Preparation methods, biological activities, and potential applications of marine algae oligosaccharides: a review

Lixin Zheng; Yang Liu; Shijie Tang; Wancong Zhang; Kit-Leong Cheong

doi:10.1016/j.fshw.2022.07.038

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Review Article | Open Access

Preparation methods, biological activities, and potential applications of marine algae oligosaccharides: a review

Lixin Zheng^{^a}, Yang Liu^{^a}, Shijie Tang^{^b}, Wancong Zhang^{^b}(), Kit-Leong Cheong^{^a}()

Guangdong Provincial Key Laboratory of Marine Biotechnology, Department of Biology, College of Science, Shantou University, Shantou 515063, China

Department of Plastic Surgery and Burn Center, The Second Affiliated Hospital, Shantou University Medical College, Shantou 515063, China

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Abstract

Marine algae are valuable sources of health-promoting molecules that have been consumed by Asians for decades. Among aquatic flora, marine algae stand out in terms of high content of marine algae polysaccharides (MAP) such as carrageenan, alginate, fucoidan, laminaran, agarose, rhamnan, and ulvan. When hydrolyzed, MAP generate marine algae oligosaccharides (MAO), which have attracted interest in recent years due to their superior solubility compared with MAP. Besides, MAO have been demonstrated numerous biological activities including antioxidant, antidiabetic, anti-inflammatory, antimicrobial, and prebiotic activities. Thus, this review summarizes the main chemical classes of MAO, their sources, and the main processes used for their production (i.e., physical, chemical, and biological methods), coupled with a discussion of the advantages and disadvantages of these methods. Highlights of the biological activities of MAO and their potential applications in food, nutraceutical, and pharmaceuticals would also be discussed and summarized.

Keywords

Marine algae MAO Preparation methods Biological activities Potential applications

References

[1]

M.A. Hannan, A.A.M. Sohag, R. Dash, et al., Phytosterols of marine algae: insights into the potential health benefits and molecular pharmacology, Phytomedicine (2020) 153201. https://doi.org/10.1016/j.phymed.2020.153201.

Marine algae	Oligsoaccharides	Sources	Mode of production	Reaction conditions	Yield	References
Red seaweed	Agaro	Gracilaria	Enzymatic methods: agarase	Incubated at 40 ℃ with 800 r/min horizontal shaking	-	[36]
	Agaro	Gelidium amansii	Enzymatic methods: agarase	Incubated at 40 ℃ for 7 h	-	[110]
	Agaro	Gracilaria fisheri	Acid hydrolysis	Hydrolyzed with 0.5% acetic acid under high pressure at 130 ℃ in a hydrothermal reactor	-	[67]
	Agaro	Gracilaria lemaneiformis	Acid degradation;Biofermentation: Flammeovirga pacifica WPAGA1;	0.6 mol/L Hydrochloric acid was added and heated at 50 ℃ for 6 h;Liquid medium shaking at 200 r/min at 37 ℃ for 42 h	-	[23,111]
	Carrageenan	Euchema striatum and Kappaphycus alvarezii	Microwave irradiation	Subjected to microwave irradiation at 140, 150 and 160 ℃ for 2, 5, 10, 20 and 30 min	56% and 40%, respectively	[42]
	Carrageenan	-	Biofermentation: in vitro gastric digestion	Simulated gastric digestion with pH 1.0 at 37 ℃ for 3 and 6 h	(6.22 ± 1.05)% and (10.32 ± 2.09)%	[112]
	Carrageenan	-	Acid hydrolysis	0.1 mol/L TFA 65 ℃ for 3 h		[113]
Brown seaweed	Alginate	Laminaria japonica	Enzymatic methods: alginate lyase;Enzymatic hydrolysis and fermentation: cellulase and engineered yeast strain	Incubated at 37 ℃ for 6 h; Hydrolyzed by 3% cellulase and fermented by the engineered yeast strain for 72 h	-29.9 g/L	[110,114]
	Alginate	-	Gamma irradiation	⁶⁰Co gamma rays in the dose range of 20–100 kGy	-	[115]
	Alginate	-	Microwave degradation	hydrolyzed under microwave irradiation (1600 W) at 130 ℃ for 15 min	71%	[116]
	Alginate	-	Enzymatic methods: alginate lyase Alg2A	Dissolved in 1.5 mL 20 mmol/L Tris-HCl aqueous buffer (pH 8.5) and incubated at 45 ℃ for 0, 5, 10, 15, 20 and 25 min, respectively	-	[117]
	Fuco	Saccharina japonica	Acid hydrolysis	Dissolved in 0.6 mol/L HCl and incubated at 80 ℃ to degrade for 2 h	-	[64]
	Fuco	Sargassum confusum	Enzymatic hydrolysis: α-amylase, cellulose, pectinase and xylanase	Incubated at 51 ℃ and pH 6.2 for 3.9 h	-	[76]
	Fuco	Schizymenia binderi	Chemical method: H₂O₂	9% H₂O₂ solution was added at 12 mL/h at 60 ℃	50%	[118]
	Laminaran	Ecklonia stolonifera	Acid hydrolysis	10 volumes of 0.1 mol/L HCl was added and stirred for 20 min at room temperature	-	[119]
	Laminaran	Eisenia bicyclis	Acid hydrolysis	0.1 mol/L HCl for 2 h at 60 ℃ (twice) using a solid-to-solvent ratio of 1:12.5 (m/V)	1.6 g/100 g	[120]
	Laminaran	Laminaria japonica	Enzymatic methods: endo-β-(1→3)-glucanase from Bacillus circulans	Hydrolyzed in 0.05 mol/L citrate buffer (pH 5.4) at 50 ℃ for 0–24 h	-	[121]
Green seaweed	Rhamnan	Iterative glycosylation with disaccharides	Biosynthesis	Alternating α-(1→2)/(1→3)-linkages and repeating α-(1→3)-linkages by iterative α-glycosylation using disaccharide building blocks	-	[19]
	Rhamnan	Monostroma latissimum	Acid hydrolysis	Hydrolyzed with 0.1 mol/L H₂SO₄ at 60 ℃ for 3 h	-	[122]
	Ulvan	Ulva lactuca	Chemical method: H₂O₂	Degraded with 30% hydrogen peroxide and ascorbic acid at 70 ℃ for 3 h	-	[123]
	Ulvan	Ulva ohnoi	Enzymatic methods: ulvan-lyase	Hydrolyzed in buffer (pH 8) at 35 ℃ for 20 h	39.8%	[18]

Marine algae	Oligsoaccharides	Sources	Stage of trial	Concentration	Biological activities	References
Red seaweed	Agaro	Gelidium amansii	In vitro fermentation:Pig fecal microbiota	5 mg/L	Regulated the gut microbial;Prevented gut disease	[110]
	Agaro	Gracilaria fisheri	In vivo:Acetic acid-induced colitis mice	100, 500 and 1000 mg/kg	Prevented and attenuated colitis symptoms and gastrointestinal dysmotility;Reduced populations of harmful bacteria;Increased SCFAs production	[67]
	Agaro	Gracilaria lemaneiformis	In vivo:Kunming mice	50, 150 and 250 mg/kg	Antioxidant;Attenuated alcohol-induced hepatopathy;Enhanced the activities of hepatic alcohol dehydrogenase	[111]
	Carrageenan	Kappaphycus alvarezii	In vitro fermentation:Pig fecal microbiota	3 mg/L	Altered the overall fecal microbiota structure;Increased the abundance of butyric acid producing bacteria	[110]
	Carrageenan	-	In vitro fermentation:Human fecal microbiota	Final concentration of 1%	Increased inflammatory effects on HT29 cells;Maintained secretion of pro-inflammatory cytokines and SIgA, mucin2	[112]
	Carrageenan	-	In vitro:LPS-treated BV-2 cells	125–500 μg/mL	Decreased the levels of TNF-α;Anti-inflammatory effects	[60]
Brown seaweed	Alginate	Laminaria japonica	In vitro fermentation:Pig fecal microbiota	5 mg/L	Regulated the gut microbial;Prevented gut disease;Inhibited the growth of pathogenic bacteria	[110]
	Alginate	-	In vitro:IPEC-J2 cells	10 and 100 μg/mL	Benefited cell integrity and cell migration;Improved small intestinal mucositis	[124]
	Alginate	-	In vitro:Human umbilical vein endothelial cells	200 µg/mL	Alleviated H₂O₂-induced cell cytotoxicity and apoptosis;Inhibited H₂O₂-induced oxidative stress	[125]
	Fuco	Sargassum confusum	In vivo:Healthy male Syrian golden hamsters	Gavaged with 150  mg/kg	Antidiabetic;Regulated gut microbiota in obese and diabetic individuals	[76]
	Fuco	Saccharina japonica	In vitro fermentation:human fecal microbiota	Final concentration of 1%	Modulate gut microbiota and the growth of beneficial colonic bacterial populations	[64]
	Fuco	-	In vitro:Human dermal fibroblasts	10 mg/mL	Inhibited the passage-dependent upregulation of elastase-type activity	[126]
	Laminaran	Laminaria japonica	In vitro:Mouse thymocytes of 4-week-old female BALB/c mice;	1−4 mg/mL	Inhibited the apoptosis of thymocytes and immunomodulatory	[121]
Green seaweed	Rhamnan	-	In vitro:Human dermal fibroblasts	10 mg/mL	Inhibited the passage-dependent upregulation of elastase-type activity	[126]
	Ulvan	Genus Ulva	In vitro:RAW264.7 cells	100 μg/mL	Promotion of cell viability;Immunomodulatory;Anti-inflammatory	[127]
	Ulvan	Ulva lactuca	In vivo:SAMP8 mice and SAMR1 mice	150  mg/(kg·day)	Prevented apoptosis;Anti-ageing	[9]