220 Annales Universitatis Paedagogicae Cracoviensis Studia Naturae, 5: 220–237, 2020, ISSN 2543-8832 DOI: 10.24917/25438832.5.14 Sylwia Śliwińska-Wilczewska*, Gracjana Budzałek, Zuzanna Kowalska, Marek Klin, Adam Latała Institute of Oceanography, University of Gdansk, Av. Piłsudskiego 46, 81-378 Gdynia, Poland; *ocessl@ug.edu.pl Baltic macroalgae as a potential source for commercial applications – review Introduction �e Baltic Sea is a well-known shallow inland sea that lies on the continental shelf in northern Europe. �e Baltic Sea separates the Scandinavian Peninsula from the rest of continental Europe and is surrounded by nine countries (i.e. Sweden, Finland, Russia, Estonia, Latvia, Lithuania, Poland, Germany, and Denmark). �e Baltic Sea is an arm of the Atlantic Ocean, extending from northern Germany and Poland in the south almost to the Arctic Circle in the north. �e area of the Baltic Sea, together with the Kattegat, covers about 415,000 km2. �e Baltic Sea is classi�ed as one of the world’s 66 “large marine ecosystems” (Snoeijs-Leijonmalm et al., 2017). �e marine in�uence on the Baltic Sea ecosystem is large but it is strongly in�uenced by freshwater as well. �e average salinity of the Baltic Sea is 7.5%, while the ocean’s salinity is 36.6%. Salinity is also one of the main determinants of species diversity in macroalgae (Rybak, 2018). �e �ora of the Baltic Sea is relatively poor, which means that there are few plant spe- cies in the Baltic Sea (Deluga, 2018). However, despite the low salinity of Baltic waters, there is a group of organisms that creates an interesting ecosystem. Algae are considered one of the �rst forms of life that demonstrated the ability to photosynthesize, and they appeared on Earth about one and a half billion years ago. �ese autotrophic non-tissue organisms are the most numerous group of self-nutrient aquatic organisms, and their growth is enabled by components such as phosphorus and nitrogen, as well as carbon dioxide and sunlight (Buchholz et al., 2012). �ey do not have vascular systems, leaves, stems, and roots, but only elements that resemble them (Bedoux et al., 2014). Macroalgae are rich in various biologically active sub- stances valued for their unique properties. Currently, algae biomass is a  renewable source with many active substances that are widely used the chemical, food, agri- culture, cosmetics, pharmacy, and medicine industries, among others (McLachlan, B altic m acroalgae as a potential source for com m ercial applications – review 221 1985). An example of the commercial application of algae mass resources from the Polish part of the Baltic Sea is the use of Furcellaria fastigiata for agar production (Biłos et al., 2016). Moreover, in Poland, selected groups of macroalgae have been used as a raw material for industry and agriculture. �is group of algae includes Ulva sp. and Cladophora sp., which most o�en form high biomass in freshwater reservoirs (Schroeder et al., 2013). Macroalgae are classi�ed as so-called: green algae (Chlorophyta Reichenbach, emend. Pascher, emend. Lewis & McCourt), brown algae (Phaeophyceae Kjellman) and red algae (Rhodophyta �uret, emend. Rabenhorst, emend. Adl et al.). Macroal- gae are a  source of mineral substances, polysaccharides, proteins, lipids, phytohor- mones, and pigments, as well as many di�erent secondary metabolites (phenolic com- pounds, terpenoids, halogenated compounds, sulfur derivatives, and nitrogen deriva- tives), and their biochemical composition depends on where the samples were taken, harvest season, and the environment (Buchholz et al., 2012). Hence, it is of important interest to present the possibilities for practical use of macroalgae derived from di- verse ecosystems, such as the Baltic Sea (Fig. 1). The potential use of bioactive compounds of Baltic macroalgae in the medical and cosmetic industry Macroalgae abound in various active substances used in medicine and the cosmetic industry (Bedoux et al., 2014). Macroalgae are considered a source of bioactive com- pounds because they can produce many di�erent secondary metabolites characterised by a broad spectrum of biological activity (Gupta, Abu-Ghannam, 2011). Fig. 1. Examples of the possible use of Baltic macroalgae as industrial resources S yl w ia Ś liw iń sk a- W ilc ze w sk a, G ra cj an a B ud za łe k, Z uz an na K ow al sk a, M ar ek K lin , A da m L at ał a 222 Baltic macroalgae used in the cosmetic industry �e use of macroalgae in the cosmetic industry is becoming increasingly desirable due to the natural ingredients’ broad spectrum and that they are easy to harvest, while at the same time they do not harm the environment. �e biomass of marine macroalgae is o�en used to produce ingredients in cosmetics. �ese ingredients can have one of three main functions: as additives that contribute to organoleptic properties, to stabilise and preserve a  product, or as bioactive compounds that perform the true function and cosmetic activity (Bedoux et al., 2014). It has been shown that metabo- lites derived from macroalgae are useful in many aspects of anti-aging, anti-cellulite, and slimming care, as well as having antioxidant, photoprotective, moisturizing, and whitening properties (Wang et al., 2014). �e diversity of macroalgae species and their broad biochemical composition means that they are a potentially a source of bioactive compounds (Buchholz et al., 2012). Macroalgae are rich in vitamins such as A, B1, B2, B3, B5, B6, B9, B12, C, D, E, and K, i.e. virtually all essential amino acids, macroelements and trace elements, such as iodine. �e skin aging process results from various factors inside and outside the body, which include diet, the passage of time and subsequent changes in the body, envi- ronmental pollution, and exposure to light or stress (Bedoux et al., 2014). During skin aging, cells lose the ability to regulate generated reactive oxygen species and su�er from oxidative stress. In the epidermis and dermis, the number of melano- cytes and keratinocytes is reduced, as well as the ability to multiply cells and migrate �broblasts, leading to a decrease in cellular activity and protein synthesis (Wang et al., 2014). Sulphated polysaccharides that are derived from marine algae may have various biological and biochemical e�ects, i.e. modulating proteolysis of connective tissue, anti-in�ammatory e�ects, adversely a�ecting the development of free radi- cals and antioxidants, as well as prevention of oxidative damage. �ese properties, among others, have been identi�ed for green algae, Ulva lactuca L. and Codium tomentosum Stackhouse (Bedoux et al., 2014). Ulva populations originated mainly from shores and estuaries, with a minor number occurring in ocean lagoons, coastal lakes, canals, and rivers. Ulva species were present in a  very wide range of saline waters (from fresh to hypersaline waters) (Rybak, 2018). �erefore, the genus Ulva is common in the Baltic Sea and may constitute 22–75% of biomass in the Gulf of Gdańsk (Filipkowska et al., 2009). It is also worth mentioning that U. lactuca is one of the macroalga from the Baltic Sea described by Linnaeus (Dominguez, Loret, 2019) and an organism that can be e�ciently used in the cosmetic industry. Additionally, other species of Ulva occur in the Baltic Sea – U. �exuosa Wulfen, U. intestinalis L., and U. linza L., whose potential health properties have not yet been studied (Fig. 2). On the other hand, Codium tomentosum is not a  typical species B altic m acroalgae as a potential source for com m ercial applications – review 223 found in the Baltic Sea. However, the other species, C. fragile, can be found in the Kattegat (Nyberg, 2007). Macroalgae are also an important source of amino acids, amino acid derivatives and peptides which can stimulate collagen production in the human skin. Addition- ally, hydrolysates of algae proteins from macroalgae of the genus Undaria, Sargassum, Porphyra, Palmaria, and Ulva show antioxidant activity, which is important in an- ti-aging care. �ese species: Sargassum muticum (Yendo) Fensholt, Porphyra umbili- calis Kützing, Palmaria palmata L., and Ulva sp., also occur in the Baltic Sea (Snoei- js-Leijonmalm et al., 2017). It is worth noting that many marine macroalgae cannot survive the low salinity of the Baltic Sea; however, these species are still found in the lower sublittoral of the Belt Sea (HELCOM, 2012; Snoeijs-Leijonmalm et al., 2017). Furthermore, a polypeptide from Ulva sp., called Aosa biopeptide, is used in cosmetic products and consists of glycine, arginine, lysine, valine, and aspartic acid. �e tripep- tide consisting of arginine-glycine-aspartic acid was found to stimulate mechanisms underlying collagen production through tissue growth factor and cause an increase in collagen biosynthesis in human �broblasts. Biopeptides from macroalgae can be used as a potential source of synthetic components and can contribute to the prevention of aging. Enzymatic hydrolysis of algae proteins could allow for the isolation of peptides useful in the development of skin bioactive compounds. External aging causes expo- sure to UV radiation and associated irritation, characterized by a deterioration of the extracellular skin matrix and keratinocyte dysplasia in the epidermis, causing wrin- kles, �abbiness, roughness, and spotty pigmentation. UV light is divided into UVA, UVB, and UVC. UVA can penetrate the dermis and not only causes wrinkles but also various skin-related ailments; UVB is more carcinogenic and causes the skin to turn red and burn 1,000 times faster than UVA; while UVC is blocked by the ozone layer, and therefore does not pose a  risk to the skin (Wells et al., 2017). Macroalgae have mechanisms that counteract the harmful e�ects of UVB and UVA, producing photo- synthetic pigments such as carotenoids and phenolic compounds (e.g. phlorotannins) Fig. 2. Di�erent Ulva species that occur in the Baltic Sea: Ulva lactuca L. (A), Ulva �exuosa Wulfen (B), Ulva intestinalis L. (C), and U. linza L. (D) (Photo. S. Śliwińska-Wilczewska) S yl w ia Ś liw iń sk a- W ilc ze w sk a, G ra cj an a B ud za łe k, Z uz an na K ow al sk a, M ar ek K lin , A da m L at ał a 224 or compounds that absorb UV radiation. UV absorbing compounds are bioactive and can protect human �broblast cells against cell death caused by UV radiation and in- hibit the aging of human skin (Bedoux et al., 2014). Moisturizing is the most important step in preventing skin aging by helping to maintain a healthy appearance and elasticity while strengthening its protective barri- er against harmful environmental factors. Polysaccharides derived from macroalgae are environmentally friendly substances, relatively inexpensive, and can be used as substitutes for petrochemical products. Polysaccharides and oligosaccharides provide a  high water storage capacity. Macroalgae extracts contain �oridoside and iso�ori- doside acids. �ese components have properties that enable them to increase water retention in the stratum corneum, and thus take part in moisturizing the skin. It was noted that the red algae Chondrus crispus (L.) J.Stackhouse are rich in polysaccharides and minerals that have a moisturizing, �rming, and soothing e�ect. Moreover, extract from the green algae Codium sp. can regulate the distribution of water in the skin, and thus protect the skin from dryness, especially in an arid environment (Wells et al., 2017). �e described macroalgae species (Chondrus crispus and Codium fragile (Suringar) Hariot) can be found in the west area of the Baltic Sea (Snoeijs-Leijonmalm et al., 2017). C. crispus and C. fragile live permanently submerged in the Kattegat at a water depth that ranges from 0.5–1 m to 4–5 m (Nyberg, 2007). Cellulite is a cosmetic problem that causes the appearance of hollows on the skin surface. �is problem is a combination of expanding fat cells that accumulate under the skin and �brous stripes that run perpendicular to the skin’s surface. Cellulite in- cludes changes in the biochemistry of the subcutaneous fat layer. �ese changes in- clude increased lipogenesis, reduced lipolysis, and increased lipid storage in fat cells. Energy homeostasis is regulated by the chronobiology of fat cells through the mecha- nisms of lipogenesis and lipolysis. Some local cellulite treatments include macroalgae extracts, such as those used to increase microcirculation �ow, reduce lipogenesis, and improve lipolysis, which restore the normal structure of the dermis and subcutaneous tissue and remove or prevent free radicals. �e macroalgae most commonly used in anti-cellulite and slimming preparations are brown algae, Fucus vesiculosus L., Fur- cellaria lumbricalis (Hudson) J.V.Lamouroux, Laminaria digitata (Hudson) J.V.Lam- ouroux, and Pelvetia sp. (Bedoux et al., 2014). �ey stimulate blood �ow and help the body excrete excess �uid. �us, the Baltic macroalgae Fucus vesiculosus and Furcellar- ia lumbricalis can reduce or eliminate cellulite problems (Fig. 3). The potential use of macroalgae in the medical industry Macroalgae are also becoming increasingly popular due to properties that are useful in the medical industry (Buchholz et al., 2012). �e most bioactive compounds in mac- B altic m acroalgae as a potential source for com m ercial applications – review 225 roalgae include sulfated polysaccharides, phlorotannins, and diterpenes. �ese com- pounds have strong antiviral, antibacterial, and anticancer properties. Polysaccharides are a  class of macromolecules that are increasingly gaining importance in the �eld of biochemistry and medicine due to their immunomodulatory, anticancer, antiviral, and antithrombotic e�ects. �ey are mainly present in cell walls and their composi- tion varies depending on the season, age, species, and geographical location of the macroalgae (Gupta, Abu-Ghannam, 2011). In addition to con�rmed anticoagulant and antiviral activity, they act on the in�ammatory and immune systems. Macroalgae produce various polysaccharides, such as alginic acid (also called algin), fucoidan, and laminarin (also known as laminaran) (Milledge et al., 2015). Alginate produced by brown algae, especially in the form of sodium and calcium alginate, is widely used in the pharmaceutical industry due to its ability to chelate metal ions and create very sticky solutions, while sulfated polysaccharides from macroalgae show various bio- logical activities with potential medical value, including antitumor, antiviral, and an- tioxidant activity. Fucoxanthin is another interesting compound. Fucoxanthin is the main biofunc- tional pigment present in brown algae and is one of the most numerous carotenoids found in nature. Fucoxanthin has antioxidant and anti-cancer properties. It has re- cently been found that fucoxanthin can help increase metabolism, thereby controlling weight gain (Gupta, Abu-Ghannam, 2011). �ere are many di�erent species of brown algae in the Baltic Sea, including species of the genus Fucus (Fucus cottonii M. J. Wynne & Magne, F. evanescens C. Agardh, F. radicans L. Bergström & L. Kautsky, F. serratus �unberg, F. spiralis L., F. vesiculosus), as well as Ascophyllum nodosum L., Ectocarpus siliculosus (Dillwyn) Lyngbye, Scytosiphon lomentaria (Lyngbye) Link, Chorda �lum L. and Pylaiella littoralis L., hence, Baltic brown algae could useful to both the pharma- ceutical and the medical industries (Snoeijs-Leijonmalm et al., 2017). Fig. 3. Examples of the Baltic macroalgae: brown algae Sargassum muticum (Yendo) Fensholt (A), red algae Chondrus crispus L. (B), and green algae Codium fragile (Suringar) Hariot (C) that can be used in the cosmetic industry (Photo. S. Śliwińska-Wilczewska) S yl w ia Ś liw iń sk a- W ilc ze w sk a, G ra cj an a B ud za łe k, Z uz an na K ow al sk a, M ar ek K lin , A da m L at ał a 226 Baltic macroalgae used in the food industry Macroalgae, due to their richness in vitamins and macroelements, are o�en use in the food industry. From a  nutritional point of view, edible macroalgae are low-cal- orie foods with a high concentration of minerals, vitamins, and proteins, and low li- pid content. Currently, they are willingly consumed on a global scale. �anks to their interesting properties, they are also used in the production and processing of food products such as emulsifying, gelling, or water-retaining agents. Macroalgae are an excellent source of vitamins A, C, D, and E and group B vitamins such as ribose, nia- cin, pantothenic acid, and folic acid (Fitzgerald et al., 2011). �ey also derive an un- usual wealth of minerals from the sea, which can constitute up to 36% of their dry matter. Macronutrients include sodium, calcium, magnesium, potassium, chlorine, sulfur, and phosphorus as well as micronutrients such as iodine, iron, zinc, copper, selenium, molybdenum, �uorine, manganese, boron, nickel, and cobalt (Kandale et al., 2011). It follows that the composition of macroalgae comprises almost all of the vitamins, the most important macroelements necessary for the proper functioning of the human body, as well as iodine which is responsible for a healthy thyroid (Buchholz et al., 2012). As a result, algae are o�en used as components of a healthy diet, in the form of salads, soups, various types of snacks, and also as widely distributed dietary supplements in well-developed countries to help maintain health. Macroalgae are a  rich source of iodine. �e highest iodine content is found in brown algae. In most cases, red and green algae have lower iodine content but still a high value compared to terrestrial plants. �e daily adult requirement for iodine is currently 150 µg per day, and this dose can be reached by very small amounts of mac- roalgae. Just one gram of dried brown algae contains 500 to 8,000 µg of iodine, and green algae and red algae provide 100–300 µg in one gram (Kandale et al., 2011). It follows that the introduction of a small number of macroalgae into the diet is enough to maintain a healthy thyroid. Furthermore, a large part of the world population re- ceives insu�cient iodine because other food sources (plants, animals) contain very low levels of this element. An interesting feature of macroalgae is their richness of proteins and bioactive peptides. �e composition and concentration of proteins depend on the species, place, and time of harvest. �e protein fraction of brown algae is relatively low (1–24% of dry matter) compared to green algae (4–44% of dry matter) and red algae (5–50% of dry matter) (Fitzgerald et al., 2011). Most macroalgae contain all necessary amino acids and acidic amino acids, e.g. glutamic and aspartic acids, and as is well known, protein is a critical nutrient due to its very important role in the human body. Macroalgae are a very good source of nutrients and have a relatively low-fat content (0.3–5% of dry matter) (Bedoux et al., 2014). B altic m acroalgae as a potential source for com m ercial applications – review 227 Macroalgae also contain large amounts of polysaccharides (which include hydro- colloids), especially in their cell walls. Hydrocolloids have gained commercial signi�- cance as food additives. �e food industry uses their gelling, water-retaining, emulsi- fying, and other physical properties. Agar is used in food products such as confection- ery, meat and poultry products, desserts and drinks, and molded foods. Carrageenan is used in salad and sauces, dietary foods, and as a preservative in meat and �sh prod- ucts, dairy products, and baked goods (Kandale et al., 2011). Regular consumption of macroalgae has many positive health bene�ts which were describe in the previous chapter. Macroalgae are also widely used in the food industry as thickening aqueous solutions, for gel production, and in the production of items such as toothpaste, ice cream, and anti-cancer mayonnaise (Milledge et al., 2015). Macroalgae have gained great popularity as an interesting addition to dishes or as basic ingredients of dishes. �e best example is sushi, which is a well–known food across the world, for which nori (red algae Porphyra umbilicalis) is needed. Other ex- amples are Kombu (brown algae Laminaria japonica Areschoug) and Wakame (brown algae Undaria pinnati�da (Harvey) Suringar), which are used in various types of sal- ads, soups, and starters (Kolb et al., 2004). Although the mentioned species do not occur in the Baltic Sea, other common Baltic species of brown algae (e.g. Fucus sp., Ascophyllum sp.) or red algae (e.g. Furcellaria sp., Polysiphonia sp.) can be successfully used in the food industry. Possible use of Baltic macroalgae in the energy industry �e energy industry is of vital importance for the proper functioning of the world’s economies. Alternative energy sources are being sought out as non-renewable re- sources are becoming depleted. Carbon, which is the most basic energy source in Po- land, is not an ideal source of energy due to the negative impact on the environment during its combustion or extraction, similar to oil. �erefore, alternative raw materials are sought, with one being biodiesel obtained from macroalgae. For now, it is quite a  promising material that has great market potential, as its production can be very pro�table with low environmental losses. At present, macroalgae are not widely used as energy sources; however, many promising studies are being conducted in this direc- tion (Filipkowska et al., 2008). Several solutions have been proposed for the production of biofuels to replace fos- sil fuels. Biodiesel and bioethanol produced by terrestrial plants have attracted the world’s attention as potential alternative solutions. However, due to the other various uses of terrestrial plants, e.g. for consumption, doubts have arisen about converting them to biofuels. �erefore, it is necessary to �nd a new raw material for the produc- tion of biofuels that can generate similar by-products as terrestrial plants but can be S yl w ia Ś liw iń sk a- W ilc ze w sk a, G ra cj an a B ud za łe k, Z uz an na K ow al sk a, M ar ek K lin , A da m L at ał a 228 produced solely for energy purposes. Macroalgae are one alternative to convention- al terrestrial plant cultivation. �e production of biofuels from macroalgae is widely considered to be one of the most suitable methods. �ese plants are an economically and environmentally sustainable renewable biomass source for biofuel production be- cause they are simple aquatic organisms that carry out photosynthesis and their diver- sity is much greater than terrestrial plants. Almost all of macroalgae biomass can be converted into energy and their waste residues into methane and hydrogen. �ey also contain oils that can be used as a raw material for biodiesel and carbohydrates that can be converted into bioethanol. Macroalgae have the advantage of not interfering with food production and have the potential to cover global demand for transport fuels (Suganya et al., 2016). Anaerobic digestion is a biological process used to produce methane-rich gas from biomass. �is digestion process involves the following steps: i) hydrolysis of organic matter, ii) the synthesis of acetic acid from hydrolysis products, and iii) the production of methane by the relevant bacteria. Macroalgae have a similar composition as other sources of organic materials and should be adapted to existing anaerobic digestion installations. However, the content of seaweed-related compounds, such as salts, can inhibit the fermentation process. �erefore, they need to be pre-processed, including at minimum washing, to prevent inhibition of the fermentation process (Milledge et al., 2014). Anaerobic fermentation of macroalgae allows for the production of biogas consisting of about 60% methane and 40% CO 2 (and trace amounts of CO, H2S, H2, N2, and O2). �e composition of macroalgae may also vary depending on the season and location, which may a�ect production performance. For example, the methane yield of Saccharina latissima (Linnaeus) C.E.Lane (syn. Laminaria saccharina (L.) Lamour- oux) algae is twice as high from material collected in autumn than material collected in spring (Roesijadi et al., 2010). S. latissima occurs in the west area of the Baltic Sea; however, this species is poorly adapted to the low salinity. It is assumed that at the inner Baltic distributional limit of S. latissima in the southern Baltic Sea proper, its up- per limit lies at the water depth of about 20 m (Wærn, 1965). Fermentation of biomass to ethanol consists of two reactions: i) hydrolysis of organic material to simple sugars (using high temperature, enzymes, or acids) and ii) fermentation of sugars to ethanol. Macroalgae use polysaccharides such as sulfated polysaccharides, mannitol, alginates, agar, and carrageenan to produce ethanol. Brown algae, especially those of the genus Laminaria, are the most desirable macroalgae for alcoholic fermentation because they contain the most polysaccharides. Macroalgae biomass has great potential for produc- ing biofuels, although there are challenges in its processing. However, much research is currently underway to identify methods for maximizing its potential for energy generation (Milledge et al., 2014). B altic m acroalgae as a potential source for com m ercial applications – review 229 Baltic macroalgae as natural fertilisers and products for wastewater treatment Macroalgae are becoming increasingly popular as natural fertilisers. �is is due to the presence of nitrogen, magnesium, potassium, and some trace elements in their com- position (Mohy El Din, 2015). �ese plants also have a great ability to absorb nitrogen and phosphorus, which are very important to their growth. In addition to macroele- ments and microelements, they also contain phytohormones, which positively a�ect growth of macroalgae. Liquid macroalgae extracts and suspensions have gained wider application than microalgae meal due to their ease of use. Most o�en, fertilisers are based on algae such as Ascophyllum sp. and Fucus sp. �ese macroalgae are found mainly in the western part of the Baltic Sea. �e intertidal species F. vesiculosus lives permanently submerged in the Kattegat. It grows just below the water surface, with F. spiralis above it and Ascophyllum nodosum (Linnaeus) Le Jolis and Fucus serratus L. below it (Snoeijs-Leijonmalm et al., 2017). Large amounts of insoluble carbohydrates act as soil improvers (better aeration, structure) and also help retain soil moisture. It has been shown that they not only provide nutrients needed for growth but also in- crease seed germination, improve tolerance to low temperatures, and are harmful to some insects (Milledge et al., 2015). �ey can, therefore, be an alternative to abused chemical fertilisers that have a negative impact on the environment �ere are two main areas where macroalgae have the potential to be used in waste- water treatment. �e �rst is for wastewater and some agricultural waste treatments to reduce total nitrogen- and phosphorus-containing compounds before release of these puri�ed waters into rivers or oceans. �e second is for the removal of toxic metals from industrial wastewater. Macroalgae can be used to reduce nitrogen and phospho- rus content in wastewater a�er treatment. Many microalgae take up ammonium as an absorbable form of nitrogen for growth, and this ion is a common form of nitrogen in most domestic and agricultural wastewater. Another important feature of many mac- roalgae is their ability to absorb large amounts of phosphorus (McHugh, 2003). �e usefulness of macroalgae in wastewater treatment is increasingly known but its large- scale application has not yet been implemented, although this may change with grow- ing awareness of the need to protect the marine environment. �e accumulation of heavy metals such as copper, nickel, lead, zinc, and cadmium by macroalgae became apparent when they were consumed and their chemical composition studied. �e con- tent of heavy metals, especially in large brown algae, depends on their geographical location as well as their proximity to industrial points. For this reason, the idea of using macroalgae as biological indicators of heavy metal pollution, both from natural sources and from activities such as the extraction or disposal of industrial waste, was proposed (McHugh, 2003; Żbikowski et al., 2006, 2007). Removal of toxic metals was S yl w ia Ś liw iń sk a- W ilc ze w sk a, G ra cj an a B ud za łe k, Z uz an na K ow al sk a, M ar ek K lin , A da m L at ał a 230 implemented using brown algae of the genera Sargassum, Laminaria and Ecklonia and the green algae Ulva sp. �ey were also used to remove heavy metals in wastewater treatment (McHugh, 2003). Among these organisms, Sargassum muticum occurs in the Baltic Sea but only in the more saline areas in the Arkona Sea, the Belt Sea, and the Öresund (Nyberg, 2007). Ulva sp. is commonly found in the entire Baltic Sea. It is possible to use Baltic macroalgae to remove heavy metals near factories, processing plants, and sewage treatment plants as one of the stages in this process. Macroalgae as a biological factor limiting the occurrence of massive cyanobacterial blooms in the coastal area of the Baltic Sea �e presence of macroalgae is of great importance for the biological structure, ecosys- tem functioning, and water quality in shallow water bodies (van Donk, van de Bund, 2002; Hilt, Gross, 2008), as well as in the Baltic Sea. Underwater meadows provide shelter for the development of numerous animals and are the basis of the diet for aquatic organisms (Rybak, 2016; Wells et al., 2017). �ey can also be used to assess the ecological state of the marine environment (Saniewski, 2013). Macroalgae e�ectively compete with phytoplankton species for available nutrients (Rybak, Gąbka, 2018). It has been shown that in a  large number of cases, allelopathic compounds produced by macroalgae act on organisms in a  di�erent way than most synthetic herbicides (Ohad, Hirschberg, 1990; Huppatz, 1996). �ese compounds have a broader range of action on target organisms than synthetic inhibitors (Duke et al., 2001). �erefore, the importance of the allelopathic e�ects of macroalgae in aquatic ecosystems is gaining interest due to their potential ability to control or limit the occurrence of organisms forming massive blooms, including harmful cyanobacteria (Berger, Schagerl, 2003; Wang et al., 2007; Tang, Gobler, 2011; Pakdel et al., 2013; Ghobrial et al., 2015). Złoch et al. (2018) tested the allelopathic activity of several representatives of Baltic macroalgae from the genus Chara on the growth of picocyanobacteria Synechococcus sp. It was shown that the addition of aqueous extracts from Chara aspera C.L.Will- denow, C. baltica (C.J.Hartmann) Bruzelius, and C. canescens Loiseleur signi�cantly a�ected the cell number in Synechococcus sp. culture. �e addition of aqueous extracts from C. canescens in a concentration of 5, 25, and 50 μL mL–1 caused the cell number of picocyanobacteria to decrease to 86%, 78%, and 48%, respectively, a�er a week of exposure, compared to control conditions. On the other hand, the addition of 25 and 50 μL mL–1 extracts obtained from C. baltica caused a reduction in the cell number of Synechococcus sp. to 55% and 44%, respectively. In turn, the addition of 50 μL mL–1 of an extract from Chara aspera inhibited the growth of picocyanobacteria a�er a week of exposure. In this experiment, the number of picocyanobacteria cells decreased to 90% compared to the control treatment. It is believed that the chemical composition B altic m acroalgae as a potential source for com m ercial applications – review 231 and proportions of allelopathic compounds may play a signi�cant role in determining their e�ect on the growth of various phytoplankton species, including cyanobacteria (Pakdel et al., 2013). �erefore, weaker inhibition of the growth of picocyanobacteria by C. aspera extract, compared to C. baltica and C. canescens, may be due to the pres- ence of various allelopathic compounds and their concentrations. �is varied sensi- tivity to allelopathic compounds indicated that species belonging to the genus Chara may a�ect the growth and occurrence of Synechococcus sp. Moreover, the negative ef- fects may be stronger in the natural environment, since these macroalgae occupy large areas of the bottom of the southern Baltic Sea and allelopathic compounds can be constantly released into environment (Granéli, Hansen, 2006). Studies demonstrating the allelopathic activity of C. aspera, C. baltica, and C. canescens on Synechococcus sp. indicated that these macroalgae may potentially control the extent of picocyanobacte- ria in coastal Baltic waters. As mentioned earlier, the lack of recognition of the allelopathic activity of Baltic macroalgae from the southern Baltic region on the associated species of �lamentous cyanobacteria prompted us to conduct relevant laboratory experiments. Representa- tives of typical the Baltic macroalgae Ulva intestinalis, as well as �lamentous cyanobac- teria Nodularia spumigena and Nostoc sp., were selected for the study. �e cyanobac- teria strains were maintained as a non-axenic batch culture in the Culture Collection of Baltic Algae (CCBA) at the Laboratory of Marine Plant Ecophysiology, University of Gdańsk, Poland. �e brackish macroalga was selected, based on the allelopathic potential of species from the order of Ulvales (e.g. Wang et al., 2007). Baltic U. intestinalis was collected manually from the coastal zone of the Gulf of Gdańsk, Poland (54°47ʹ13.8ʺN 18°25ʹ33.7ʺE) and carefully washed several times with distilled water in the laboratory to remove attached organisms as described by previous researchers (Złoch et al., 2018). �e allelopathic e�ects of U. intestinalis were tested according to a method proposed by Wang et al. (2007) with modi�ca- tions. �e monocultures of cyanobacteria Nodularia spumigena Mertens ex Bornet & Flahault and Nostoc sp. were exposed to three concentrations of both water ex- tracts and �ltrate originating from U. intestinalis. �e �nal concentrations of extract and �ltrate were: 5, 25 and 50 µL mL–1. Moreover, to compare the e�ects on the two cyanobacteria of di�erent concentrations of fresh tissue from the U. intestinalis, coexistence assays were performed using a mixed culture system of one macroalga and one cyanobacteria. Di�erent initial inoculation concentrations (0, 0.5, 2.5, and 5 g-wet wt L−1) of fresh macroalgal tissues were inoculated into 25 mL Erlenmeyer �asks containing 20 mL f/2 culture medium. Selection of these concentrations was based on preliminary experiments to determine the most relevant e�ectiveness. It was found that the growth of target cyanobacterium N. spumigena, a�er addition of 5, 25, and 50 µL mL–1 �ltrate and the presence of 0.5, 2.5, and 5 g-wet wt L−1 live tis- S yl w ia Ś liw iń sk a- W ilc ze w sk a, G ra cj an a B ud za łe k, Z uz an na K ow al sk a, M ar ek K lin , A da m L at ał a 232 sue from U. intestinalis, was signi�cantly reduced to approximately 40%, compared to the control treatment (Fig. 4). On the other hand, the addition of �ltrate and the presence of live tissue of U. intestinalis had no statistical e�ect on the number of Nostoc sp. cells (p > 0.05; Fig. 5). Slight stimulation of the tested cyanobacteria was noted a�er the addition of aque- ous extract, which may be the result of hormesis or the accumulation of nutrients in macroalgae tissue. Based on the results, it can be concluded that Baltic macroalgae of the genus Ulva have the potential to a�ect the occurrence and abundance of some bloom-forming species of cyanobacteria. Research on the allelopathic e�ect of mac- roalgae on the growth of �lamentous and bloom-forming cyanobacteria occurring in the southern Baltic Sea region is an interesting pursuit that should be recognized as requiring continuation. Fig. 4. �e number of Nodularia spumigena Mertens ex Bornet & Flahault cells (105 cell mL−1) for con- trols and experiments with addition of (A) extracts: 5 (a), 25 (b), and 50 (c) (μL mL−1), (B) �ltrate: 5 (a), 25 (b), and 50 (c) (μL mL−1), and (C) tissue: 0.5 (a), 2.5 (b), and 5 (c) (g-wet wt L−1) obtained from Ulva intestinalis L. a�er 14 days of exposure. �e values refer to means (n = 3, mean ± SD). Asterisks indicate statistically signi�cant di�erence compared to the control obtained with the ANOVA. Levels of signi�- cance were *p < 0.05; **p < 0.01; ***p < 0.001. B altic m acroalgae as a potential source for com m ercial applications – review 233 Conclusions Baltic macroalgae are organisms which may be used as industrial resources thanks to their unique properties. Due to their content of vitamins, as well as macro- and microelements, they are becoming increasingly popular as foods and supplements but also have great potential to gain signi�cance in the pharmaceutical industry. Similar trends can also be observed in the cosmetic industry, where macroalgae are an in- creasingly important ingredient in anti-aging, anti-cellulite, and moisturizing prod- ucts. �e energy industry has also become interested in macroalgae due to the search for natural solutions for energy production, i.e. biofuel. Baltic macroalgae can also be used as natural fertilisers and products for wastewater treatment. Finally, based on the research, it can be concluded that some Baltic macroalgae may allelopathically a�ect bloom-forming cyanobacteria. �us, the study of the allelopathic activity of macroal- Fig. 5. �e number of Nostoc sp. cells (105 cell mL−1) for controls and experiments with addition of (A) extracts: 5 (a), 25 (b), and 50 (c) (μL mL−1), (B) �ltrate: 5 (a), 25 (b), and 50 (c) (μL mL−1), and (C) tissue: 0.5 (a), 2.5 (b), and 5 (c) (g-wet wt L−1) obtained from Ulva intestinalis L. a�er 14 days of exposure. �e values refer to means (n = 3, mean ± SD). Asterisks indicate statistically signi�cant di�erence compared to the control obtained with the ANOVA. Levels of signi�cance were *p < 0.05; **p < 0.01; ***p < 0.001. S yl w ia Ś liw iń sk a- W ilc ze w sk a, G ra cj an a B ud za łe k, Z uz an na K ow al sk a, M ar ek K lin , A da m L at ał a 234 gae may help determine their possible role as an important biological factor a�ecting cyanobacterial blooms. Our review shows that the most economically important macroalgae species are found in the western part of the Baltic Sea. �is is due to the greatest richness and variety of species. Although it is worth noting that cosmopolitan species, such as Ulva, occur throughout the Baltic Sea, so in every region of this sea it is possible to utilize these organisms for commercial purposes. �us, in our opinion, there are su�- cient species resources in the waters of the Polish part of the Baltic Sea for com- mercial use. �e question that arises is whether the degree of pollution of the Baltic Sea waters allows for the use of registered algae for cosmetic, pharmaceutical, and food purposes. Unfortunately, the current literature does not provide unambiguous answers to this question. Lack of su�cient data on the amount of accumulated heavy metals and other anthropogenic pollutants in macroalgae tissues and the speci�c lim- its that must be met leave this question open. �e authors can only speculate that the use of algae that come from open water near the Danish straits, where the amount of pollution is less due to greater water exchange, is more favourable. Studies on the prac- tical use of Baltic macroalgae are still ongoing. �e results of previous studies are quite promising because Baltic macroalgae are easy to grow, relatively inexpensive, and less invasive, and these features are highly desirable in order to protect the environment and natural resources. Acknowledgements �e authors would like to thank the anonymous Reviewers for their valuable comments and suggestions to improve the quality of the paper. Con�ict of interest �e authors declare no con�ict of interest related to this article. References Bedoux, G., Hardouin, K., Burlot, A.S., Bourgougnon, N. (2014). Bioactive components from seaweeds: Cosmetic applications and future development. In: N. Bourgougnon (ed.), Advances in Botanical Research, 71, 345–378. Academic Press. https://doi.org/10.1016/B978-0-12-408062-1.00012-3 Berger, J., Schagerl, M. (2003). Allelopathic activity of Chara aspera. Hydrobiologia, 501(1–3), 109–115. https://doi.org/10.1023/A:1026263504260 Biłos, Ł., Golla, S., Patyna, A. (2016). Wykorzystanie glonów w rolnictwie i przemyśle spożywczym (�e use of algae in agriculture and the food industry). Przemysł Chemiczny, 95(9), 1797–1801. [In Polish] Buchholz, C.M., Krause, G., Buck, B.H. (2012). Seaweed and man. In: Wiencke C., Bischof K. (eds.), Sea- weed Biology, 471–493. Berlin, Heidelberg: Springer. https://doi.org/10.1007/978-3-642-28451-9_22 Deluga, W. (2018). �e role of ecological marketing in preserving the purity of wasters of the Baltic Sea. Folia Pomeranae Universitatis Technologiae Stetinensis. Oeconomica, 346(92), 5–16. https://doi. org/10.21005/oe.2018.92.3.01 [In Polish] B altic m acroalgae as a potential source for com m ercial applications – review 235 Dominguez, H., Loret, E.P. (2019). Ulva lactuca, a source of troubles and potential riches. Marine Drugs, 17(6), 357. https://doi.org/10.3390/md17060357 Duke, S.O., ScheÁer, B.E., Dayan, F.E. (2001). Allelochemicals as herbicides, in physiological aspects of allelopathy. In: M.J. Reigosa, N.P. Bonjoch (eds.), First European OECD Allelopathy Symposium, Vigo, Spain, pp. 47–59. Filipkowska, A., Lubecki, L., Szymczak-Zyla, M., Kowalewska, G., Zbikowski, R., Szefer, P. (2008). Utilisa- tion of macroalgae from the Sopot beach (Baltic Sea). Oceanologia, 50(2), 255–273. Filipkowska, A., Lubecki, L., Szymczak-Zyla, M., Lotocka, M., Kowalewska, G. (2009). Factors a�ecting the occurrence of algae on the Sopot beach (Baltic Sea). Oceanologia, 51(2), 233–262. Fitzgerald, C., Gallagher, E., Tasdemir, D., Hayes, M. (2011). Heart health peptides from macroalgae and their potential use in functional foods. Journal of Agricultural and Food Chemistry, 59(13), 6829– 6836. https://doi.org/10.1021/jf201114d Ghobrial, M.G., Nassr, H.S., Kamil, A.W. (2015). Bioactivity e�ect of two macrophyte extracts on growth performance of two bloom-forming cyanophytes. �e Egyptian Journal of Aquatic Research, 41(1), 69–81. https://doi.org/10.1016/j.ejar.2015.01.001 Granéli, E., Hansen, P.J. (2006). Allelopathy in harmful algae: a  mechanism to compete for resources? In: E. Granéli, J.T. Turner (eds.), Ecology of Harmful Algae, Ecological Studies. 189 Berlin Heidelberg, Germany: Springer-Verlag, p. 189–201. Gupta, S., Abu-Ghannam, N. (2011). Bioactive potential and possible health e�ects of edible brown sea- weeds. Trends in Food Science & Technology, 22(6), 315–326. https://doi.org/10.1016/j.tifs.2011.03.011 HELCOM (2012). Development of a  set of core indicators: interim report of the HELCOM CORESET project. Part B: Descriptions of the indicators. Baltic Sea Environment Proceedings, 129B, 1–219. Hilt, S., Gross, E.M. (2008). Can allelopathically active submerged macrophytes stabilise clear-water states in shallow lakes? Basic and Applied Ecology, 9(4), 422–432. https://doi.org/10.1016/j.baae.2007.04.003 Huppatz, J.L. (1996). Quantifying the inhibitor-target site interactions of photosystem II herbicides. Weed Science, 44, 743–748. https://doi.org/10.1017/S0043174500094625 Kandale, A., Meena, A.K., Rao, M.M., Panda, P., Mangal, A.K., Reddy, G., Babu, R. (2011). Marine algae: an introduction, food value and medicinal uses. Journal of Pharmacy Research, 4(1), 219–221. Kolb, N., Vallorani, L., Milanović, N., Stocchi, V. (2004). Evaluation of marine algae wakame (Undaria pinnati�da) and kombu (Laminaria digitata japonica) as food supplements. Food Technology and Biotechnology, 42(1), 57–61. McHugh, D.J. (2003). A guide to the seaweed industry. FAO Fish Tech Pap 441, Rome, Italy, pp. 105. McLachlan, J. (1985). Macroalgae (seaweeds): industrial resources and their utilization. In: J. Mclachlan (ed.), Biosalinity in Action: Bioproduction with Saline Water. Plant and Soil, 89(1/3), 137–157. Dor- drecht: Springer. Milledge, J.J., Nielsen, B.V., Bailey, D. (2015). High-value products from macroalgae: the potential uses of the invasive brown seaweed, Sargassum muticum. Reviews in Environmental Science and Bio/Tech- nology, 15(1), 67–88. Milledge, J.J., Smith, B., Dyer, P.W., Harvey, P. (2014). Macroalgae-derived biofuel: a  review of meth- ods of energy extraction from seaweed biomass. Energies, 7(11), 7194–7222. https://doi.org/10.3390/ en7117194 Mohy El Din, S.M. (2015). Utilization of seaweed extracts as bio-fertilizers to stimulate the growth of wheat seedlings. �e Egyptian Journal of Experimental Biology (Botany), 11(1), 31–39. Nyberg, E. (2007). Introduced marine macroalgae and habitat modi�ers – their ecological role and signi�- cant attributes. Göteborg University, pp. 61 [PhD �esis]. S yl w ia Ś liw iń sk a- W ilc ze w sk a, G ra cj an a B ud za łe k, Z uz an na K ow al sk a, M ar ek K lin , A da m L at ał a 236 Ohad, N., Hirschberg, J. (1990). A  similar structure of the herbicide binding site in photosystem II of plants and cyanobacteria is demonstrated by site speci�c mutagenesis of the psbA gene. Photosynthe- sis Research, 23, 73–79. https://doi.org/10.1007/BF00030065 Pakdel, F.M., Sim, L., Beardall, J., Davis, J. (2013). Allelopathic inhibition of microalgae by the freshwater stonewort, Chara australis, and a submerged angiosperm, Potamogeton crispus. Aquatic Botany, 110, 2–30. https://doi.org/10.1016/j.aquabot.2013.04.005 Roesijadi, G., Jones, S.B., Snowden-Swan, L.J., Zhu, Y. (2010). Macroalgae as a biomass feedstock: a pre- liminary analysis (No. PNNL-19944). Paci�c Northwest National Lab.(PNNL), Richland, WA (United States). https://doi.org/0.2172/1006310 Rybak, A.S. (2016). Freshwater population of Ulva �exuosa (Ulvaceae, Chlorophyta) as a food source for great pond snail: Lymnaea stagnalis (Mollusca, Lymnaeidae). Phycological Research, 64(4), 207–211. https://doi.org/10.1111/pre.12138 Rybak, A.S. (2018). Species of Ulva (Ulvophyceae, Chlorophyta) as indicators of salinity. Ecological Indi- cators, 85, 253–261. https://doi.org/10.1016/j.ecolind.2017.10.061 Rybak, A.S., Gąbka, M. (2018). �e in�uence of abiotic factors on the bloom-forming alga Ulva �exuosa (Ulvaceae, Chlorophyta): possibilities for the control of the green tides in freshwater ecosystems. Journal of Applied Phycology, 30(2), 1405–1416. https://doi.org/10.1007/s10811-017-1301-5 Saniewski, M. (2013). Roślinność bentosowa jako indykator stanu środowiska Morza Bałtyckiego (Benthic vegetation as an indicator of the state of the Baltic Sea environment). Polish Hyperbaric Research, 1(42), 83–102. [In Polish] Schroeder, G., Messyasz, B., Łęska, B., Fabrowska, J., Pikosz, M., Rybak, A.S. (2013). Biomasa alg słod- kowodnych surowcem dla przemysłu i rolnictwa (Biomass of freshwater algae as raw material for the industry and agriculture). Przemysł Chemiczny, 92(7), 1380–1384. [In Polish] Snoeijs-Leijonmalm, P., Schubert, H., Radziejewska, T. (2017). Biological oceanography of the Baltic Sea. Switzerland: Springer Science & Business Media. Suganya, T., Varman, M., Masjuki, H.H., Renganathan, S. (2016). Macroalgae and microalgae as a  po- tential source for commercial applications along with biofuels production: a  biore�nery approach. Renewable and Sustainable Energy Reviews, 55, 909–941. https://doi.org/10.1016/j.rser.2015.11.026 Tang, Y.Z., Gobler, C.J. (2011). �e green macroalga, Ulva lactuca, inhibits the growth of seven common harmful algal bloom species via allelopathy. Harmful Algae, 10(5), 480–488. https://doi.org/10.1016/j. hal.2011.03.003 van Donk, E., van de Bund, W.J. (2002). Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquatic Botany, 72, 261–274. https://doi.org/10.1016/S0304-3770(01)00205-4 Wærn, M. (1965). A vista on the marine vegetation. Acta Phytogeographica Suecica, 50, 13–27. Wang, H.M.D., Chen, C.C., Huynh, P., Chang, J.S. (2014). Exploring the potential of using algae in cos- metics. Bioresource Technology, 184, 355–362. https://doi.org/10.1016/j.biortech.2014.12.001 Wang, R., Xiao, H., Zhang, P., Qu, L., Cai, H., Tang, X., (2007). Allelopathic e�ects of Ulva pertusa, Cor- allina pilulifera and Sargassum thunbergii on the growth of the dino�agellates Heterosigma akashiwo and Alexandrium tamarense. Journal of Applied Phycology, 19(2), 109–121. https://doi.org/10.1007/ s10811-006-9117-18 Wells, M.L., Potin, P., Craigie, J.S., Raven, J.A., Merchant, S.S., Helliwell, K.E., Smith, A.G., Camire, M.E., Brawley, S.H. (2017). Algae as nutritional and functional food sources: revisiting our understanding. Journal of Applied Phycology, 29(2), 949–982. https://doi.org/10.1007/s10811-016-0974-5 Żbikowski, R., Szefer, P., Latała, A. (2006). Distribution and relationships between selected chemical el- ements in green alga Enteromorpha sp. from the southern Baltic. Environmental Pollution, 143(3), 435–448. https://doi.org/10.1016/j.envpol.2005.12.007 B altic m acroalgae as a potential source for com m ercial applications – review 237 Żbikowski, R., Szefer, P., Latała, A. (2007). Comparison of green algae Cladophora sp. and Enteromorpha sp. as potential biomonitors of chemical elements in the southern Baltic. Science of the Total Environ- ment, 387(1–3), 320–332. https://doi.org/10.1016/j.scitotenv.2007.07.017 Złoch, I., Śliwińska-Wilczewska, S., Kucharska, M., Kozłowska, W. (2018). Allelopathic e�ects of Chara species (C. aspera, C. baltica, and C. canescens) on the bloom-forming picocyanobacterium Syn- echococcus sp. Environmental Science and Pollution Research, 25(36), 36403–36411. https://doi. org/10.1007/s11356-018-3579-5 Bałtyckie makroglony jako potencjalne źródło zastosowań komercyjnych Streszczenie Morze Bałtyckie jest wyjątkowym ekosystemem wodnym, charakteryzującym się wyraźnymi zmianami w środowisku, szczególnie w odniesieniu do zasolenia i klimatu. Jest to także miejsce występowania mor- skich i słodkowodnych organizmów roślinnych, które od stuleci fascynują naukowców. Niewiele jest jednak prac prezentujących bałtyckie glony makroskopowe, jako potencjalne źródło dla zastosowań komercyjnych. Celem niniejszego opracowania było przedstawienie bałtyckich makroglonów, jako źródła zasobów prze- mysłowych. W  przeglądzie uwzględniono, m.in. potencjał wykorzystania tych organizmów w  przemyśle kosmetycznym i medycznym, w tym najważniejsze składniki, które czynią je cennym produktem spożyw- czym. Zwrócono także uwagę na ich rosnącą popularność i potencjalne wykorzystanie w przyszłości, np. jako biopaliwa, nawozy naturalne lub składniki oczyszczalni ścieków. Przedstawiono także możliwość wy- korzystania makroglonów jako biologicznego czynnika, ograniczającego występowanie masowych zakwi- tów sinic w Morzu Bałtyckim. Key words: Baltic macroalgae, Baltic Sea, bioactive compounds, biomass, industrial resources Received: [2020.02.27] Accepted: [2020.06.04]