1 Introduction

The environmental and economic costs of biological invasions of non-native species in the early part of the last decade were estimated to be worth ~ US$ 1.4 trillion per year, globally, equivalent to 5 % of the world economy (Engelen and Santos 2009). For comparison, the costs of non-native species to the economy of Great Britain alone for 2010 was £1.7 billion per year with the specific cost of invasive marine species to shipping and aquaculture estimated to be in excess of £40 million per year (Cook et al. 2013).

Sargassum muticum (Fig. 1), Japanese wireweed, is native to the northwest Pacific region (Edwards et al. 2014). It first was ‘introduced’ outside its natural range to British Columbia and has become the dominant species at the low-tide level in many areas on the west coast of North America (Fletcher and Fletcher 1975). It appeared in Europe in the early 1970s, and is now found on shorelines from Norway to Portugal (Engelen and Santos 2009). Since its first recorded find in the UK, on the coast of the Isle of Wight, it has spread along the south-coast and around the British Isles (Davison 2009; Gibson 2011) (Fig. 2). The growth rate of S. muticum is generally considerably higher than most UK seaweed species, being over 10-times higher than that of Ascophyllum nodosum (Davison 2009). S. muticum has been described as very invasive and perhaps the most ‘successful’ invasive species in the UK in terms of its rate of spread (Davison 2009).

Fig. 1
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Sargassum muticum. a Underwater photograph courtesy of Chris Wood, Marine Conservation Society. b Sample of wet S. muticum taken from Kent Coast

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Fig. 2
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Distribution of Sargassum muticum in British Isles courtesy of National Biodiversity Network

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The UK has identified S. muticum as a species of high priority under the EU’s Water Framework Directive (Davison 2009). It causes considerable problems in certain areas of the Kent coast, especially on chalk ledges, and is spreading, possibly displacing native algae (Kent Wildlife Trust 2006; Medway Swale Estuary Partnership ND; The River Stour (Kent) Internal Drainage Board 2012). The clearance of this seaweed is an issue in southern England and could have considerable financial and energy costs (CABI 2011; Williams et al. 2010). The harvesting of S. muticum has failed to eradicate it from the coast of the British Isles, but regular harvesting is used as a method to reduce its spread and the problems caused by its growth (Critchley et al. 1986; Lodeiro et al. 2004).

Critchley et al. (1986) have reviewed the methods and cost of harvesting S. muticum, with the cost of harvesting by mechanical methods being estimated at £20–24 per tonne of wet algae collected (equivalent to £52–63 in 2015 based on Bank England inflation data). However, seaweed including S. muticum is currently mainly harvested by hand in the British Isles (Bruton et al. 2009; Environment and Heritage Service NI 2007; Murphy et al. 2013; Scottish Natural Heritage 2012).

The harvesting of S. muticum, in attempt to control it, results in the need to dispose of large quantities of seaweed biomass (Davison 2009). Although, S. muticum has been exploited for aquaculture in China (Liu et al. 2013) and as a traditional food in Korea (Yang et al. 2013), there is currently no commercial exploitation of this biomass in Europe (Lodeiro et al. 2004). The valorisation of S. muticum biomass for fuel and other products could encourage its harvesting and control.

The object of this article is to briefly introduce some of the current and potential applications of seaweed in general, and then review the potential products for the valorisation of S. muticum.

2 Current and potential applications of seaweed

Macroalgae (seaweeds) have been used by mankind for generations as a food and for soil conditioning or fertiliser. Global utilisation of macroalgae is a multi-billion dollar industry (Smit 2004) with world production of seaweed increasing, between 1970 and 2010 from <2 million to 19 million tonnes fresh weight (Yeong et al. 2014).

The current uses of seaweeds include human foods, fertilisers, phycocolloids and cosmetic ingredients (Kraan 2013), with Asia being the main market (Kelly and Dworjanyn 2008; Roesijadi et al. 2010a). However, seaweed is still considered an under-utilised resource worldwide (Marquez et al. 2014). The chemical composition of seaweed has been reported for a variety of species, a selection of which is shown in Table 1.

Table 1 Compositional data (% dw) for species of seaweed being considered as potential biofuels
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2.1 Biofuel

There has been considerable discussion in recent years about the potential of microalgae for the production of sustainable and renewable biofuels, however after nearly 70 years of sometimes intensive research on microalgal fuels, and over two billion US dollars of private investment since 2000 (Service 2011) economically viable commercial-scale quantities of microalgal fuel have yet to be produced (Milledge and Heaven 2014). The amount of research on macroalgal biofuel is considerably less than that directed towards microalgal biofuel (Milledge et al. 2014; Zhou et al. 2010), and the use of macroalgae as a commercial feedstock for fuel production is currently ‘non-existent’ (Roesijadi et al. 2010b). Despite the focus of much biofuel research being on microalgae rather than macroalgae, the macroalgal non-fuel industry is currently 100 times bigger in wet tonnage terms than the microalgal industry (Lundquist et al. 2010).

2.2 Food and food supplements

Seaweeds are used as food by a number of societies around the world (Laver in Wales, Dillisk in Ireland, Dulse in Scotland, Limu in Hawaii, Nori in Japan), and there is a long history of a variety of seaweeds being consumed in many countries in Asia (Edwards and Watson 2011; Milledge 2011). McHugh (2003) reviewed the worldwide use and potential uses of seaweed and concluded that there is a potential for oversupply of some seaweed foods such as Nori. Thus, innovative and niche products may lead to greater success for future investors, rather than attempts to break into existing large markets for established products such as Nori. In the UK the exploitation of wild seaweed for food is currently as higher value gourmet ingredients and meals (Rose 2013). There appears to be only one current example of commercially farmed seaweed in the UK for food use: at Loch Fyne, which in 2013 produced 3 t (dw) of Alaria esculenta grown on 2 km of lines in a site area of 5 ha (Hughes 2014).

2.3 Phycocolloids

Phycocolloids or hydrocolloids are polysaccharides of high molecular weight that are composed mainly of simple sugars. The three major phycocolloids from algae, with total annual volume of 86,000 t, are alginates, agars, and carrageenans (E400, E406 and E407, respectively) (Holdt and Kraan 2011). They are widely used in the food industry for applications such as thickening aqueous solutions, forming gels and water-soluble films, and stabilising products such as tooth paste, ice-cream and mayonnaise (Holdt and Kraan 2011; Milledge 2012). In addition to their roles as thickeners, both alginate and carrageenan have been used for microencapsulation of probiotic cells (where they are effective in protecting the cells from the acidic environment of the stomach allowing the release of cell contents into the intestine), as well as aiding in more generalised freeze drying and other food process operations (Cheow and Hadinoto 2013; Gibbs et al. 1999). It is suggested that of all seaweed products, hydrocolloids have attained the greatest commercial significance and influence on modern western societies, and that there is little commercial exploitation of products extracted from seaweeds outside the phycocolloid industry (Bixler and Porse 2011; Smit et al. 2004).

2.3.1 Alginates

Alginates are hydrocolloid polymers, available in both acid and salt forms, of 12,000–180,000 molecular weight, composed of D-mannuronic and L-guluronic acid and extracted from brown seaweeds. These polymers react with calcium ions to form a stable gel (Gibbs et al. 1999; Holdt and Kraan 2011; Wargacki et al. 2012). Alginates are U.S. Food and Drug Administration (FDA) approved polymers, and represent some of most important biomaterials for diverse applications not only in the food and cosmetic industry, but also in the textile industry, and for biomedical applications such as wound dressings (Sun and Tan 2013).

Alginates were discovered in the 1880s by the British pharmacist, Edward C. Cortis Stanford, with industrial production beginning in California in 1929 (Holdt and Kraan 2011). Worldwide annual alginate production has been estimated at 30,000 t (Rehm 2009); in Norway 6400 t of alginates are produced annually from 150,000 t of fresh Laminaria hyperborea (Horn et al. 2000). The uses of alginate have been extensively reviewed by Rehm (2009) and Holdt and Kraan (2011); and for biomedical applications by (Sun and Tan 2013).

2.3.2 Carrageenan

Carrageenans are linear sulphated polysaccharides that are extracted from red seaweeds (Holdt and Kraan 2011). The name Carrageenan is derived from the Irish name, Carraigin, of Chondrus crispus, also known as Carrageen Moss or Irish Moss, which has been used in Ireland as a gelling agent and remedy for coughs since around 400 AD (Necas and Bartosikova 2013). Carrageenan (E 407) is used in food preparation for its gelling, thickening, and emulsifying properties and is found in canned foods, dessert mousses, salad dressings, bakery fillings, ice cream, instant desserts and canned pet foods (Holdt and Kraan 2011; Necas and Bartosikova 2013). It has also been used for the clarification of beer, and wines, but this use is reported to be declining (Holdt and Kraan 2011). The industrial, cosmetic and pharmaceutical applications of carrageenan are extensive and have been reviewed by Smit (2004), Holdt and Kraan (2011) and Necas and Bartosikova (2013).

Although carrageenan was originally derived from wild stocks of Chondrus crispus until the 1960s, the majority of carrageenan is now produced from the cultivation of Kappaphycus and Eucheuma (Valderrama et al. 2014). Growth of both these species has increased significantly with the main production sites being the Philippines and Indonesia, and on a smaller scale in Tanzania and a few other developing countries (Valderrama et al. 2014). The cultivation of red seaweeds has contributed most to the recent expansion in global seaweed production with red seaweed farming production worldwide increasing from 2 million wet tonnes in 2000 (21 % of the production of all cultivated seaweeds) to 9 million wet tonnes in 2010 (47 %) due to the increased demand for carrageenan in processed foods (Valderrama et al. 2014). The FAO has recently published an extensive report on the production of carrageenan from seaweed aquaculture and its social and economic impact (Valderrama et al. 2014).

2.3.3 Agar

Agar is a mixture of polysaccharides, which can be composed of agarose and agaropectin, and has similar properties to carrageenan (Holdt and Kraan 2011). Prior to the Second World War it was the most popular colloid for food, but research during the war showed that it could be substituted by carrageenan (Valderrama et al. 2014): during the last 40 years agar has gradually been replaced in some of its traditional uses by other hydrocolloids such as carrageenan (McHugh 2003). The red seaweed Gracilaria is the primary raw material for agar production (Valderrama et al. 2014), although it is also produced from Gelidium (Holdt and Kraan 2011). Agar is a traditional food material in Japan used for cooking and Japanese-style confectionary, and is also used in cell culture media and the manufacture of capsules for medical applications (Holdt and Kraan 2011). “No modern microbiological laboratory in the world can survive without agar, and no satisfactory substitute has been found even with today’s technological advances” (Guiry 2014). However, over 90 % of global agar production is used in food applications (McHugh 2003). It has also been reported that agar has been used as a laxative (McHugh 2003), and that agar leads to decreases in the concentration of blood glucose (Holdt and Kraan 2011).

2.4 Iodine

Iodine deficiency is the world’s most prevalent cause of brain damage, impairing mental health and intellectual capacity. Serious iodine deficiency during pregnancy can result in stillbirth, spontaneous abortion, and congenital abnormalities (World Health Organisation 2014). In the UK it has been reported that up to 66 % of adult women and 76 % of school-aged girls could be iodine deficient (Rose 2013). Seaweed is a rich source of iodine, especially brown algae where iodine content can be up to 1.2 % (dry weight), and Laminaria japonica has been used in China for centuries as a dietary iodine supplement (Holdt and Kraan 2011). It has been suggested that only a “relatively small amount of seaweed” in a portion of a food would be required to allow it to become a “good source” of iodine and allow its associated health benefits to be noted on packaging under EU (1924/2006) Approved Health Claims regulations (Rose 2013).

Iodine was extracted from kelp in Ireland during the seventeenth century (Holdt and Kraan 2011), but by 1900 the industry was petering out due to competition from imported cheaper iodine from mineral deposits; by the start of World War II production ceased in Ireland (Biomara 2014). The world market for iodine in 2011 was ~32,100 t per year. It is primarily obtained as a by-product in nitrate production, with Chilean companies accounting for ~58 % of global sales (Iofina 2011).

2.5 Fertiliser and animal feed

Nitrogen fertiliser is generally manufactured from atmospheric nitrogen using fossil fuel energy, with phosphorus being obtained from phosphorite, a diminishing global resource which may not be sustainable (Kraan 2013). Seaweed fertilisers could not only be a sustainable alternative, but near-shore cultivation may also sequestrate both phosphates and nitrates in run-off as macroalgae have high uptake rates of both N and P (Kraan 2013). The high ash content of seaweed can also provide minerals and trace elements that are beneficial in both fertiliser and animal feed (McHugh 2003; Philippsen 2013). In addition to macro- and micro-nutrients, seaweeds contain many growth promoting hormones (Sridhar and Rengasamy 2011).

Twenty-five species of seaweed are currently used in agriculture as animal feed and fertilisers (Pereira 2011). However, agricultural sales volumes are limited, relative to those of industrial phycocolloids, and in 2003 the value of seaweed animal feeds and fertiliser were both estimated at only $5 million per year (McHugh 2003).

Seaweed has traditionally been collected and used by coastal communities as a fertiliser (Fig. 3) (Bruton et al. 2009). Liquid seaweed extracts and suspensions, introduced in the 1950s, have now achieved a broader use and market than seaweed and seaweed meal, due to their ease of use. They have been shown not only to provide N, P and K in horticulture, but to enhance seed germination, increase frost resistance and improve resistance to fungal and insect pests (Booth 1969; McHugh 2003).

Fig. 3
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Twentieth century painting, “Gathering Seaweed” by Harold Harvey, courtesy of David Messum Fine Art

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Coastal communities have traditionally not only used seaweed as fertiliser, but also as an animal feed. Despite the suggestion of nutritional benefits especially for sheep and cattle, the use of seaweed as a feed may have declined (McHugh 2003). In addition to feed for terrestrial animals, macroalgae have been extensively used for abalone aquaculture (Dang et al. 2011). The higher sodium content of seaweed relative to land plants (Philippsen 2013; Ruperez 2002) and limited digestibility of many seaweed proteins and carbohydrates (McHugh 2003) may restrict its use as a feed. A number of substances in seaweed have been found to have animal nutritional and health benefits (Holdt and Kraan 2011; McHugh 2003; Sweeney et al. 2012), and seaweed could have considerable further potential for the supply of animal and aquaculture nutritional supplements.

2.6 Therapeutic products

The use of algae for therapeutic purposes has a long history, but the search for biologically active substances from algae, especially examination for antibiotic activity, began only in the 1950s. In fact, much of that laboratory work up until the 1980s has focused on macroalgae rather than microalgae (Borowitzka 1995). Algae have been reported to be the source of ~35 % of the newly discovered chemicals between 1977 and 1987, but the discovery of new products from seaweeds has decreased since 1995 and attention in marine natural product chemistry is now mainly focused on sponges and marine microorganisms (Fig. 4) (Blunt et al. 2015; Smit 2004). Approximately, 15,000 natural marine products have now been screened for biological activity and 45 marine derived natural products have been tested for use as medical drugs in preclinical and clinical trials. Only 2 have been developed into registered drugs, one from a marine snail and the other from a sea squirt, although none as yet from algae (Murphy et al. 2014; Wijffels 2007).

Fig. 4
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Marine natural product research community phylum-preferences 1963–2013 (Blunt et al. 2015). [The brown and yellow–green seaweeds belong to the phylum Ochrophyta (Pizzolla 2008)]

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Smit (2004) has extensively reviewed medicinal and pharmaceutical uses of seaweed: a number of algal polysaccharides have been found to have antiviral properties, with sulphated polysaccharides, from red and brown algae, showing antiviral activities towards human infectious viruses. Successful infection by pathogens depends on subversion of host immune mechanisms that detect cell wall components such as fucans (Berteau and Mulloy 2003) and glucans (Rappleye et al. 2007). Glucans from the macroalgae, L. hyperborean and L. digitata as well as those from baker’s yeast, S. cerevisiae, are all reported to decrease the number of Enterobacteriacea in pigs (Sweeney et al. 2012). The medicinal uses of a number of compounds from marine sources have recently been reviewed: glycans (Pomin 2014), glycolipids (Plouguerné et al. 2014) and sulphated polysaccharides and fucoidans (Wijesinghe and Jeon 2012).

Non-saccharide compounds have also shown antiviral properties, with kahalalide F, a small natural peptide from a species of Bryopsis, being studied as a possible treatment of cancer and AIDS (Sewell et al. 2005; Smit 2004; Suárez et al. 2003). Phenolics, steroids, terpenoids, and a range of other secondary metabolites from seaweeds have all been shown to have potential therapeutic activity (Blunt et al. 2015; Gupta and Abu-Ghannam 2011; Plouguerné et al. 2014), with terpenoids as a chemical class being associated with over half of potential new natural products isolated so far from algae (Fig. 5) (Leal et al. 2013). The antimicrobial activity of a crude dichloromethane extract from the brown alga, Sargassum paradoxum, has been attributed to meroditerpenoids, comprised of a polyprenyl chain attached to either a p-benzoquinone or hydroquinone moiety (Brkljača and Urban 2014).

Fig. 5
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The distribution of marine natural products from different chemical groups by macroalgal phyla (Leal et al. 2013)

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Chemicals with antimicrobial activity are widespread in macroalgae, and several compounds have been shown to have additional anti-thrombic, anticoagulant and coagulant activities (Holdt and Kraan 2011; Smit 2004). Macroalgae thus appear to have considerable potential as a source of therapeutic compounds, although as yet commercial exploitation appears limited.

2.6.1 Cancer chemotherapy

Extensive recent reviews have been published on the potential of seaweed as a source of drugs for use in cancer chemotherapy (Murphy et al. 2014; Stonik and Fedorov 2014). Glucan oligomers, for example, hydrolysed from laminarin extracted from kelp, inhibit the proliferation of human leukaemia U937 cells (Pang et al. 2005). Fucose containing compounds from seaweed have been widely reported to have anti-cancer activity (Ale et al. 2011a, b; Chen et al. 2014a). Moreover, the artificial conjugation of glycans to immunogens has been shown to dramatically increase their immunogenicity in anti-cancer applications. With antigens such as fucose-containing Lewis X thought to play a central role in cancer cell immune recognition (Miyoshi et al. 2008; Rabinovich et al. 2012), there is a pressing need to characterise the involvement of fucosylated and sialylated glycans in these processes.

However, despite the potential, translation to clinically useful preparations is almost non-existent with only one seaweed derived compound (kahalalide F) known to be undergoing clinical trials (Murphy et al. 2014).

2.7 Other non-fuel uses

Products from seaweed could have a wide range of further uses. One company, Hercules, was capable of producing 54 chemicals from seaweed during the First World War, but closed shortly after the war when demand fell and alternative supplies became available (Kelly and Dworjanyn 2008). Seaweed has been used for the production of alkali, soda (sodium carbonate) and potash (potassium carbonate), for use in a variety of processes, but has again been replaced by cheaper sources of supply (Kelly and Dworjanyn 2008).

Research is being carried out on the use of red algae for a wide range of applications. Halogenated furanones from Delisea pulchra are being considered as antifouling compounds (Smit 2004). Carrageenan gel, derived from red seaweed, has been used to immobilise microbial cells, and has been studied as a method of cleaning up industrial effluents (Necas and Bartosikova 2013).

Algae, especially red algae, also contain phycobiliproteins, deeply coloured (red or blue) water soluble, complex, proteinaceous photosynthetic accessory pigments (Milledge 2011). These algal pigments have potential as natural colourants for food, cosmetics and pharmaceuticals (Baghel et al. 2015). In 1997 the global market for phycobiliprotein colourants was estimated at US$ 50 million (Spolaore et al. 2006). Dainippon Ink and Chemicals produces a blue food colourant from the microalga, Spirulina, called Lina Blue, that is used in chewing gum, ice slush, sweets, soft drinks, dairy products and wasabi (Milledge 2011). Phycobiliproteins are also commercially produced from the red microalgae Porphyridium and Rhodella (Milledge 2012), and can be produced from red macroalgae (Baghel et al. 2015).

Brown seaweeds have been identified as potential producers of a wide spectrum of natural ‘cosmeceuticals’ (cosmetic products claimed to have biologically active ingredients with medicinal or drug like benefits) for a variety of uses from anti-wrinkle to skin whitening products (Wijesinghe and Jeon 2011). In summary seaweed could be a potential feedstock for a wide range of novel materials.

2.8 Biorefineries

The term ‘biorefinery’ has been used in the literature since the 1980s, and refers to the co-production of a spectrum of high value bio-based products (food, feed, nutraceuticals, pharmaceuticals and chemicals) as well as energy (fuels, power, heat) from biomass (Gonzalez-Delgado and Kafarov 2011; Olguin 2012; Taylor 2008; Wageningen University 2011). The biorefinery concept is an ‘emerging research field’ (Rawat et al. 2013) and in December 2009 the US Department of Energy announced a US$ 100 million grant for three organisations to research algal biorefineries (Singh and Ahluwalia 2013).

Not all commercially harvested seaweed biomass is processed into products: in the production of agar only ~17 % of the seaweed is utilised with ~83 % of the biomass being waste or low value products (Baghel et al. 2015). There thus appears considerable opportunity to use biorefining to add value. Biorefineries could allow the exploitation of the entire algal biomass, and improve the economics of biofuel production (Pires et al. 2012), but they are likely to be energy intensive (Olguin 2012; Rawat et al. 2013). A biorefinery plant should be capable of operating sustainably with its energy demands met by the biofuels produced (Cherubini 2010). However, it should be noted that the extraction of alginate, laminarin and fucoidan is estimated to lower the amount of fermentable compounds available in seaweed, reducing bioenergy production by half (Bruton et al. 2009).

A biorefining technology that maximises the utilisation of seaweed for the production of additional high-value products such as ‘nutraceuticals’, pigments and vitamins, could be a viable and sustainable way of supporting the development of a commercial seaweed biofuel industry, but considerably more research is required to support this contention (Baghel et al. 2015; Boonstra 2014; Hannon et al. 2010; Horn 2000; Jung et al. 2013; Milledge et al. 2014; Rajkumar et al. 2014).

3 Potential applications of Sargassum muticum

S. muticum is a relatively high water content biomass (80–90 %) (Critchley et al. 1990; Milledge et al. 2015; Wernberg et al. 2001) compared to terrestrial crops (sugarcane ~75 %, grain maize 14–31 %) (European Commission 2014; McLaren 2009). It also has a high ash content of between 27 and 42 % dry weight (Hardouin et al. 2014; Shekhar et al. 2012). For comparison, wood has a typical ash content of 0.5–2 % (Misra et al. 1993; Saidur et al. 2011). The higher ash content of S. muticum results in its biomass having a Higher Heating Value (HHV) of 16 MJ kg−1 (Milledge et al. 2015) that is somewhat less than that of the terrestrial energy crops of 17–20 MJ kg–1 (Ross et al. 2008). This high moisture and ash content will influence the applications of S. muticum and it economics.

Despite S. muticum being widely distributed in Asia, America and Europe, few studies have been reported on its chemical composition, metabolite landscape or the bioactivities to be found in its extracts and the purified natural products found in them (Shekhar et al. 2012). However, a recent review of the therapeutic potential of Sargassum species, although containing no data relating directly to S. muticum, showed that Sargassum species in general contain a wide range of potentially bioactive compounds including sulphated polysaccharides fucoxanthin, steroids, terpenoids, and flavonoids (Yende et al. 2014). A recent chemical analysis of the composition S. muticum is given in Table 2.

Table 2 Compositional (% dw) analysis of Sargassum muticum (Milledge et al. 2015)
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Phylogenetic relationships of Sargassum species (Fig. 6) particularly that of the subgenus, Bactrophycus, of which S. muticum is a member, have been the subject of a number of studies (Mattio and Payri 2011; Oak et al. 2002; Stiger et al. 2003). The genetic diversity within the European population has been found to be much lower than that of the native Pacific population (Bae et al. 2013; Zhao et al. 2008). This reduced genetic diversity will have implications for the range of compounds available from S. muticum found on the coast of Europe in comparison to those species in the Far East. A study of S. muticum, growing on the European coast between Portugal and Norway, found that although there are differences in the relative composition of amino acids, carbohydrates and especially phenolic compounds, no specific major compounds were either present or absent due to changes in latitude or environment (Tanniou et al. 2015).

Fig. 6
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Phylogenetic tree within the genus Sargassum (Stiger et al. 2003)

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The mitochondrial genome of S. muticum has recently been sequenced (Liu and Pang 2014). It is a circular molecule of 34,720 bp (base pairs) encoding 65 genes typically found in the mitochondria of other brown algae. Phylogenetic analyses based on 35 protein-coding genes reveal that S. muticum has a close evolutionary relationship with S. horneri supporting the currently accepted taxonomic classification (Liu and Pang 2014; Liu et al. 2014). The nuclear genome of S. muticum does not, as yet, appear to have been mapped and sequenced, but it is of a similar size (213 Mbp (Phillips et al. 2011)) to that of the model brown alga, Ectocarpus siliculosus [214 Mbp (Cock et al. 2010)].

The nuclear genomes of brown algae, judged by data from Ectocarpus, are somewhat enigmatic: many of the gene models revealed by the published assemblies do not appear to correlate with those seen in the majority of eukaryotes, leading to the suggestion that the brown algae are specialised examples of multicellular organisms (Cock et al. 2010). The genetic differences seen in brown algae give an indication of the very different evolutionary history that these organisms display compared to that of green plants, to which they are only distantly related. Importantly, these differences may reflect seaweed’s ability to cope with highly variable tidal environments due to the presence of an extended set of light-harvesting and pigment biosynthesis genes and unique metabolic processes, such as halide metabolism (Cock et al. 2010). Sargassum muticum and other brown seaweeds, therefore, may be a potential source of novel biochemicals unobtainable from terrestrial plants. Glycans from such marine sources, for example, have already been shown to be unique in terms of their structure and function, differing considerably from those of terrestrial origin (Pomin 2014). Further detailed studies of the biochemistry and metabolic pathways present in brown seaweeds are warranted.

3.1 Fuel

It has been suggested that the high ash content and low calorific value (~17 kJ g−1) of residues from S. muticum following alginate extraction would not make it a suitable target for ‘energetic valorisation’(Gonzalez-Lopez et al. 2012). In a study of the energy balance on the pyrolysis of S. muticum it was found that drying, prior to pyrolysis, required more energy than was produced in biofuel (Milledge et al. 2015). Biofuel processes that require the S. muticum to be dry, therefore, may not be energetically viable, unless a low fossil energy drying method such as solar drying is used. Solar drying does not require fossil fuel energy (Brennan and Owende 2010), but is weather dependent, and weather conditions in countries such as the UK may not be conducive to solar drying. It also requires large areas of land as only around 100 g of dry matter can be produced from each square metre of sun-dryer surface (Oswald 1988). S. muticum is unable to survive drying (Edwards et al. 2014), therefore if sufficient areas of land adjacent to the areas from where it is to be removed could be found for solar drying there may be low risk of potential ‘re-infestation’.

A recent review suggests that macroalgal biomass has potential for the production of various biofuels, but currently anaerobic digestion (AD) is closest to industrial exploitation (Milledge et al. 2014). Not only is AD a relatively simple process from an engineering/infrastructure perspective, but it also has the potential to exploit the entire organic carbon content of macroalgae, and can readily tolerate high moisture content, therefore eliminating energy intensive drying (Jard et al. 2013; Milledge and Heaven 2014). However, the biomethane potential of S. muticum is low at 0.13 L CH4 g−1 VS (Jard et al. 2013; Soto et al. 2015), and considerably below that typical of seaweed at 0.2 L CH4 g−1 VS (Alvarado-Morales et al. 2013; Chen et al. 2015) and ~30 % of that from common commercially exploited feedstocks (Astals et al. 2015; Banks and Zhang 2010; Golueke et al. 1957; Nallathambi Gunaseelan 1997; Nguyen et al. 2014). This, together with the availability of a variety of other more readily fermentable wastes, may make the collection of S. muticum for AD commercially unattractive. The cost of methane produced from seaweed has been estimated to be 3 to 6 times more than natural gas (Chynoweth 2002, 2005), with the projected cost of energy from macroalgae being 5–60 $ GJ−1, considerably above cost of energy from fossil fuel (Chen et al. 2015).

Co-digestion can enhance anaerobic biodegradability. A recent study found that co-digestion of Sargassum spp. with glycerol or waste cooking oil, containing little nitrogen, increased methane production by 19–56 % compared to the individual materials digested separately (Oliveira et al. 2015). However, the increasing availability and low cost of ‘waste’ glycerol from biodiesel production (Pagliaro et al. 2008) may not give sufficient financial incentive to collect and use S. muticum as a co-digestion substrate.

3.2 Food

Although, S. muticum is a traditional food in Korea (Yang et al. 2013) it does not appear to have been commercially exploited as a food in Europe. However, a British company, Haeckles, is exploring the production of a nutritional drink based on seaweed found on the Kent coast including S. muticum (Bridges, Haeckles private communication 2015), and S. muticum has been suggested as a general nutraceutical for the prevention and treatment of cancer due to the presence of antioxidants, antimicrobial and antitumor compounds within it (Namvar et al. 2013). A study using S. muticum as a dietary supplement found that it produced a 14 % reduction in blood low-density lipoprotein (believed to be a major contributor to atherosclerosis) and an increase in natural killer NK lymphocytes (Park et al. 2015). However, considerable care should be taken in the use of seaweeds for food since brown macroalgae, including S. muticum, contain much higher levels of absorbed heavy metals than terrestrial plants (Carro et al. 2015; Lodeiro et al. 2004; Ungureanu et al. 2015).

3.2.1 Antioxidants

Lipid oxidation is one of the most important factors in deterioration in the quality of food, and S. muticum has been suggested as a potential source of food antioxidants (Farvin and Jacobsen 2013; Joana Gil-Chávez et al. 2013). S. muticum was found to have the highest levels of both α and γ tocopherol (antioxidants that have vitamin E activity) of 16 species of seaweeds collected from the Danish coast, but extracts from S. muticum were found not to increase the oxidative stability of edible oils (Farvin and Jacobsen 2013).

3.3 Feed

Although S. muticum has been used as aquaculture feed for sea cucumber and abalone in China (Liu et al. 2013; Zhao et al. 2008), little further data exist to support its use as an animal feed additive.

3.4 Fertiliser

S. muticum extracts have been shown to stimulate higher dry matter yield in both mung bean and pak choi plants (Shekhar et al. 2012). This additional growth was attributed not only to the nitrogen, phosphorus and potassium content but also to trace minerals and metabolites in S. muticum. It is also suggested that S. muticum may contain rooting-factors such as indole acetic acid (Shekhar et al. 2012). The use of seaweed as a fertiliser may not be permitted in areas close to the coast. In an area of coast where S. muticum is being removed, Thanet, Kent, England, the aquifer area near the coast is designated as a Nitrate Vulnerable Zone (NVZ), with strict controls over any further increases in the levels of nitrate in the soil. Most farms in Thanet are therefore unable to use locally harvested seaweed as a fertiliser because of the potential effect on groundwater supply (Thanet District Council 2014).

3.5 Carbohydrates

The most abundant carbohydrates in brown macroalgae are alginate, mannitol and glucans present as laminarin and cellulose (Enquist-Newman et al. 2014). The carbohydrate composition (w/w dry biomass) of S. muticum is 2.2 % cellulose, 16.9 % algenic acid, 7.7 % mannitol and 0.3 % laminaran (Gorham and Lewey 1984; Marquez et al. 2014). Crude or partially purified polysaccharide mixtures from seaweeds including S. muticum have been shown to have antitumor activity, but the anticancer activity of these extracts is complex to interpret because of the diverse range of compounds present and the multiple interactions they display (Namvar et al. 2013).

In an interesting application, aqueous polysaccharide-containing extracts from S. muticum have been used to produce derivatised iron oxide nanoparticles that have significant cytotoxicity against human leukaemia cells, but did not affect normal liver cells (Namvar et al. 2014). Although at an early stage of development, these results suggest that S. muticum extracts might be useful in producing nanoparticles for use in anticancer therapy. S. muticum polysaccharides have also been used to produce silver, zinc and gold nanoparticles that could have applications in the electronics industry as well as in pharmaceuticals and cosmetics (Azizi et al. 2014).

3.5.1 Hydrocolloids

The alginate content of S. muticum growing in UK waters was found be relatively constant over the growth season (Gorham and Lewey 1984). Although, there have been reports of S. muticum being used for alginate production (Liu et al. 2013; Zhao et al. 2008), Critchley et al. (1986) suggest that the low yield (5–11 % compared to 16–30 % for commercially exploited brown algae (Gonzalez-Lopez et al. 2012)) and quality of algenic acid from S. muticum do not make it a viable source of commercial alginates.

3.5.2 Sulphated carbohydrates

The sulphated polysaccharides of seaweeds are chemically very different from those of land plants with those in brown seaweed being mainly sulphated fucans (fucoidans), with other sulphated polysaccharides containing galactose, xylose, glucose and other simple sugars also being found (Berteau and Mulloy 2003; Rodriguez-Jasso et al. 2014). S. muticum contains 8 % dry weight as fucans (Gorham and Lewey 1984) with fucose being the dominant sugar in S. muticum sulphated polysaccharides (Balboa et al. 2013). S. muticum harvested in Kent was found to have a lower sulphur content (1.5 % dw) than A. nodosum (2.51 % dw) (Milledge 2014 unpublished data). Fucans have been classified as non-toxic (Rodriguez-Jasso et al. 2014). They play an important role in the removal of ‘oxygen-species’ from organisms (Rodriguez-Jasso et al. 2014); they have been proposed as alternatives to the anticoagulant, heparin; inhibit virus infection of cells; and they inhibit parasite invasion, showing antimalarial activity as well as inhibiting another widespread parasite, Toxoplasma gondii, the disease vector for toxoplasmosis (Berteau and Mulloy 2003).

The structure of fucans can vary with the algal species, life-stage and environment with the antioxidant capacity of the fucans related to their molecular mass and sulphate content (Rodriguez-Jasso et al. 2014). Sulphated polysaccharides having a molecular mass <30 kDa have been shown to be the most biologically active, and sulphated polysaccharides of 26–35 kDa from other Sargassum species have been shown to block carcinogens and display antiviral properties. Fucoidans from seaweeds can have a wide range of molecular masses, extending from 8 to at least 627 kDa (Liu et al. 2013).

The molecular biology, biochemistry and enzymology of fucan and fucoidan production in brown seaweeds such as S. muticum is a relatively underexplored area with considerable promise for future commercialisation.

3.6 Lipids

The higher lipid content of some microalgae (>70 %) compared to macroalgae (0.3–6 %) has focused much of the published research work on microalgal lipids for both fuel and non-fuel uses (Bahadar and Bilal Khan 2013; Huang et al. 2010; Milledge and Heaven 2014; Milledge et al. 2014). As in the case of other brown algae, the lipid content of S. muticum is low, typically <1.3 % (Hardouin et al. 2014; Shekhar et al. 2012). Macroalgae may therefore not be a commercially attractive target for bulk lipid production, although specific lipid species may have considerable value.

3.6.1 Fats and fatty acids

In S. muticum, palmitic acid constitutes 21.5 % of the total fatty acids, and has been shown to have antimicrobial activity against bacteria and diatoms (Bazes et al. 2009). Similarly free fatty acids extracted from Sargassum pallidum have considerable antimicrobial activity against bacteria, yeast and fungi, with glycolipids and neutral lipids demonstrating ‘moderate’ activity (Gerasimenko et al. 2014). The exact mechanism of antimicrobial action is unknown, but specific algal fatty acids may initiate lipid peroxidation and inhibit fatty acid synthesis within bacteria (Gerasimenko et al. 2014).

3.6.2 Sterols

The use of sterols in managing high cholesterol levels and cardio-vascular health is extremely topical (Clifton 2009; Genser et al. 2012). The structures and biological activities of the sterols in seaweed are likely to be very different from those of terrestrial plants, since seaweeds function under very different environmental conditions. Recent evidence from other Sargassum species (e.g. S. fusiforme) support this contention, with saringosterol showing potent natural cholesterol-lowering activity, with other sterols contributing to anti-atherosclerotic functions (Chen et al. 2014b). A wide range of sterols (C16–C30) have been described in S. muticum, with C29 and C30 sterols accounting for 25 and 18 % of total sterols respectively (Wang et al. 2006). The biological activities of these components remain to be determined.

3.7 Carotenoids

Most brown seaweeds contain the carotenoid pigment fucoxanthin which has important antioxidant, anti-inflammatory, anti-obesity, antitumor and UV-preventative activities (Chae et al. 2013; Kumar et al. 2013; Wijesinghe and Jeon 2011). Balboa et al. (2014) have suggested that fucoxanthin may represent a major commercial product from S. muticum.

Gammone et al. (2015) have recently reviewed the effect of various carotenoids (including fucoxanthin) on human health, and in particular cardiovascular health; Maeda (2015) has reviewed the use of fucoxanthin for obesity and diabetes therapy; and Zorofchian Moghadamtousi et al. (2014) have reviewed the anticancer and antitumor potential of fucoxanthin.

Extracts from S. muticum also contain apo-9′-fucoxanthinon (C15H22O4) which has been shown to have anti-inflammatory properties (Yang et al. 2013) inhibiting pro-inflammatory cytokine production in bone marrow-derived macrophages and dendritic cells (Chae et al. 2013).

Despite fucoxanthin being the main carotenoid produced by brown seaweeds and its demonstrated benefits for human health, the biosynthetic pathway of fucoxanthin in seaweed is poorly understood; considerably more research is required to fully characterise the biochemistry and molecular biology of the enzymes that biosynthesise fucoxanthin, together with their structure and subcellular localisation (Mikami and Hosokawa 2013; Wang et al. 2014).

3.8 Phenols

The phenolic compounds in brown algae play a primary role in the structure of cell walls and are generally considered to be a chemical defence against grazers, bacteria, fungi and other epiphytes (Le Lann et al. 2008; Plouguerne et al. 2006). S. muticum has been suggested as a sustainable source of bioactive phenolic compounds (Tanniou et al. 2013). It is a rich source of phenolic compounds having the highest phenolic content of 6 seaweeds found in Portugal (Silva et al. 2013), containing up to 5 % dry weight polyphenols (Gorham and Lewey 1984), with its phenolic content varying with light intensity (especially UV radiation), salinity and nutrient availability (Plouguerne et al. 2006; Tanniou et al. 2014). The phenolic compounds extracted in a methanol/water solution from S. muticum have been shown to have antioxidant activity, but are rapidly degraded if the seaweed was dried at >40 °C (Le Lann et al. 2008). A methanol extract from S. muticum has been found to inhibit MCF-7 and MDA-MB-231 breast cancer cell line proliferation, with the phenolic compounds suggested to be major agents in the anti-proliferative efficacy of the algal extract (Namvar et al. 2013). The observed antioxidant activity of S. muticum extracts may be due to synergism with other compounds such the carotenoid, fucoxanthin (Farvin and Jacobsen 2013; Gonzalez-Lopez et al. 2012; Tanniou et al. 2014).

3.9 Proteins

A recent extensive review has found that the proteins, peptides and amino acids from seaweeds have shown positive bioactive effects in the treatment of diabetes, cancer, AIDS and the prevention of vascular diseases (Holdt and Kraan 2011). Nutritional studies have shown that algal proteins are comparable to vegetable proteins (Becker 2007), and algal proteins, and potentially those from S. muticum, could be used in ‘health-foods’, animal feed and cosmetics.

The protein content of S. muticum growing in UK waters was found to be highest in the spring (Gorham and Lewey 1984). Gonzalez-Lopez et al. (2012) found the typical average protein content of S. muticum to be 6.9 % of the total dry weight, but Hardouin et al. (2014) reported protein levels of 29 %. Although the carbon content of S muticum was found be relatively constant at ~30 %, the nitrogen content varies throughout the growing season, being highest in the spring 3–4 % and lowest in the autumn 1–2 % (Wernberg et al. 2001). Jard et al. (2013) found the nitrogen content (between 1 and 1.7 % dw for S. muticum harvested in Brittany, France during July) to be the lowest of 10 seaweeds, but S. muticum harvested in Kent, England during March had a higher N content (4.9 %) than the native species, A. nodosum (3 %) (Milledge 2014 unpublished data). A summary of protein, ash, carbohydrate and lipid content of S. muticum is given in Table 3.

Table 3 Compositional (% dw) of Sargassum muticum
Full size table

Free amino acids were found to be consistently low throughout the growing season at <1 mg g−1 (Gorham and Lewey 1984).

3.10 Emerging therapeutic products

S. muticum has been used in traditional Chinese medicine to treat a variety of diseases, including thyroid disease, but the exact nature of its efficacy is often not clear (Liu et al. 2012). Nevertheless, S. muticum has not generally been considered a medicinal seaweed (Yoon et al. 2010). A recent review of Sargassum species, although not giving specific results for S. muticum, found that various extracts from Sargassum species showed significant therapeutic potential, and suggested Sargassum could provide novel functional ingredients for pharmaceuticals for the treatment and prevention of several disorders (Yende et al. 2014).

3.10.1 Inflammation

The dichloromethane-soluble fraction from ethanolic extracts of S. muticum contains effective inhibitors of lipopolysaccharide induced pro-inflammatory mediators (nitric oxide and prostaglandin E2) in murine macrophage RAW 264.7 (leukemia) cells, and S. muticum has been suggested as a possible source of anti-inflammatory products (Yoon et al. 2010). Also, a methanolic dichloromethane extract from S. muticum has been found to have antibacterial activity against Proteus mirabilis (a cause of wound and urinary tract infections) (Villarreal-Gomez et al. 2010). The specific compounds responsible for anti-inflammatory activity were not determined, but a recent study has found that fucoxanthin has anti-inflammatory effects in obese mice (Tan and Hou 2014); fucoxanthin, the main carotenoid in S. muticum, could therefore be one of the anti-inflammatory agents.

3.10.2 Cytoprotection

Ethyl acetate extracts from S. muticum have been found to have a cytoprotective effect against ultraviolet B (UVB)-induced oxidative cell damage in human keratinocytes (the predominant cell type in the epidermis) (Piao et al. 2011, 2014). Although the compounds responsible for this cytoprotective effect were not identified, sargaquinoic acid and sargachromenol isolated by methanol extraction from other species of Sargassum have been shown to influence UV-induced damage to keratinocytes (Hur et al. 2008).

3.10.3 Obesity

Ethanol extracts from S. muticum significantly decreased expression of adipogenic marker genes, body weight gain, fat tissue content, serum cholesterol and triglyceride levels in mice fed a high fat diet, and could be the basis for an anti-obesity treatment (Ahn et al. 2012, 2013). The active compounds responsible for this potential anti-obesity treatment were not identified, but it was suggested that the effect is due to activation of the AMPK (adenosine monophosphate-activated protein kinase) pathway. Fucoxanthin, the main carotenoid in S. muticum, has also been found to have anti-obesity properties by induction of the mitochondrial uncoupling protein UCP1 in abdominal white adipose tissue leading to fatty acid oxidation and heat production (Abidov et al. 2010; Kozak and Anunciado-Koza 2008; Maeda 2015; Miyashita et al. 2011). Fucoxanthin could again be one of the active ingredients in ethanol extracts from S. muticum.

3.11 Other uses

In addition to fuel, food, fertiliser, and therapeutic products, S. muticum is being researched for a number of other applications.

3.11.1 Wastewater treatment

S. muticum has been suggested as a low cost bio-sorbent for the treatment of wastewater from industries that use dyes and phenolic compounds due to its rapid absorption and high absorption capacity for phenolic compounds and industrial dyes such as methylene blue (Rubin et al. 2005, 2006; Zhao et al. 2008). Liu et al. (2013) have reported that S. muticum has been used in China for the sorption of heavy metals.

3.11.2 Insecticides

Aqueous extracts of S. muticum have recently been shown to have insecticidal activity, although the compounds responsible for this activity were not determined (Moorthi et al. 2015).

3.11.3 Anti-fouling

Chloroform (Plouguerne et al. 2008, 2010) and ethanol (Hellio et al. 2001; Silkina et al. 2009) extracts from S. muticum have antimicrobial activity against several bacterial, fungal, and microalgal strains involved in marine biofilm formation and could be the basis of an antifouling product. Palmitic acid extracted by solvents from S. muticum is potentially one of the active compounds inhibiting biofouling organisms (Bazes et al. 2009).

3.12 Economics and biorefinery processes for valorisation of S. muticum

There appears to have been little work on the economics of valorisation of S. muticum. However, Balboa et al. (2015) have recently examined the biofinery concept for S. muticum for the production of 6 potential products including fucoidans and fucoxanthin. It was concluded that it was essential that only “green processes” such autohydrolysis and supercritical-CO2 extraction and fractionation should be applied, and that biorenewable, reusable and less toxic solvents (subcritical water, ethanol, and supercritical-CO2), rather than traditional fossil fuel solvents, should be used. The biorefining of S. muticum that includes the production of fucoxanthin (assuming a commercial value of €9000 g−1) has been shown to be the most commercially promising of four processes to produce combinations of alginate, antioxidants and fucoxanthin, although it had the highest environmental impact (Perez-Lopez et al. 2014).

4 Conclusion

In spite of several eradication attempts, Japanese wireweed, S. muticum, has now become a permanent member of the European coastline’s aquatic flora. At present, this macroalga has no real economic value, and is therefore not harvested for commercial exploitation. Due to high heavy metal uptake, ash and water content, it is unlikely that this seaweed would be useful as a source of food or fuel. However, using S. muticum grown under aquaculture conditions could produce a food supplement with health benefits due to naturally high levels of certain antioxidants (tocopherol, fucoxanthin, and other carotenoids and phenolic compounds). Precise mechanisms of action are still not clear and further research is required to determine both the preventative and therapeutic roles of bioactive compounds isolated from S. muticum, although anti-inflammatory, anti-obesity, anti-tumour and antioxidant activities have been demonstrated. Fucoxanthin itself has a range of therapeutic effects and its extraction from S. muticum as part of a biorefinery approach to exploit this invasive seaweed may be a profitable avenue for further research. The most commercially viable use for S. muticum may therefore be to turn this macroalgal ‘menace’ into natural medicines.