1. Introduction
Macroalgae play an important role as components of the marine environment, providing many essential services to the coastal ecosystem engineering [
1], including global climate change mitigation [
2,
3], nutrient supply to the intertidal communities, and coastal protection from marine erosion [
1]. Seaweed encompasses the usually benthic, multicellular, and macroscopic algae [
4], and is classified into Division Chlorophyta (green macroalgae), Division Rhodophyta (red macroalgae), and Division Ochrophyta (brown macroalgae).
Algae inhabit intertidal, subtidal, and estuarine habitats, being exposed to multiple stressors, such as temperature, light, salinity, wave action, or even predation, competition, and parasitism. As an adaptive response, algae produce a large range of secondary metabolites [
4]. Algae are considered an outstanding source of valuable compounds, such as polysaccharides, vitamins, minerals, proteins, peptides and amino acids, pigments (chlorophylls, carotenoids, xanthophylls, or phycobiliproteins), phenolic compounds, and lipids, including the biological active n-3 long-chain (≥C20) polyunsaturated fatty acids (LC−PUFA) [
5,
6,
7,
8,
9]. Polysaccharides, peptides, carotenoids, and fatty acids (FA) have antiaging, antibiotic, and antioxidant activities [
8,
10,
11], while fucoxanthin, which is mainly present in brown macroalgae and diatoms, has demonstrated anti-obesity and lipolytic properties [
12,
13]. Among complex lipids, phospholipids and glycolipids, such as mono-galactosyl-diacylglycerol (MGDG), di-galactosyl-diacylglycerol (DGDG), and sulfoquinovosyl-diacylglycerol (SQDG), have been described as anti-inflammatory and anti-thrombotic agents [
14,
15]. Moreover, phytosterols (PTS) have interesting antioxidative, anti-inflammatory, and antilipidemic properties [
16], lowering the total and low-density lipoprotein (LDL) cholesterol levels in humans [
17]. Importantly, algae can biosynthesize LC−PUFA, such as eicosapentaenoic acid (EPA; 20:5n-3), docosahexaenoic acid (DHA; 22:6n-3), and arachidonic acid (ARA; 20:4n-6), and their PUFA precursors, alpha-linolenic acid (ALA; 18:3n-3) and linoleic acid (LA; 18:2n-6) [
18]. LC−PUFA have been proven to prevent a panel of human pathologies, such as colon and breast cancers, and neurodegenerative or inflammatory disorders [
18,
19]. As a result, consumers’ demand for algal products is increasing significantly with the rising evidence supporting the nutritional and health benefits of seaweed consumption. Several indices have been established for evaluating the nutritional value of food products based on their FA composition. Among them, the atherogenicity index (AI) and thrombogenicity index (TI), and the ratio between hypocholesterolemic and hypercholesterolemic FAs (hH) are the most commonly used indicators [
20].
Additionally, seaweeds are gaining global recognition within the context of transitioning to an environmentally friendly blue bioeconomy. Thus, the use of macroalgae as raw material in food and feed industries, nutraceuticals, natural cosmetics, bio-based materials (biopolymers and bioplastics), and biofuels, or for the extraction of pharmaceutical, biomedical, and biotechnological resources (alginate, agar–agar, and carrageenan) [
9,
21,
22,
23,
24], is receiving growing attention. Furthermore, algae are acquiring greater acceptance as fertilizers and plant bio-stimulants or as instruments for bioremediation and biomonitoring [
25,
26,
27].
Seaweed farming, practiced in a relatively small number of countries predominantly in Eastern and Southeastern Asia, together with the collection of naturally occurring marine beach-casts and their transformation into a marketable product, are complementary strategies to cope with the global demand for algae. Seaweed aquaculture—which is already the most important source of macroalgae worldwide [
28]—offers the opportunity for a more controlled production of target species, resulting in a predictable production outcome. In contrast, the variability in the taxonomic composition and biochemical properties of beach-cast biomass has the potential to offer a broader range of biochemical and bioactive compounds with possible synergistic activity and complementary functions, compared to monospecific biomass. Moreover, the accumulation of large amounts of beach-cast seaweeds on beaches represents an environmental problem, mainly related to the decomposition of the biomass, which can produce anoxic layers and threaten the survival of coastal communities. It can also cause economic damage in touristic areas, where large algal biomass deposition and bad odors are usually unpleasant for beach users [
1]. Consequently, beach-cast macroalgae are often removed by local governments, transported, and dumped in landfills, and ultimately wasted, creating the need for developing new strategies to optimize the management and use of this biomass [
1,
9,
21,
22,
29]. Therefore, the utilization of beach-cast seaweed is especially interesting because it allows the valorization of a waste into a resource, enabling not only to avoid the costs for the generation of biomass ex novo through aquaculture, but also to prevent economical losses related to waste management. In this sense, seaweed wracks could be a potential source of n-3 LC−PUFA in a global scenario of reduced availability of these compounds due to global warming and fish stock reduction [
30]. However, the seasonal and geographical variation of the composition and nutritional value of algal biomass, together with the reduced digestibility and bioavailability of many beneficial seaweed compounds to humans or animals [
28], slow down the development of this potential industry [
25,
28,
31].
The main objective of this study is to characterize the lipid and FA profiles of 12 seaweed species present in the still understudied macroalgal wracks from Gran Canaria Island coasts. In particular, it is intended to evaluate their potential as sources for both n-3 LC−PUFA and other healthy lipid molecules for human and animal nutrition, encouraging the efficient management of marine resources in coastal communities.
4. Discussion
The global demand for seafood products, including macroalgae, has been steadily increasing in the last decades, mainly due to the rising awareness of the population about their important nutritional properties [
41]. In macroalgae, the lipid levels are generally low (0.2–8% DW) and highly variable intra- and inter-specifically, being influenced by season, environment, or geographic origin, among others [
42]. Overall, the set of beach-cast seaweeds analyzed here presented lipid contents in line with values previously reported in the existing literature [
5,
43]. Among the 12 macroalgae studied, the two Chlorophyta species, together with
Dictyota sp. and
T. atomaria (Ochrophyta), stood out for their higher lipid proportions (2–3% DW).
Despite the reduced abundance of lipids, macroalgae possess a wide variety of bioactive lipid compounds, exhibiting a broad spectrum of health benefits for humans [
41,
44]. In particular, antioxidant, antifungal, antiviral, fibrinolytic, and antitumor activities have been described for phospholipids and glycolipids from seaweeds [
14,
45,
46]. The high biological activity of these molecules seems to be closely related to the structural features of the glycosyl and acyl chains [
15]. In this sense, the two green macroalgae analyzed here clearly differed in their glycolipid profiles. Interestingly, high SQDG and DGDG levels were found exclusively in
C. barbata (
Table 2), in agreement with values previously reported for two other Chlorophyta species,
Dasycladus vermicularis and
Ulva sp. [
5]. Also, glycolipid levels were very variable within the red macroalgae of our study [
47], emphasizing the highest proportions of SQDG and MGDG in
Asparagopsis sp. (9.1 and 5.6% of TL, respectively) and of DGDG in
H. spinella (4.9% of TL;
Table 3). In contrast, the four Ochrophyta species showed similar contents of glyceroglycolipids (
Table 4), preventing them from being considered as a valid taxonomic character within this group of macroalgae [
46]. However, the relevant abundance of SQDG in
Stypocaulon sp. and
T. atomaria (>8% of TL) must be stressed.
PTS are essential components of eukaryotic life, regulating the fluidity and permeability of cellular membranes [
48], which cannot be biosynthesized by humans [
49]. The Food and Drug Administration (FDA) from the U.S. Department of Health and Human Service (HHS) specifies that the daily dietary intake of PTS may reduce the risk of coronary heart disease (CHD), as their LDL cholesterol-lowering properties have been demonstrated [
50]. Thus, the higher the dietary intake of plant sterols, the lower the intestinal absorption of cholesterol, and the lower the serum cholesterol level [
49,
51]. Remarkably, PTS exceeded 12% of TL in all studied species, particularly
A. stellata,
J. rubens,
Liagora sp., and
Asparagopsis sp., with values of 20–23%.
Algae are a natural source of PUFA, especially the physiologically important omega-3 FA. The FA profile is characteristic of each macroalga species and may change depending on factors such as season and/or growth conditions [
41,
42]. Despite this, green macroalgae usually have similar FA patterns to terrestrial plants, with higher proportions of C16 and C18 FA [
49,
52,
53]. Accordingly, both
C. barbata and
A. stellata were rich in 16:0, 18:1n-9, LA, and ALA, despite the remarkable differences existing between their FA profiles. In addition,
C. barbata had notable proportions of 16:2n-4 (~7%) and 18:3n-6 (~10%). Even though 16:2n-4 has been previously cited in some diatoms [
54] and green microalgae [
55], its proportion in
C. barbata is striking and may suggest a taxonomic character that requires further study. Moreover, gamma linolenic acid (18:3n-6), together with its elongation product dihommo−gamma linolenic acid (20:3n-6), have been pointed out as important nutraceutical compounds for preventing the development of atherosclerosis [
56].
Green macroalgae usually lack the physiologically important LC−PUFA, especially DHA [
57]. Interestingly,
C. barbata presented ~2% of DHA, and
A. stellata contained ~7% and ~9% of ARA and EPA, respectively, which are valuable compounds for animal health and well-being. The red macroalgae species in our work presented an FA profile consistent with previous studies, where 16:0, 18:1n-9, ARA, and EPA were the major components [
5,
58,
59]. Thus,
H. spinella showed the highest abundance of ARA (~5%), while both DHA and EPA were remarkably high in
Jania sp. (~4% and ~6%, respectively;
Table 6). In contrast,
J. rubens contained low amounts of EPA (~1%) and no DHA, thus strengthening the hypothesis of high inter-specific and intra-generic variations in the FA composition of macroalgae. In accordance with our study, brown algae were characterized by moderate–high proportions of C14 and C16 SFA, 18:1n-9, ARA, EPA, and SDA [
41,
53,
60,
61]. It is also noticeable that DHA was not detected in any of the four brown species analyzed, but
Lobophora sp. and
Dictyota sp. were rich in other n-3 PUFAs, such as EPA (6.12 ± 0.97%) and SDA (4.28 ± 0.16%), respectively. SDA is a metabolic intermediate in the n-3 LC−PUFA biosynthetic pathway with similar beneficial physiological effects as EPA [
62], enhancing the presence of n-3 PUFA in tissues [
63]. SDA has been previously stated as particularly abundant in
Dictyota dichotoma [
5]. Finally,
T. atomaria and
Dictyota sp. showed remarkably high contents of 16:1n-5 (~18% and ~6% of total FA, respectively), a quimiotaxonomic FA from the genera Dictyopteris and Dictyota [
64]. The high content of this C16 MUFA in
T. atomaria points to its broader presence in genera of brown macroalgae other than those already reported in the literature.
Western diets currently have an n-6/n-3 ratio of 10–20/1, which is clearly far from the balanced 1–2/1 ratio of the Paleolithic period. Consequently, current occidental society intake of n-3 PUFA is generally insufficient, whereas that of n-6 PUFA should be reduced [
65,
66]. Unbalanced n-6/n-3 ratios strengthen systemic inflammation and overweight [
67], and at the same time, compromise the n-3 LC−PUFA biosynthesis [
68]. It has been proposed that the optimal dietary n-6/n-3 ratio should vary between 1:1 and 5:1 for good health and well-being [
69]. In this sense, all macroalgae covered in our study had beneficial n-6/n-3 ratios and could potentially contribute to reducing the dietary n-6/n-3 ratio in the occidental population. Furthermore, particularly interesting macroalgae, such as
Jania sp., could likely be considered as an additional natural source of n-3 LC−PUFA.
The dietary FA composition has implications in determining the risk factors of several pathologies, including cardiovascular diseases [
19], namely ischemic heart disease and stroke. In this sense, AI, TI, and hH are analytical indicators commonly used to assess the nutritional quality of ingested lipids based on their FA profile, and their potential effects to human health [
20,
70]. AI and TI are powerful predictors that characterize the atherogenic and thrombogenic potential of FA, respectively [
20]. Thus, AI measures the proportion of pro- and anti-atherogenic FAs, evaluating the proportions between FA that favor the adhesion of lipids to cells of the immunological and circulatory systems and FA that inhibit the aggregation of lipid plaques. TI shows the tendency to form clots in the blood vessels [
71]. The hH ratio assesses the effect of hypocholesterolemic and hypercholesterolemic fatty acids on cholesterol metabolism [
72], as the hypocholesterolemic FAs diminish the LDL cholesterol, while hypercholesterolemic FAs raise it. Low values of AI and TI and high values of hH are considered cardiovascular health promoters, preventing thrombosis and atherosclerosis [
70]. Overall, all macroalgae studied here showed AI, TI, and hH values in line with those reported in existing literature [
5,
20], yet both green algae displayed the most favorable cardiovascular health indicators (
Table 8).
The different clusters obtained in both dendrograms (
Figure 1 and
Figure 2), based on the lipid class and FA composition of macroalgae, evidenced a unique lipid signature for each species. As a result, it is complicated to determine the best macroalgae species from beach-cast seaweeds for practical use in creating valuable biologically active food and feed additives for human consumption and animal husbandry. In spite of this, more than 1000 tons wet weight/year of macroalgal wracks were collected in 2018 and 2019 from Las Canteras beach, in line with previous studies conducted in the same area between 1994 and 2007 [
73]. After eliminating water, sand, and other undesirable materials, the average dry vegetal matter represented nearly 10% of the initial weight; that is, 100 tons per year. Based on the PUFA and EPA + DHA contents (
Table 5 and
Table 7) of the three most abundant macroalgal species collected during 2018 and 2019:
Lobophora sp. (41.8% of total biomass),
Dictyota sp. (16.4%), and
C. barbata (14.8%;
Supplementary Table S1), it is estimated that a total of 55 kg of PUFA and 7.6 kg of n-3 LC−PUFA would be obtained per year through the collection of algal wracks from this specific area. In this context, the use of macroalgae as a dietary supplement in several industries, such as cattle raising, in which they have recently been used at low percentages, might be interesting [
74,
75]. In fact, similar macroalgal wracks collected from the same area have been used as a feed additive for
Ctenopharyngodon idella and
Sparus aurata, with encouraging results [
21,
22]. However, seasonal and geographical variations, as well as potential hydrolytic and oxidative rancidity due to degradation processes, which may affect the lipid composition of macroalgal wracks, should also be considered in further studies, as well as by biotechnological companies that might be interested in exploiting this biological resource. Additionally, it should be noticed that beach-cast seaweeds’ compositions in the Northeast Atlantic have very recently and unexpectedly changed due to the proliferation of the invasive
Rugolopteryx okamurae, which has caused massive stranding events [
76]. It remains to be clarified whether
R. okamurae has a similar lipid profile as
Dictyota sp., with which it shares the taxonomic (Dictyotales and Ochrophyta) and morphological features, and whether its use for nutritional purposes can be envisaged [
77].