Seaweeds: History
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Subjects: Biochemistry & Molecular Biology
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Diane Purcell-Meyerink

Seaweeds have a long history of use as food, as flavouring agents, and also used in traditional folk medicine. Seaweed products range from food, feed, and dietary supplements to pharmaceuticals, and from bioenergy intermediates to materials. At present, 98% of the seaweed required by the seaweed industry is provided by five genera and only ten species. The two brown kelp seaweeds Laminaria digitata, a native Irish species, and Macrocystis pyrifera, a native New Zealand species, are not included in these eleven species, although they have been used as dietary supplements and as animal and fish feed. The properties associated with the polysaccharides and proteins from these two species have resulted in increased interest in them, enabling their use as functional foods. Improvements and optimisations in aquaculture methods and bioproduct extractions are essential to realise the commercial potential of these seaweeds.

  • aquaculture
  • seaweed
  • Laminaria digitata
  • Macrocystis pyrifera
  • extraction

1. Introduction

Nearly three hundred seaweed species of interest have been identified for their potential commercial value [1], yet only ten are cultivated extensively with a handful of other species grown for niche applications. These include three brown seaweeds Saccharina japonica, Undaria pinnatifida, and Sargassum fusiforme (Ochrophyta, Phaeophyceae); four red seaweeds Neopyropia/Pyropia/Porphyra spp., Eucheuma spp., Kappaphycus alvarezii, and Gracilaria spp. (Rhodophyta); and five green seaweeds Ulva clathrata (formerly Enteromorpha clathrata), Monostroma nitidum and Caulerpa spp., Ulva spp., Oedogonium termedium (Chlorophyta) [2]. The brown seaweed commonly called Japanese kelp, Saccharina japonica, formerly known as Laminaria japonica, was the most cultivated seaweed in the world until 2010. It still retains a considerable market share, commanding 29% of global production in 2014 and over 33% in 2018 [3][4]. However, in 2010, production of Eucheuma/Kappaphycus surpassed 9.07 million tonnes with a value of over EUR 1,079 million [5], and by 2014, Eucheuma (35%) and Kappaphycus (6%), collectively at 41% global production, were the most cultivated species [3]. In the context of the cultivation advantage gained by aquaculture, seaweed cultivation is unequalled in mariculture, as 94% of the annual seaweed biomass used globally is from cultivated sources [6].

At present 98% of seaweed cultivated across the globe comes from five genera: Saccharina, Undaria, Neopyropia/Pyropia/Porphyra, Eucheuma/Kappaphycus, and Gracilaria [4][5][7][8]. These species are predominantly cultivated at sea, with a few groups including kelps and nori requiring an extra step, often onshore, to facilitate their microscopic life cycle stage. This step, known as the aquaculture hatchery phase, enables growth and seeding of ropes prior to deployment at sea [9].

Seaweed products range from food to pharmaceuticals, and bioenergy intermediates to materials. Brown and green seaweeds are predominately used in food as a source of fibre, protein, and minerals, especially throughout Asia [2]. Red seaweeds have been used as food, and as a source of agars and carrageenan which are used in food, cosmetic ingredients, and for biomedical applications [10]. The global seaweed industry is worth more than USD 6 billion per annum, of which 85% is for human consumption, and seaweed-based polysaccharides (carrageenan, agar, and alginates) account for nearly 40% of the world’s hydrocolloid market [2]. In Europe, brown seaweeds were traditionally used to produce additives (e.g., alginates) or animal feeds in the form of meal [11]. L. digitata and M. pyrifera are two brown seaweed species that are harvested and cultivated globally. In comparison to other kelp species such as Saccharina japonica, Saccharina latissima, and Undaria pinnatifida, M. pyrifera is a native species to New Zealand whereas Undaria pinnatifida is an invasive species and Saccharina japonica is not a native species [12][13]. L. digitata is a native Irish species with a wide distribution at low water on the Irish coast, when compared to Saccharina latissima, also a native Irish species, yet not comparable to L. digitata in distribution and abundance on the Irish coast [14][15]. In 2016, L. digitata global wild harvest yielded ~45,000 tonnes, and M. pyrifera yield reached 31,835 tonnes; however, only one tonne of M. pyrifera was produced through aquaculture [3]. Chile was the highest producer of brown seaweed from natural populations at 300,000 dry tonnes per year by 2012 [16], in a global context 7% of the brown seaweed from natural populations was provided by Macrocystis sourced in Chile and Mexico [17]). Seaweed is sourced mainly from wild harvesting, with only 2.4% from cultures, which are dominated by Agarophyton chilense [18]. It can be observed from these data that M. pyrifera when compared with L. digitata has significant future cultivation potential through aquaculture. Additionally, this aquaculture potential may assist in a reduction in the impact of wild harvesting on M. pyrifera’s distribution off the Chilean coast.

Specifically, L. digitata has been used in Europe as a food supply for algivores in the mariculture of abalone and sea urchins; it has also been harvested and supplied to Asia as a dried product and used as stock for soup making [14]. Within the fuel and renewable energy sector, it has been investigated for methane gas production through bioconversion trials in France and the US [14]. In Australia, Chile, and the US, M. pyrifera was also used to feed abalone [14][19][20]. In Mexico, M. pyrifera was used as a meal for goats. The digestibility of this seaweed was 77% when fed to this ruminant animal [21]. Digestibility increased to 85% when fed to male bovine zebu bulls [22]. Due to its low digestibility in salmonids, M. pyrifera in a derived flour form was added as a food supplement at 1.5%, 3%, and 6% dry weight (DW) of the total diet as a mineral and carbohydrate source [23].

2. Delivery Methods and Applications of Seaweeds

2.1. Food and Feed Delivery and Applications

L. digitata and M. pyrifera have been approved as food flavour additives by the FDA as dehydrated or ground products, for direct addition to food for human consumption as a source of iodine or dietary supplement [24]. Delivery of these two seaweeds in food is in an unrefined form as dried seaweed and is added to food ingredients such as breadsticks and huiro fritters [25]. Delivery of seaweed extracts such as the phycocolloid, alginate, in food has been in the form of powder or gel, to be applied to biscuits, yoghurts, and ice creams, and as a food thickening and emulsifying agent [26][27][28]. The extracted polysaccharides of laminarin and fucoidan from L. digitata were delivered as wet and dry spray and applied to mince pork patties to improve appearance and reduce lipid oxidation [29].

The use of L. digitata, L. hyperborea, and M. pyrifera for animal feed was delivered as fresh seaweed and applied as the main food source for abalone and sea urchin and North Ronaldsay sheep; unrefined dried seaweed or flour seaweed was added as a dietary supplement for goats, bulls, rabbit, fish, and shrimp diets [14][19][20][21][22][23][30][31][32]. Extracted phycocolloid, called crude alginate, from M. pyrifera and Laminaria spp., was used in fish feeds as a binding agent [26].

Dietary supplements for sows and piglets were delivered using a seaweed extract from Laminaria sp. containing polysaccharides laminarin and fucoidan [33][34]. L. digitata also provided feed supplements for pigs through seaweed extracts containing laminarin and fucoidan, and purified β-glucans were added to their basal diets [35][36][37]. These polysaccharides were used as a prebiotic dietary supplement to improve the microbial gut populations of pigs, and specifically, weaning piglets [35][36][37].

 

2.2. Pharmaceutical Delivery and Applications

Macrocystis pyrifera is used to treat thyroid conditions, anaemia in pregnancy in the US, and hypertension in Japan; an oral dose of 300 mg of iodine is recommended for hypertension treatment, with M. pyrifera reported to contain iodine at 0.1 to 0.5%. Medicinal preparations of iodine from M. pyrifera should be taken from the thallus [38]. Conversely, over consumption of seaweed was found to coincide frequently with medical ailments including goitre, hypothyroidism, and Hashimoto’s thyroiditis in countries where seaweed is used traditionally as food [39].

Alginates sourced from both L. digitata and M. pyrifera have been delivered in gels, powders, beads, and fibres and applied in wound dressings, indigestion control, and drug delivery [26][27][40][41][42]. With a growing global population, these alginate uses will continue to increase in demand and will undoubtedly require improved technology in their mode of delivery of these products. For example, the drug delivery speed or mode of action may need to be increased or consumed by a different method; in the case of wound dressings, alginates and sodium alginate are used in hydrogel which has the potential to contain bioactive compounds to improve the healing process [43].

Fucoidan has been extracted from M. pyrifera, L. digitata, and Saccharina japonica, and has shown bioactive properties, potentially making these fucoidans suitable to act as therapeutic agents for cancer and infectious diseases by assisting the immune system’s response, as an antitumour remedy, anti-inflammatory, antioxidant, and antibacterial, and to assist in lipid inhibition [44][45]. Fucoidan is a highly polar polysaccharide which limits its transport through the intestinal epithelial cells. Administration orally is then considered the easiest method; however, due to its molecular weight, oral bioavailability is considered low. To harness the clinical potential of fucoidan, a better understanding of preparation, quality standards, and administration must be acquired [46].

Secondary metabolites, phlorotannins extracted from several laminaria species including S. japonica and L. hyperborea, have been used in the effective control of human tumour cell proliferation, wound sealing, and reconstruction [47][48]. M. pyrifera, has also had two phlorotannins, phloroeckol and tetrameric phloroglucinol, identified as demonstrating antidiabetic and antioxidant activity as well as preventing skin aging [49]. Regarding application of phlorotannins, a study on the seaweed Ishige okamurae, which contains phlorotannins, suggested inclusion in potential functional food ingredients or nutraceuticals [50].

Seaweed extracts from L. digitata have been applied as a treatment to improve gut microbiota, and in commercial products as a skin moisturiser and as a homeopathic medicine [51][52][53]. A combination seaweed extract using M. pyrifera, Fucus vesiculosus, Saccharina japonica, zinc, and vitamin B6 was used to treat osteoarthritis, with positive results [54][55]. M. pyrifera seaweed extract in combination with krill oil was proposed to be useful as a pharmaceutical product with total antioxidant protection [56].

 

2.3. Other Applications

2.3.1. Fuel

Three seaweed species were listed as potential fuel producers in Table 3: M. pyrifera, Saccharina latissima, and Laminaria hyperborea [26][57][58]. Saccharina japonica, another commercially grown brown seaweed species, has been investigated for its fuel potential using a novel engineered microbial platform. S. japonica was used as a model brown seaweed species, due to the high alginate content found in brown seaweeds and was fermented to produce ethanol. The novelty in this platform was the use of genetically modified Escherichia coli to produce an alginate-degrading enzyme called “Aly”, followed by consolidated bioprocessing (CBP), which incorporates enzyme production, with feedstock degradation (in this case, alginate) and metabolism, (through fermentation at a temperature range of 25–30 °C), resulting in an ethanol yield of ~4.7% v/v [59]. S. japonica has also been used as a feedstock for the production of bio-oil, gas, and char using fast pyrolysis, with the highest yield of 40.91 wt% at a temperature of 350 °C and sweeping-gas velocity of 300 mL/min [60]. Whether either of these processes will be implemented as a commercial fuel production system remains to be seen. Interestingly, M. pyrifera, like S. japonica, has been trialled for its fuel producing capacity using a similar process to CBP. A pilot study used 75 L fermentation of genetically modified E. coli on M. pyrifera biomass. The higher alginate to mannitol content in M. pyrifera required a four-stage process to exploit more of the carbohydrates present; this included acid leaching, de-polymerisation, saccharification, and fermentation steps, which yielded 0.213 kg ethanol kg−1 dry macroalgae, reaching 64% of the maximum theoretical ethanol yield [61]. Whether these systems will gain commercial success remains to be seen. More recently, the biorefinery process has been proposed and trialled in an attempt to utilise seaweeds, completely reducing any waste products during extraction [9]. This extraction system, which is still in the emerging technology stage, may enable a significant increase in seaweed biomass usage during extraction than a single product production allows [62]. The caveat is that the seaweed species being used in the biorefinery must produce a fuel feedstock. As M. pyrifera has already proven its potential as a fuel, this opens the utility of it as a biorefinery species.

 

2.3.2. Nutricosmetics and Cosmeceuticals

Fucoidan’s well documented anti-inflammatory properties have been investigated as potential additional ingredients in nutricosmetics, with a focus towards anti-aging or sunscreen products. Marinova, an Australian-based seaweed bioproduct-producing company, utilises a cold water-based extraction for the polysaccharide fucoidan, which is supplied to the functional food and cosmetics industry [63]. Marinova also uses clinical trials to investigate the utility of fucoidan as anti-inflammatory and anti-aging ingredients in nutricosmetic products [64]. For potential nutricosmetics products, seaweeds and their extracts are well placed to be utilised for their inhibition of glycation, elastin calcification, and matric enzymes, as well as anti-inflammatory activity, all properties which assist in providing cosmetic anti-aging benefits [64].

 

2.3.3. Bioplastics

Sourcing bioplastics from L. digitata and M. pyrifera has not been documented to date; however, emerging uses for glycans extracted from the green seaweed Ulva include bioplastic. The Australian company Phycohealth already produces seaweed products including cosmetics, food, and food supplements and are behind this bioplastic product. The bioplastic they are working on is made using a glycan-based extract from Ulva, which is used to make thread which is then woven to produce a plastic film; other applications include potential 3D fabrication of materials [65].

 

2.3.4. Bioremediation

Bioremediation of ions from metals is another use of both M. pyrifera and L. digitata [66][67][68]. In the context of aquaculture, the potential dual purpose of these species is to be cultivated as an aquaculture crop and be used to remove metals that may be a potential environmental hazard is promising.

 

2.3.5. Aquaculture

The addition of these species to an Integrated Multi-Trophic Aquaculture system (IMTA) could potentially improve the productivity of the seaweeds, while also producing multiple aquaculture products from one environmental footprint. The IMTA initial conceptual design is a system that allows several species to be grown within the same encloser system, utilising nutrients from each trophic level to the level below it. The system includes a fed aquaculture tank, for example, fin fish, beside a shellfish growing station (called organic extractive aquaculture). This takes advantage of the enrichment in particulate organic matter (POM) from the fish tank; next to the shellfish is the seaweed growing station, called the inorganic extractive aquaculture, which gains nutritional advantage from the dissolved inorganic nutrients (DIN) [69]. An integrated approach enables efficient nutrient cycling to take place, attempting to partially close the nutrient loop, reducing external nutrient supply to the system and improving efficiency, and minimising environmental impact to the local ecosystem by utilising the fish waste within the other trophic levels. Chopin described this system as extremely flexible, and it could be applied to land-based, freshwater, or marine, and could be termed “aquaponics”. Implementation of the IMTA system was trialled in Chile using the red seaweed Agarophyton chilense as a biofilter for nitrogen on an open-water salmon farm. The study found a significant reduction in nitrogen at 9.3 g M−1 per m of line. These long lines were positioned within 800 m of the salmon pens within the effluent flow. Seaweed tissue analysis for nitrogen noted up to 2% of the daily weight (DW) in the Agarophyton chilense that were growing within 800 m of the salmon pens. This site had the highest level of nitrogen in the seaweed tissue and the highest growth rates of up to 4% DW in summer and 2% DW in winter. This Chilean study concluded that IMTA was a successful biofiltration platform using red seaweed Agarophyton chilense and proposed that a 100 hectare (ha) Agarophyton chilense farm would effectively reduce the inorganic N inputs of a 1500-tonnes salmon farm [70].

This entry is adapted from the peer-reviewed paper 10.3390/molecules26051306

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