Red and brown seaweeds extracts: A source of biologically active compounds
Graphical abstract
Introduction
The marine environment contains a vast array of organisms with unique biological properties. Among these organisms seaweeds are well documented in the literature as a source of bioactive compounds, which can be used in the preparation and development of functional foods and nutraceuticals. Seaweed bioactive compounds include pigments, lipids, proteins, polysaccharides and phenolics, which present biological activities such as antioxidant, antimicrobial, anticancer, anti-inflammatory, anti-diabetic and anti-obesity. Various extraction techniques can be used to obtain these bioactive compounds from algal biomass. The extraction yields and biological activities of the extracts are strongly dependent on the extraction method and the type of solvents used. Traditional extraction methods with solvents are the most used, however the rigid and complex structures of seaweed cell walls reduce the extraction efficiency. Thus, new extraction methods such as enzyme-assisted extraction (EAE) and mechanochemically-assisted extraction (MAE) have been proposed as alternatives to the traditional solvent extraction, in order to improve the yield and to preserve the bioactive properties of the extracted compounds. Furthermore, these methods are safe and more environmentally friendly.
Ball milling (BM) is a mechanical technology applied to improve the extraction by disrupting algal cells through a multi-directional, simultaneous beating of balls or beads on the sample to release compounds into the surrounding solvent (Wang et al., 2016). This method has been used successfully in the extraction of natural compounds from plants (Wang et al., 2016) and significantly decreases processing time and solvents consumption.
Several studies have demonstrated that EAE is characterised by high extraction rates and high yields, being an economical and sustainable methodology (Rodrigues et al., 2015). Bioactive compounds are sometimes bound to or embedded within larger polymers, which hinder their release during solvent extraction. Thereby, enzymes can aid in breaking down these polymers and release these compounds. The use of enzymes such as cellulases, hemicellulases, β-glucanase, and xylanases has been described as a food-grade approach to breakdown the complex seaweeds cell wall. However, the choice of carbohydrase(s) and the optimization of the hydrolysis conditions, such as enzyme-substrate ratio, temperature, hydrolysis time, agitation speed, and pH, are critical in order to maximize the yield in terms of bioactive compounds recovery (Gligor et al., 2019).
Antioxidants from seaweeds have been widely studied because they may be safer and more effective than synthetic ones, which may exhibit some harmful effects. Antioxidants present in many seaweeds play an important role in the prevention of various diseases and ageing processes through protection of cells from oxidative damage (Farvin & Jacobsen, 2013). Carotenoids (fucoxanthin and astaxanthin), polyphenols (phenolic acid, flavonoids and tannins), sterols, carbohydrates and vitamins (E and C) are among the most well known antioxidants.. Moreover, proteins (phycobiliproteins) and peptides or aminoacids (mycosporine-like aminoacids) also show antioxidant properties. Several red and brown seaweed species have presented antioxidant activity, with the latter being reported to have higher antioxidant potential, possibly due to the presence of phenolic compounds, optimally extracted with water (Farvin and Jacobsen, 2013, Dang et al., 2018, Vega et al., 2020).Furthermore, crude water and enzymatic extracts from brown seaweed showed radical scavenging and ferrous ion chelating activities (Balboa et al., 2013).
Diabetes and hypertension are two significant chronic metabolic diseases that represent the biggest causes of death worldwide. Since the available oral drugs cause several adverse effects, it is worth searching for natural compounds, without side effects, that may benefit patients. Investigations have demonstrated that brown and red seaweeds contain bioactive compounds (for example phlorotannins and fucoxantin) with promising anti-diabetic properties, which operate through different mechanisms, such as the inhibitory effect of enzyme targets like α-amylase and α-glucosidase (Lordan et al., 2013). On the other hand, it was shown that peptides released from seaweed proteins by enzymatic hydrolysis exhibited Angiotensin-Converting-Enzyme (ACE) inhibitory activity. Several studies reported the isolation of ACE inhibitory peptides from seaweeds and their application in hypotensive commercial products as reviewed by Seca and Pinto (2018). Furthermore, phlorotannins, phenolic compounds bound to proteins and released during enzymatic hydrolysis are also excellents ACE inhibitory compounds. Additionally, seaweeds are also promising sources of antimicrobial agents due to several compounds (fatty acids, polysaccharides, alkaloids, terpenes, phenols, steroids, phlorotannins and carotenoids). Several studies have revealed the efficacy of red seaweed extracts against Gram (+) and (−) bacteria (El-Shafay et al., 2016).
Thus, the objective of this work was to evaluate the biological activities (antioxidant, anti-diabetic, anti-hypertensive and antimicrobial) of red (Porphyra sp. and Gracilaria gracilis) and brown (Alaria esculenta and Saccharina latissima) seaweed extracts, obtained using the following methods: enzyme-assisted (Alcalase, Viscozyme and Cellulase), hot water and ball milling.
Section snippets
Seaweed species
Red seaweeds, Porphyra sp. and G. gracilis, were harvested in June 2019 (Cabo Mondego, Figueira da Foz, Portugal). Brown seaweeds, S. latissima and A. esculenta, were harvested respectively in September 2019 (Viana do Castelo, Portugal) and June 2019 (Bantry bay, Cork, Ireland). The seaweeds were washed with seawater, then twice with distilled water and freeze-dried. The dried seaweeds were milled with a MM400 Mills (Retsch, Haan, Germany).
Seaweed extracts: Mechanochemical- and enzyme-assisted extractions
Mechanochemical extraction, using a ball mill (BM), hot
Principal components analysis
In order to detect similarities/differences among seaweed species a PCA was performed using the data from the tested extraction methods and from the analysis of extraction yield, TPC and TFC and biological activities. The first principal component (PC1, 35.57% of the total explained variance) was correlated with ACE inhibitory activity (loading −0.84), DPPH (-0.82) radical scavenging activity, TPC (-0.75), Cu2+ chelating activity (-0.74), RP (-0.65) and ABTS radical scavenging activity (0.84) (
Conclusions
This study is a contribution for the valorization of several seaweeds species as a result of their biological activities. The results of this study showed that enzyme-assisted extraction was the most effective allowing to obtain the highest yields. In general, EAA exhibited the highest chelating activity and inhibitory activities of α-glucosidase and ACE. None of the extracts showed antimicrobial activity against the tested bacteria. Due to the biological activities evaluated in Porphyra sp.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgment
This work was financially supported by the Interreg Atlantic Area project SEAFOOD-AGE (EAPA_758/2018) and the National project I9 + PROALGA (Mar2020, Ref.: 16-01-03-FMP-0011). The authors are grateful to Professor Leonel Pereira and João Cotas (University of Coimbra) for the collection and identification of seaweeds.
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