regulation of iNOS expression and reduce the expression of COX-2 and IL-1β.	(Catarino et al. 2020)
	Eisenia bicyclis (Portugal)	Crude extracts	THP1 human monocytes	Reduce 43.5% of nitrite in the medium. Reduce 1.2-fold in IL-8 mRNA expression, and approximately 3.7-6-fold in the expression of TNF-α, IL-1β, IL-8, and IL-6. Increase 4-fold anti-inflammatory cytokine IL10 expression.	(Raja et al. 2023)
	Eisenia arborea (Japan)	6,6′-bieckol and 6,8′-bieckol	Mice	Significantly suppress mice ear swelling, with 35.7%–61.8% in 6,6′-bieckol and 55.7%–77.6% in 6,8′-bieckol.	(Sugiura et al. 2017)
Anti-allergy/ histamine	E. arborea (Japan)	Eckol, 6,6′-bieckol, 6,8′-bieckol, 8,8′-bieckol, phlorofucofuroeckol-A/-B	Rat mast cell line (RBL-2H3 cells)	Suppressed histamine release at a concentration of 100 mM, while phlorofucofuroeckol-B showing a suppressive ratio at 200 mM of 37.1%. Suppress PGE2 release at 10, 100, 200 mM.	(Sugiura et al. 2018)
	Eckolonia cava (South Korea)	Fucodiphloroethol G, eckol, phlorofucofuroeckol-A	Human leukemia cell line (KU812) & rat basophilic leukemia cell line (RBL-2H3)	KU812 – Reduced IgE induced stimulated histamine release to 23.97, 44.26, and 34.54% at the concentration of 100 mM. Reduced A23187 stimulated histamine release to 27.40, 61.15, and 37.05%, respectively. RBL-2H3 – A23187 stimulated: 27.73, 50.63, and 34.18%, respectively. Reduced β-hexosaminidase release to 18.02, 31.67, and 20.80%, respectively.	(Y. Li et al. 2008)
Anti-diabetic	E. bicyclis (Portugal)	Crude extracts	Mouse myoblast cell line (C2C12 cells)	Superiorly inhibit α-glucosidase inhibitory action with an IC50 of 31.7 ± 0.84 mg/mL, comparable to acarbose. Significantly inhibit glycation, PTP1B, α-glucosidase, and α-amylase activity. Increase glucose uptake by 51.09% (p < 0.05) under insulin-stimulated conditions.	(Raja et al. 2023)
	Sargassum linifolium (Egypt)	Phlorotannin-rich extracts	White albino male Wistar rats	Significant decrease in serum glucose levels. Promote the β-cell in the pancreas to secret insulin. Reduce glucosidase, α-amylase, and CAT levels. Lower the urea, creatinine, cholesterol and triglyceride levels. Activate of AMPK pathway and inhibit adipogenesis.	(Gheda et al. 2023)
	Cystoseira compressa (Egypt)	Phlorotannin-rich extracts	White albino Wistar rats	Significant reduce the blood glucose, urea, creatinine, cholesterol, and triglyceride levels compared to the diabetic control. Increase the insulin levels. Reduce the α-amylase and glucosidase activities. Increase CAT activity to decrease the hepatic lipid peroxidation.	(Gheda et al. 2021)
	Sargassum tenerrimum (India)	Phlorotannin-rich extracts	Wistar albino rats	Elevate insulin levels after 21 days of treatment (p < 0.001). Considerably improve oral glucose tolerance by 52% and 63% at 200 mg/kg and 400 mg/kg (p < 0.001). Reduced the production of the lipid oxidation product MDA level but increase SOD and CAT concentrations. Alleviate the TNF-α level.	(Vijay and Vellapandian 2023)
Anti-bacterial/microbial	Halidrys siliquosa (France)	Phlorotannin-rich extracts	Pseudomonas aeruginosa (ATCC 9027), Staphylococcus aureus (ATCC 6538), and E. coli (ATCC 8739)	Reduce higher than 5 log of the initial bacterial concentration with Pseudomonas aeruginosa and E. coli (<1 CFU/mL). 4.5 log reduction of the initial bacterial concentration of Staphylococcus aureus (75 CFU/mL).	(Le Lann et al. 2016)
	Hizikia fusiforme (China)	Phlorotannin-rich extracts	S. aureus (ATCC 25923), E. coli (ATCC 25922), P. aeruginosa (PAO1), Aeromonas hydrophila (YJ-1), and Vibrio parahaemolyticus (X-1)	The MIC of phlorotannins against the selected bacteria was: 0.1943 g/ml for C. violaceum and E. coli, and 0.0972 g/ml for S. aureus, A. hydrophilia, V. parahaemolyticus, and P. aeruginosa. Inhibit the formation of biofilm.	(Tang, Wang, and Chu 2020)
	F. vesiculosus & Pelvetia canaliculate (Russia)	Cell wall extracts & intracellular phlorotannin-rich extracts	E. coli (ATCC 25922), P. aeruginosa (ATCC 27853), Listeria monocytogenes (EGD), S. aureus (ATCC 25923), S. aureus (SG-511), methicillin resistant S. aureus (ATCC 33591), Micrococcus luteus (CIP A270)	Low or moderate antimicrobial activity for all extracts. Cell wall extracts exhibited higher antimicrobial activity in comparison to the intracellular phlorotannin-rich extracts. For E. coli and S. aureus (ATCC 25923) –Cell wall fraction (MIC = 31.2 µg/mL), intracellular fraction (MIC = 62.5 µg/mL), For methicillin resistant S. aureus–Cell wall fraction (MIC = 125 µg/mL), intracellular fraction (MIC = 500 µg/mL)	(Meshalkina et al. 2023)

Note: DPPH: 2-diphenyl1-picryl-hydrazine-hydrate; ABTS: 2,2-azino-bis-3-ethylbenzothiazoline-6-sulfonic acid; EC50: half maximal effective concentration; ROS: reactive oxygen species; NO: nitric oxide; iNOS: inducible nitric oxide synthase; COX-2: cycloocygenase-2; IL: interleukin; PGE2: prostaglandin E2; Ig: immunoglobulin; IC50: half maximal inhibitory concentration; PTP1B: protein tyrosine phosphatase 1B; AMPK: AMP-activated protein kinase; MDA: malondialdehyde; SOD: superoxide dismutase; CAT: catalase; TNF-α: tumor necrosis factor alpha; MIC: minimum inhibitory concentration.

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