Critical Reviews in Food Science and Nutrition

ISSN: 1040-8398 (Print) 1549-7852 (Online) Journal homepage: http://www.tandfonline.com/loi/bfsn20

Algae in food- a general review

Sylwia Ścieszka & Elżbieta Klewicka

To cite this article: Sylwia Ścieszka & Elżbieta Klewicka (2018): Algae in food- a general review,
Critical Reviews in Food Science and Nutrition, DOI: 10.1080/10408398.2018.1496319

To link to this article: https://doi.org/10.1080/10408398.2018.1496319

Accepted author version posted online: 12

Jul 2018.

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 Algae in food- a general review
Sylwia Ścieszka, Elżbieta Klewicka
Institute of Fermentation Technology and Microbiology, Faculty of Biotechnology and Food
Science, Lodz University of Technology, Łódź, Poland
*Correspondence: Sylwia Ścieszka, Email: sylwia.scieszka@edu.p.lodz.pl
Abstract

Algae are common all over the Earth. Due to their rich chemical composition and
content of bioactive substances they have been used in many fields of industry. Their gelling,

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thickening and stabilizing properties have led to the development of such products as agar,
alginate and carrageenan. Moreover, algae are used in the food industry as food supplements

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and an addition to functional food. Algae are also added to meat products, such as pasty,
steaks, frankfurters and sausages, as well as to fish, fish products, and oils, to improve their

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quality. Cereal-based products, such as pasta, flour and bread, are another group of products
enriched with algae. Due to their properties algae may also be used for construction of
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fermented functional food. Fermented products containing algae are, most of all, dairy
products, such as cheese, cream, milk deserts, yoghurt, cottage cheese, and processed cheese.
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Combination of fermented products offering a high content of lactic acid bacteria with algae
possessing biologically active metabolites of natural origin allows not only to compose
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products with a high content of nutrients, but also to create a brand new segment of
fermented food.
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Keywords: algae in the food industry, fermented food, lactic acid bacteria, functional food
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Characteristics of algae

Algae are some of the most common organisms inhabiting the Earth. They are able to
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grow even in extreme conditions. They are present in terrestrial and aqueous environments,
and they grow in both fresh and salt waters (Singh and Sharma 2012). It is estimated that the
number of known species of algae ranges between 30,000 and 1 million. According to Guiry
(2012) the number of described species is estimated at even 350 million, and the Internet
database AlgaeBase (http://www.algaebase.org) describes over 150,000 species.
The morphology and size of algae are highly variable. There are unicellular species
measuring 3-10 μm, and huge water algae reaching as much as 70 m in length, and growing

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by 50 cm a day (El Gamal 2010). They are typical Eucaryotes with a well-developed nucleus,
a cell wall, a chloroplast containing chlorophyll and other pigments, and a flagella (Singh and
Sharma 2012). Microalgae are able to carry out photosynthesis – the process of
transformation of solar energy into chemical energy with absorption of carbon dioxide. Those
organisms are ideal for biochemical studies, as their growth cycle is short. Because of that
they may be used for direct reaction to phytohormones on a cellular level, as the reception of
the signal molecule and the response/biochemical reaction occur in the same cell, under
controlled conditions (Bajguz and Piotrowska-Niczyporuk 2013).
Microalgae are traditionally classified according to their cytological and
morphological aspects, type of reserve metabolites, components of the cell wall and pigments.

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Marine diatoms are golden-brown because of their content of xanthophyll pigments, blue-

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green algae contain chlorophyll a, and blue phycocyanins. Macroalgae are classified based on

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their chemical and morphological characteristics, in particular, the presence of specific
pigments. They are divided into brown algae (Phaeophyceae), where the brown or yellow-

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brown colour is the result of the presence of fucoxanthin, red algae (Rhodophyceae), with
dominating phycoerythrin and phycocyanin, and green algae (Chlorophyceae) containing
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chlorophyll a and chlorophyll b (Domínguez 2013).

It was demonstrated that algae produce a broad spectrum of bioactive secondary

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metabolites and valuable bioactive substances, including: proteins, carbohydrates, lipids,

polyunsaturated fatty acids (PUFA), including omega-3 fatty acids, polysaccharides,
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polyphenols, steroles and pigments (chlorophyll, carotenoids, phycobilines) (Borowitzka

2013; Charoensiddhi et al. 2018; Mohsenpour and Willoughby 2013). Interestingly, the
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quality of proteins from algae was found superior to other plant sources, including wheat, rice
or beans, but inferior to animal proteins, such as milk or meat (Mendes, Lopes da Silva and
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Reis 2007). Moreover, algae are a good source of food fibre, and they contain vitamins: A,
B1, B12, C, D, and E, riboflavin, niacin, pantothenic acid and folic acid (Gupta and Abu-
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Ghannam 2011). Algae are a rich source of elements: calcium, sodium, magnesium,
phosphorus, potassium, iron, zinc, and iodine (Cofrades, Serdaroğlu and Jiménez-Colmenero
2013). They are also able to absorb heavy metals, such as: cadmium, zinc, lead, nickel and
copper (Suresh and Ravishankar 2004).
Studies of algae biological activity demonstrated that they possess antioxidant,
antibacterial, antiviral, and also antifungal properties (Table 1). They also demonstrate the
following effects: prebiotic, neuroprotective, anti-inflammatory, immunomodulating,

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antidiabetic, anticoagulant, and anticancer (Charoensiddhi et al. 2018). Dietary supplement of
food fibre from algae favours growth and maintenance of the beneficial intestinal flora,
significantly increases the volume of stool, and reduces the risk of colorectal cancer. It was
also found that regular consumption of marine algae was associated with exceptionally low
incidence of breast cancer (because of a high availability of dietary iodine) (Gupta and Abu-
Ghannam 2011).

The application of algae

Algae have been used in many industries (Fig. 1). They are used in the chemical
industry, among others as a source of bactericidal substances, and also in the cosmetic

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industry. Creams and cosmetics made of algae supply nutrients to the skin, increase the rate of

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epidermal regeneration, reduce scars, moisturize, rejuvenate and restore firmness. Considering

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the increasing number of pathogenic bacteria resistant to antibiotics, finding new drugs which
will fight with those pathogens is necessary. Bioactive compounds from algae may constitute

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an alternative for many chemotherapeutics (El Gamal 2010; Al-Saif et al. 2014; Ariede et al.
2017). Algae remove organic pollutants, heavy metals and pathogens (Muñoz and Guieysse
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2006), and for that reason they are used for cleaning the environment (Suresh and
Ravishankar 2004), bioremediation (Kalin, Wheeler, and Meinrath 2005; Mallick 2002), and
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as a bioformula for removal of nitrogen (Vaishampayan et al. 2001). Moreover, the symbiotic
system of algae and bacteria constitutes an ecological basis for natural treatment of running
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waters (Ji 2018). There are also numerous studies indicating the possible use of algae for
production of biofuels. Micoalgae are characterized by a rapid increase of biomass, and
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absorption of significant amounts of carbon dioxide. Due to those properties, algae may be
used as a renewable source of energy. The variety of biofuels obtained from algae depends on
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which components of their cells will be used. Anaerobic fermentation of algae biomass allows
production of biomethane, oil from microalgae may be used as a biodiesel, and bioethanol is
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obtained after saccharidification and fermentation of algae (Brennan and Owende 2010; Chisti
2007; Chen et al. 2011). The use of microalgae for the production of fuel is not a new idea
(Nagle and Lemke 1990). However, only today, and because of the increasing price of oil,
climate change and global warming concerns associated with combustion of fossil fuels, the
use of algae for production of biofuels is a seriously considered solution (El Arroussi et al.
2017; Zhu et al. 2017). Algae are also used in animal feed industry. Already in the 1970s they
were introduced as an addition to animal feed. It is a good method for improvement of animal

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health, and thus also improvement of the quality of meat and meat products. He, Hollwich,
and Rambeck (2002) fed pigs with a feed containing Laminaria digitata and demonstrated
that supplementation with algae may lead to increased iodine content in muscles, adipose
tissue, the heart, the liver and kidneys, and may increase the daily body weight gain by 10%.
Another example of algae used in production of animal feed and fertilisers is the case of
brown algae Ecklonia radiata (Charoensiddhi et al. 2018). For improvement of the quality of
meat, algae-containing supplements were also given to lambs. Studies demonstrated that such
supplementation had effect mostly in relation to the main groups of fatty acids in muscles.
The content of eicosapentaenoic acid (EPA) and of docosahexaenoic acid (DHA) in lamb
meat could be doubled by supplementation of animals’ diet with 1.8% of algae. The increased

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content of EPA + DHA in muscles has led to improved oxidation of lipids, but with no effect

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on the colour of meat (Ponnampalam et al. 2016). Studies on lambs were also conducted by

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Hopkins et al. (2014). They confirmed that supplementation with algae increased the level of
omega-3 fatty acids (EPA + DHA), and therefore improved the quality of lamb meat. Algae-

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containing supplements are also successfully used in feeds for aquatic animals. Moreover,
algae are commonly used in the food industry (Pina-Pérez et al. 2017). They are used for
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production of functional food and dietary supplements (Borowitzka 2013).
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Algae in the food industry

Algae have been used as food since ancient times. In the Far East and Asia the
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tradition of eating algae is a long-standing one; whereas in Western countries the interest in
algae-based products is quite recent. Algae are very popular among vegetarians, who use them
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as starters, additions and main courses (Cofrades, Serdaroğlu and Jiménez-Colmenero 2013).
In Europe, the interest in algae was for a long time focused on the production of gelling,
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thickening and stabilising substances to be used in the food industry (Pina-Pérez et al. 2017).
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Agar, alginate and carrageenan

The main polysaccharides obtained from marine algae are: alginate, agar, and
carrageenan. Those hydrocolloids are commonly used in food, pharmaceutical industries, and
in biotechnology, among others due to their ability to form highly viscous solutions and gels.
Agar and carrageenan form thermoreversible gels. However, agar melts at a higher
temperature than carrageenan (Hernández-Carmona, Freile-Pelegrín, and Hernández-Garibay
2013).

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 Alginate has the ability to form thermally stable gels with selected divalent metals. It
forms parts of the cell wall and the intercellular matrix of all brown marine algae. In seaweed,
alginate provides elasticity and mechanical strength required to survive in the sea. Due to its
strong hydrophilic properties and the ability to bind water, it prevents algae from drying out
during a low tide. The main commercial sources of alginate are marine brown algae:
Laminaria, Ascophyllum, and Lessonia (Hernández-Carmona, Freile-Pelegrín, and
Hernández-Garibay 2013). Alginate is a linear polysaccharide composed of residues of β-D-
mannuronic acid (M) (Fig. 2a) and α-L-guluronic acid (G) (Fig. 2b), arranged in various
proportions and sequences. They may be present as uniform blocks MM or GG, or alternately
as MG. The composition and monomer sequence, as well as the source of algae have a great

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influence on the gelling characteristics of alginate. Alginate with a high content of G fractions

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offers stronger gelling properties, while that with a higher content of M fractions is more

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viscous (Murillo-Álvarez and Hernández-Carmona 2007). Alginate is commonly used in
many fields of industry, for example as a component of material for dental impressions, a

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thickening agent for pigment pastes used for printing textiles, material for rod welding, a pill
disinfecting agent and a component of absorbable bandages that do not to be removed. It is
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also used in the food industry for production of gels or as a viscosity regulator. It enhances the
appearance of dairy products and canned food, supports water retention, thus improving the
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appearance of bakery products, and ensures a smooth texture and even dehydration of frozen
food. Alginate is also used as a stabiliser of beer foam (Hernández-Carmona, Freile-Pelegrín,
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and Hernández-Garibay 2013).

Agar is a structural polysaccharide of marine algae. It is composed of strongly gelling

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agarose, and non-gelling agaropectin. Agarose is made of agarobiose units, that is D-galactose
moieties bound with the β-1,4-glycosidic bond with 3,6-anhydro-L-galactose. The structure of
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agaropectin is more complex. Its basic component is a D-galactose chain bound with β-1,3-
glycosidic bonds, in which part of sugar units are substituted in the C-6 position with sulfone
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groups (Fig. 3) (Kączkowski 2017). Agar is obtained from red algae (Rhodophyta). The
biological function of agar is to provide an elastic structure that is resistant to the tensions of
tides and waves. Mostly Gelidium and Gracilaria algae are used for production of agar. One
of the most unusual properties of agar gels is their thermoreversibility. Agar is a strongly
gelling hydrocolloid, that – depending on the species – melts at 85°C or higher temperature,
but after cooling down becomes a colourless, odourless gel. The big difference between
gelling and melting points is characteristic only for agar. Approximately 90% of produced

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agar is used in the food industry, and the remaining 10% is used for the purposes of
bacteriology and biotechnology (Hernández-Carmona, Freile-Pelegrín, and Hernández-
Garibay 2013). In laboratories, agar is used as a thickening component of the mediums for
culture of bacteria tissue, cells, filamentous fungi and yeast. In the food industry, the
application of agar is based mostly on its ability to form gels offering some unique properties.
Agar is used as a vegetarian gelatine with a high fibre content. It is used in fruit jellies and
canned meat, but also for stuffing pastries and for glazing that may be placed before baking,
as it does not melt in the oven (Bixler and Porse 2011).

Carrageenan is an ionic polysaccharide made of galactose and sulphate groups

distributed over the polymer chain. It is extracted from various red marine algae, where it is a

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structural compound. Some carrageenans are soluble in cold water. In that case, they have
only viscosifying properties. Other are soluble in hot water and they are able to form

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thermoreversible gel with potassium or calcium ions. The original raw material for production
of carrageenan is Chondrus crispus, commonly referred to as the "Irish moss". However, with

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increasing demand and development of new applications, finding some new sources of the
substance become necessary (Hernández-Carmona, Freile-Pelegrín, and Hernández-Garibay
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2013). Mostly Kappaphycus alvarezii and Eucheuma denticulatum algae are used for
production of carrageenan. Different species produce different types of carrageenan. The main
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commercial types are: Kappa, Iota and Lambda (Fig. 4). Carrageenan is used in the
pharmaceutical and food industries. Due to its exceptional ability to bind milk proteins, it is
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used in dairy products. Even at a very low concentration, carrageenan is able to maintain milk
solids in suspension, thus stabilising them. That prevents separation of whey in cheese
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products, and facilitates the formation of crystals in milk ice cream, resulting in a smoother
texture. For that reason it is used in the production of cheese, cocoa and chocolate milk
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products. Another field of application of carrageenan (particularly that obtained from

Eucheuma) is the meat industry. Due to its water retention properties it is used in the
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production of ham, hamburgers, seafood and poultry products. Carrageenan is also used in
aqueous gels, such as jelly-candies, fruit gels, juices, and marmalade (Bixler and Porse 2011;
Hernández-Carmona, Freile-Pelegrín, and Hernández-Garibay 2013).

Supplements

Due to their nutritional value, algae are commonly used as dietary supplements. The
best known ones are Spirulina and Chlorella. Including algae in one’s diet supplements it

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with wholesome proteins. Algae offer detoxification of the organism, protect the gastric
mucosa and support digestion. Algae have also a favourable effect on memory and
concentration, support treatment of diabetes, rheumatic diseases, and arterial hypertension.
They also counteract viral, fungal and bacterial infections.

Algae-containing food

In food for human consumption algae have been mostly introduced to meat and bakery
products. The addition of algae, including Enteromorpha, Himanthalia elongata, Undaria
pinnatifida and Porphyra umbilicalis resulted in changes in the antioxidative potential of meat
and cereal-based products (Gupta and Abu-Ghannam 2011).

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Meat and meat products are valuable sources of proteins and vitamins, but they

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contain an insufficient amount of food fibre and an excessive amount of sodium that may be

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harmful for humans. Therefore, the addition of algae as a functional component may help
overcome technological problems associated with meat products with a low salt content,

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including fat and water binding properties. Some attempts were made to develop model
systems of meat emulsions with low fat and salt content, with an addition of various bioactive
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compounds from marine algae. Edible algae Sea Spaghetti (H. elongata), Wakame (U.
pinnatifida) and Nori (P. umbilicalis) were added to meat, which resulted in increased levels
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of K, Ca, Mg, and Mn. Moreover, the presence of Nori algae increased the levels of serine,
glycine, alanine, valine, tyrosine, phenylalanine, and arginine. The addition of Sea Spaghetti
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increased the content of sulphur amino acids by 20%. Meat enrichment with algae supplied
soluble polyphenolic compounds, which increased the antioxidative potential of the whole
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system (López-López et al. 2009a). The effect of addition of U. pinnatifida (Wakame algae)
on the properties of beef patties with a low content of salt (0.5%) and a low content of fat
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(<10%) when stored in a freezer was also studied. The addition of algae caused less thawing,
and reduced loss on cooking, as well as improved the product's consistence by making it
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softer (López-López et al. 2010). Sasaki et al. (2008) studied the effect of fucoxanthin, the
main carotenoid pigment in U. pinnatifida, on peroxidation of lipids and colour of meat in
ground chicken breast meat. It was found that fucoxanthin improved the appearance and
prolonged the period of usability of chicken meat and chicken meat products. Marine algae
Sea Spaghetti were introduced to poultry steaks, which resulted in less loss on cooking. There
was also an increased number of lactic acid bacteria, as well as increased levels of tyramine
and spermidine (Cofrades et al. 2011). Algae H. elongata were added to frankfurters (López-

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López et al. 2009b), and brown algae Lamina japonica (powdered) to breakfast sausages
(Kim et al. 2010). Attempts were also made to introduce raw algae and create innovative meat
products, such as sausages and hamburgers. However, some aspects, including quality and
organoleptic acceptance, still require more detailed analysis (Pina-Pérez et al. 2017). Algae
Fucus vesiculosus were added to fish and fish products (Wang et al. 2010). Senthil, Mamatha,
and Mahadevaswamy (2005) used Eucheuma as an ingredient of a fish cutlet. The researchers
found that the addition of up to 10% algae had no negative effect on appearance, texture and
acceptance. Also oils are enriched with algae. The extract of marine red algae Grateloupia
filicina was added to linoleic acid and fish oil. The addition constituted 0.01%, 0.03%, and
0.05% of those products. Studies demonstrated that the addition inhibited oxidation of linoleic
acid and fish oil at the level of 0.05% (Athukorala et al. 2003). Another study on fish oil and

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linoleic acid was carried out by Siriwardhana et al. (2004) who analysed the inhibitory effect
of the methanolic extract from Hizikia fusiformis on peroxidation of lipids. The algae contain

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antioxidants resistant to heat and UV radiation. Results showed that antioxidants from H.

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fusiformis may be useful in prevention of oxidative changes in consumable oils.

Cereal-based products are commonly accepted, among others due to the easy
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preparation process, long usefulness for consumption and low cost. However, their nutritional
and health properties could be improved. That objective may be achieved by addition of
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algae, as they are rich in bioactive substances. Pasta is one of the most versatile cereal-based
product. Dietitians find it a highly digestible source of complex hydrocarbons, B group
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vitamins and iron. Unfortunately it is also characterized by a low content of protein and
essential amino acids. For that reason the introduction of high-protein additives, such as algae,
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will increase the quality of pasta. Studies of edible algae Wakame (U. pinnatifida), rich in
fucoxanthin were conducted that concluded that pasta with 10% of algae was acceptable for
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the senses. It had a mild taste of algae, but it was still close to the control sample. Moreover,
the presence of algae supported the interaction between starch granules and the protein
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matrix, which resulted in higher quality of pasta (Prabhasankar et al. 2009b). Pasta containing
Indian brown algae Sargassum marginatum was also developed. Supplementation with algae
improved its bio-functionality and quality (Prabhasankar, Ganesan, and Bhaskar 2009a). Also
Chinese fresh egg noodles was created with an addition of green algae Monostroma nitidum
(Chang and Wu 2008).
Algae-based flour and lipid powders are currently very widely discussed, as they are an
element of modern cuisine, also appreciated in the vegan market, where they are used instead

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of eggs (Pina-Pérez et al. 2017). Bread is another perfect cereal-based product that may be a
carrier for various bioactive components, including algae. The quality of bread was improved
by addition of both green algae Ulva lactuca, and 2.5% of powdered Laminaria algae
(Cofrades, Serdaroğlu and Jiménez-Colmenero 2013). Functional bread with the addition of
algae was also created (Bang et al. 2009). Studies confirmed that it was possible to add
Ascophyllum nodosum algae to basic food, such as bread, at the level of 4% per 400 g of
wholemeal loaf. Consumption of that bread for breakfast led to a significant decrease (16.4%)
of energy consumption during a test meal 4 hours later (Hall et al. 2012). Goñi, Valdivieso,
and Garcia-Alonso 2000 assessed the effect of Nori algae (Porphyra tenera) on the glycemic
postprandial response after the consumption of white bread. The study demonstrated that
algae might be used not only as food, but also as a component which supplies the body with

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high amounts of soluble food fibre. Supplementation with algae decreased the rate of starch
hydrolysis, and also decreased the glycemic response to white bread in healthy volunteers

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from 100% to 68%.

Fermented food with the addition of algae us

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Production of fermented food, such as milk, meat, vegetables and cereals, involves
participation of lactic acid bacteria (LAB). From the industrial point of view they are very
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important microorganisms (McKay and Baldwin 1990). They provide an effective method of
conservation of fermented food, affect its taste, texture and often also the nutritional value
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(Neves et al. 2005). Consumption of LAB-rich products is associated with numerous health
benefits. They may be effective in fighting food allergies (Adolfsson, Meydani, and Russell
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2004; Carr, Chill, and Maida 2002). They are used for alleviation of atopic dermatitis, Crohn's
disease, ulcerative colitis, rheumatoid arthritis and acute gastroenteritis caused by rotaviruses
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(Carr, Chill, and Maida 2002). LAB demonstrate anticancer, immunostimulating effect, and
also reduce blood cholesterol level (Welman and Maddox 2003). They are also used in the
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cases of lactose intolerance, for treatment of constipation, enteritis and infection with
Helicobacter pylori. Moreover, they have an antagonist effect for intestinal pathogens. For
that reason they are used as a support treatment of diarrhoea (Adolfsson, Meydani, and
Russell 2004).
Lactic acid bacteria are a variable group of microorganisms which carry out anaerobic
fermentation, the main product of which is lactic acid. They are able to metabolise glucose via
three catabolic pathways. There is homofermentation, transformation of sugar along the
Embden-Meyerhof-Parnas (EMP) pathway, heterofermentation, decomposition of glucose
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along the pentose phosphoketolase pathway, and the mixed fermentation occurring in the case
of limited availability of glucose, at increased pH, or at a lowered temperature (Felis and Pot
2014; Hofvendahl and Hahn-Hägerdal 2000; Wee, Kim, and Ryu 2006; Yun, Wee, and Ryu
2003)
Considering the saccharides fermentation method Lactobacillus genus bacteria were divided
into three groups (Table 2): obligatively homofermentative – degrading hexoses to lactic acid,
and unable to ferment pentoses or gluconate; obligatively heterofermentative – that besides
lactic acid produce also acetic acid, ethanol and carbon dioxide; and facultatively
heterofermentative – combining properties of homofermentative and heterofermentative
bacteria, metabolising hexoses using the EMP pathway, and metabolising pentoses along with

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some other substrates using the pentose phosphoketolase pathway (Libudzisz 2008;

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Narayanan, Roychoudhury, and Srivastava 2004; Zaremba and Borowski 1997).

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Studies indicate that fermented products enriched with algae are dairy products. Dairy
products contain high levels of nutrients providing numerous components, such as protein,

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calcium, potassium, phosphorus, magnesium, zinc, vitamins A, D, and B12, and riboflavin.
They are also the main source of nutritional calcium. However, in cheese calcium is
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immobilised in casein, and people lacking enzymes able to digest casein cannot absorb
calcium from those products. Therefore, the addition of calcium-rich algae may increase the
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level of the element in dairy products, and help in treatment of hypocalcemia (Cofrades,
Serdaroğlu, and Jiménez-Colmenero 2013). Dairy products, particularly cheese, were
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enriched with various kinds of algae, to improve their nutritional value. Combining both types
of food allows to create of healthy products offering a rich content of various nutrients.
Brown algae Laminaria were added to smoked cheese, milk deserts and yoghurt. In order to
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make dairy products a source of iodine, Laminaria saccharina algae from the North Sea were
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introduced to cottage cheese and fresh cheese (Cofrades, Serdaroğlu and Jiménez-Colmenero
2013). Results obtained by Lalic and Berkovic (2005) demonstrated that Wakame (U.
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pinnatifida) and Kombu (L. japonica) algae increase the quality of cheese during storage. The
best influence on the texture quality was observed for industrial and home cottage cheese
containing 9% of Wakame algae. Green algae Chlorella were added at a concentration of 0.5-
1.0% (w/w) to processed cheese (Jeon 2006), and also the effect of powdered Chlorella on
growth of lactic acid bacteria, maturation rate and organoleptic properties of the Appenzeller
sea was studied (Heo et al. 2006). Algae were added at a concentration of 0-2%. The count of
LAB was higher in the algae-enriched cheese compared to the control samples. Studies
demonstrated that the appropriate addition of Chlorella to the Appenzeller cheese of

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satisfactory quality was 0.5% (Heo et al. 2006). Uchida et al. 2017 developed high-salt
content seaweed sauce by lactic acid fermentation. They prepared two sauces from nori
(Pyropia yezoensis), which were rich in total nitrogen compounds and potassium. Therefore
they had a unique components, such as free amino acid composition. These results suggest
that that the fermented sauce prepared from seaweeds has a high potential as a novel
nutritional source for humans. Moreover, Uchida et al. 2018 obtained fermented sauce from
low-quality nori (dried and fresh fronds of Pyropia yezoensis), which can be commercially
used as a component of low allergen-risk sauce products after mixing with other spices
without wheat or soy ingredients. Furthermore, Uchida et al. 2014a conducted isolation and
characterization of halophilic lactic acid bacteria that can act as a starter in a Nori (Porphyra

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yezoensis)‐sauce culture. Another example of the use of algae is storage of cheese in film

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made of red algae, containing 1% of the grapefruit seed extract. After 15 days of storage the

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count of E. coli O157: H7 was reduced by 1.21 log CFU/g, and the population of L.
monocytogenes was reduced by 0.85 log CFU/g, compared to control samples. Those results

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suggest that the film made of red algae with addition of the grapefruit extract is a useful
material for food packaging, providing a longer shelf life of, e.g. cheese (Shin et al. 2012).
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Fermentation of algae
Lactic acid fermentation of seaweeds was observed for the first time in 1998 and
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published in 2004 on a cellulase-treated culture of Ulva spp. (Chlorophyta) (Uchida, and

Murata 2004). Results obtained by Uchida, Murata and Ishikawa 2007 demonstrated that
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addition of yeast is not necessary for carring out lactic acid fermentation. They observed that
Lactobacillus plantarum, Lactobacillus casei, Lactobacillus rhamnosus and Lactobacillus
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brevis are suitable species for performing fermentation of algae (Undaria pinnatifida)
(depending on the used of Lactobacillus strains and fermentation conditions). Moreover,
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ethanol fermentation on seagrass seed Zostera marina by yeast was studied. Fermented
seagrass seed products with such a high ethanol concentration can enable the development of
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a distillery industry (Uchida et al. 2014b). Recent research Suraiya et al. 2018 shown fungal
fermentation of seaweed Saccharina japonica and Undaria pinnatifida to increase their
biofunctional properties. These brown algae were fermented by red molds: Monascus
purpureus and Monascus kaoliang. Results shown that the phenolic, flavonoid, antidiabetic,
antioxidant and antilipase activity in Monascus-fermented seaweed extracts were higher than
those of unfermented seaweed. Moreover, fermented extracts exhibited higher DNA
protection and the absence of any toxic effect on intestinal epithelial Caco-2 cells. Therefore,

11
fermented seaweed extracts may be useful as “therapeutic diets” for patients suffering from
oxidative stress, hyperglycemia or hyperlipidemia.

Summary

The increasing incidence of diseases caused by intensive lifestyle and the growing
importance of diet in human life result in the need for natural and beneficial nutritional
products. The value of food is based not only on presence of essential nutrients, but also on
the availability of other bioactive compounds that influence health and facilitate homeostasis
of the human organism. Algae are a great source of biologically active compounds, and may
be used for development of functional food. They are a rich source of natural antioxidants and
antimicrobials. Addition of their natural extracts not only improves the quality of food

t
ip
products, but also limits the use of chemical preservatives and brings numerous health
benefits. Despite the availability of extensive literature regarding antimicrobial properties of

cr
algae, only few studies have focused so far on the practical use of fermented food. Therefore,

us
the field still constitutes a challenge for the scientists who work to take a full advantage of
potential of algae. Both fermented food and algae offer a high nutritional value. Combination
an
of those two will create a product rich in all essential nutrients that are necessary for correct
and healthy functioning of the organism. Considering the need for constant innovations and
M

for meeting the changing tastes of consumers, algae offer some interesting possibilities for
creation of novel food products. Studies on the use of algae as a component of fermented food
will open new horizons for the food industry, offering nutritional and health benefits based on
ed

the use of this abundant, yet currently underestimated, natural resource. Developments in this
field will bring some new, innovative functional products that will meet the expectations of
pt

consumers and fill the gap in the food industry.

ce
Ac

12
1. Adolfsson, O., S. N. Meydani, and R. M. Russell. 2004. Yogurt and gut function. Am.
J. Clin. Nutr. 80 (2):245–256. doi.org/10.1093/ajcn/80.2.245.
2. Afify, A. E.-M. M. R., H. H. Abd El Baky, G. S. El Baroty, F. K. El Baz, and S. A.
Murad. 2017. Antioxidant activity of protein hydrolysates derived from blue-green
algae spirulina platensis extracted with three different methods and treated with
enzymes. Bioscience Res. 14 (3):485-497.
3. Alencar, D. B., S. R. Silva, K. M. Pires-Cavalcante, R. L. Lima, F. N. Pereira Júnior,
M. B. Sousa, F. A. Viana, C. S. Nagano, K. S. Nascimento, B. S. Cavada, A. H.
Sampaio, and S. Saker-Sampaio. 2014. Antioxidant potential and cytotoxic activity of
two red seaweed species, Amansia multifida and Meristiella echinocarpa, from the
coast of Northeastern Brazil. An. Acad. Bras. Ciênc. 86 (1):251-263.
doi.org/10.1590/0001-37652014116312.
4. Al-Saif, S. S. A.-I., N. Abdel-Raouf, H. A. El-Wazanani, and I. A. Aref. 2014.
Antibacterial substances from marine algae isolated from Jeddah coast of Red sea,
Saudi Arabia, Saudi J. Biol. Sci. 21 (1):57-64. doi.org/10.1016/j.sjbs.2013.06.001.

t
5. Ariede, M. B., T. M. Candido, A. L. M. Jacome, M. V. R. Velasco, J. C. M. de

ip
Carvalho, and A. R. Baby. 2017. Cosmetic attributes of algae- A review. Algal Res.
25:483-487. doi.org/10.1016/j.algal.2017.05.019.

cr
6. Athukorala, Y., K.-W. Lee, F. Shahidi, M. S. Heu, H.-T. Kim, J.-S. Lee, and Y.-J.
Jeon. 2003. Antioxidant efficacy of extracts of an edible red alga (Grateloupia
filicina) in linoleic acid and fish oil. J. Food Lipids. 10 (4):313-327.
doi.org/10.1111/j.1745-4522.2003.tb00024.x.

us
7. Bajguz, A., and A. Piotrowska-Niczyporuk. 2013. Synergistic effect of auxins and
brassinosteroids on the growth and regulation of metabolite content in the green alga
an
Chlorella vulgaris (Trebouxiophyceae). Plant Physiol. Biochem. 71:290-297.
doi.org/10.1016/j.plaphy.2013.08.003.
8. Bang, S.-J., S.-H. Choi, I.-S. Shin, and S.-M. Kim. 2009. Development of functional
M

bread with sea tangle single cell detritus (SCD). J. Korean Soc. Food Sci. Nutr. 38
(10):1430–1437. doi.org/10.3746/jkfn.2009.38.10.1430.
9. Bixler, H. J. and H. Porse. 2011. A decade of change in the seaweed hydrocolloids
ed

industry. J. Appl. Phycol. 23 (3):321–335. doi.org/10.1007/s10811-010-9529-3.

10. Borowitzka, M. A. 2013. High-value products from microalgae-their development and
commercialisation. J. Appl. Phycol. 25 (3):743-756. doi.org/10.1007/s10811-013-
9983-9.
pt

11. Brennan, L., and P. Owende. 2010. Biofuels from microalgae– A review of
technologies for production, processing, and extractions of biofuels and co-products.
ce

Renew. Sustain. Energy Rev. 14 (2):557–577. doi.org/10.1016/j.rser.2009.10.009.

12. Carr, F. J., D. Chill, and N. Maida. 2002. The lactic acid bacteria: a literature survey.
Crit. Rev. Microbiol. 28 (4):281–370. doi.org/10.1080/1040-840291046759.
Ac

13. Chang, H.C., and L.-C. Wu. 2008. Texture and quality properties of Chinese fresh egg
noodles formulated with green seaweed (Monostroma nitidum) powder. J. Food Sci.
73 (8):S398-S404. doi.org/10.1111/j.1750-3841.2008.00912.x.
14. Charoensiddhi, S., A. J. Lorbeer, C. M. M. Franco, P. Su, M. A. Conlon, and W.
Zhang. 2018. Process and economic feasibility for the production of functional food
from the brown alga Ecklonia radiate. Algal Res. 29:80-91.
doi.org/10.1016/j.algal.2017.11.022.
15. Chen, C.-Y., K.-L. Yeh, R. Aisyah, D.-J. Lee, and J.-S. Chang. 2011. Cultivation,
photobioreactor design and harvesting of microalgae for biodiesel production: A
critical review. Bioresour. Technol. 102 (1):71–81.
doi.org/10.1016/j.biortech.2010.06.159.

13
16. Chisti, Y. 2007. Biodiesel from microalgae. Biotechnol. Adv. 25 (3):294-306.
doi.org/10.1016/j.biotechadv.2007.02.001.
17. Cofrades, S., I. López-López, C. Ruiz-Capillas, M. Triki, and F. Jiménez-Colmenero,
2011. Quality characteristics of low-salt restructured poultry with microbial
transglutaminase and seaweed. Meat Sci. 87 (4): 373-380.
doi.org/10.1016/j.meatsci.2010.11.014.
18. Cofrades, S., M. Serdaroğlu, and F. Jiménez-Colmenero. 2013. Design of healthier
foods and beverages containing whole algae. In: Functional Ingredients from Algae
for Foods and Nutraceuticals, ed. H. Dominguez, 609-633. Woodhead Publishing
Series.
19. Domínguez, H. 2013. Algae as a source of biologically active ingredients for the
formulation of functional foods and nutraceuticals. In: Functional Ingredients from
Algae for Foods and Nutraceuticals, ed. H. Dominguez, 1-19. Woodhead Publishing
Series.
20. El Arroussi, H., R. Benhima, N. El Mernissi, R. Bouhfid, C. Tilsaghani, I. Bennis, and

t
I. Wahby. 2017. Screening of marine microalgae strains from Moroccan coasts for

ip
biodiesel production. Renew. Energy. 113: 1515-1522.
doi.org/10.1016/j.renene.2017.07.035.
21. EL Gamal, A. A. 2010. Biological importance of marine algae. Saudi Pharm. J. 18

cr
(1):1-25. doi.org/10.1016/j.jsps.2009.12.001.
22. Eom, S.-H., S.-Y. Moon, D.-S. Lee, H.-J. Kim, K. Park, E.-W. Lee, T. H. Kim, Y.-H.

us
Chung, M.-S. Lee, and Y.-M. Kim. 2015. In vitro antiviral activity of dieckol and
phlorofucofuroeckol-A isolated from edible brown alga Eisenia bicyclis against
murine norovirus. Algae. 30 (3):241-246. doi.org/10.4490/algae.2015.30.3.241.
an
23. Felis, G. E., and B. Pot. 2014. The family Lactobacillaceae. In: Lactic Acid Bacteria :
Biodiversity and Taxonomy, ed. W. H. Holzapfel, and B. J. B. Wood, 245-247. John
Wiley & Sons.
M

24. Fleita, D., M. El-Sayed, and D. Rifaat. 2015. Evaluation of the antioxidant activity of
enzymatically-hydrolyzed sulfated polysaccharides extracted from
red algae; Pterocladia capillacea. LWT- Food Sci. Technol. 63 (2):1236-1244.
ed

doi.org/10.1016/j.lwt.2015.04.024.
25. Goiris, K., K. Muylaert, I. Fraeye, I. Foubert, J. De Brabanter, and L. De Cooman.
2012. Antioxidant potential of microalgae in relation to their phenolic and carotenoid
content. J. Appl. Phycol. 24 (6):1477-1486. doi:10.1007/s10811-012-9804-6.
pt

26. Goñi, I., L. Valdivieso, and A. Garcia-Alonso. 2000. Nori seaweed consumption
modifies glycemic response in healthy volunteers. Nutr. Res. 20 (10):1367-1375.
ce

doi.org/10.1016/S0271-5317(00)80018-4.
27. Guiry, M. D. 2012. How many species of algae are there? J. Phycol. 48 (5):1057–
1063. doi.org/10.1111/j.1529-8817.2012.01222.x.
Ac

28. Guiry, M. D., and G. M. Guiry. Algae Base. 2018. World-wide electronic publication,
National University of Ireland, Galway. Accessed February 18, 2018.
http://www.algaebase.org.
29. Gupta, S., and N. Abu-Ghannam. 2011. Recent developments in the application of
seaweeds or seaweed extracts as a means for enhancing the safety and quality
attributes of foods. Innov. Food Sci. Emerg. Technol. 12 (4):600-609.
doi.org/10.1016/j.ifset.2011.07.004.
30. Gupta, S., G. Rajauria, and N. Abu-Ghannam. 2010. Study of the microbial diversity
and antimicrobial properties of Irish edible brown seaweeds. Int. J. Food Sci. Technol.
45 (2):482-489. doi.org/10.1111/j.1365-2621.2009.02149.x.

14
31. Hall, A. C., A. C. Fairclough, K. Mahadevan, and J. R. Paxman. 2012. Ascophyllum
nodosum enriched bread reduces subsequent energy intake with no effect on
postprandial glucose and cholesterol in healthy, overweight males. A pilot study.
Appetite. 58 (1):379–386. doi.org/10.1016/j.appet.2011.11.002.
32. Han, L., N. Xu, J. Shi, X. Yan, and C. Zheng. 2005. Isolation and pharmacological
activities of bromophenols from Rhodomela confervoides. Chin. J. Oceanol. Limnol.
23 (2):226-229. doi.org/10.1007/BF02894243.
33. Hayashi, T., K. Hayashi, M. Maeda, and I. Kojima. 1996. Calcium spirulan, an
inhibitor of enveloped virus replication, from a blue-green alga Spirulina platensis. J.
Nat. Prod. 59 (1):83–87. doi.org/10.1021/np960017o.
34. He, M. L., W. Hollwich, and W. A. Rambeck. 2002. Supplementation of algae to the
diet of pigs: A new possibility to improve the iodine content in the meat. J. Anim.
Physiol. Anim. Nutr. 86 (3-4):97-104. doi.org/10.1046/j.1439-0396.2002.00363.x.
35. Heo, J.-Y., H.-J. Shin, D.-H. Oh, S.-K. Cho, C.-J. Yang, I.-K. Kong., S.-S. Lee, K.-S.
Choi, S.-H. Choi, S.-C. Kim, H.-Y. Choi and I. Bae. 2006. Quality properties of

t
Appenzeller cheese added with Chlorella. Korean J. Food Sci. Anim. Resour. 26

ip
(4):525–531.
36. Hernández-Carmona G., Y. Freile-Pelegrín, and E. Hernández-Garibay. 2013.

cr
Conventional and alternative technologies for the extraction of algal polysaccharides.
In: Functional Ingredients from Algae for Foods and Nutraceuticals, ed. H.
Dominguez, 475-516. Woodhead Publishing Series.

us
37. Hofvendahl, K., and B. Hahn-Hägerdal. 2000. Factors affecting the fermentative lactic
acid production from renewable resources. Enzyme Microb. Technol. 26 (2-4):87-107.
doi.org/10.1016/S0141-0229(99)00155-6.
an
38. Hopkins, D. L., E. H Clayton, T. A. Lamb, R. J van de Ven, G. Refshauge, M. J Kerr,
K. Bailes, P. Lewandowski, and E. N. Ponnampalam. 2014. The impact of
supplementing lambs with algae on growth, meat traits and oxidative status. Meat Sci.
M

98 (2):135-141. doi.org/10.1016/j.meatsci.2014.05.016.
39. Jeon, J.-K. 2006. Effect of Chlorella addition on the quality of processed cheese. J.
Korean Soc. Food Sci. Nutr. 35 (3):373–377. doi.org/10.3746/jkfn.2006.35.3.373.
ed

40. Ji, X., M. Jiang, J. Zhang, X. Jiang, and Z. Zheng. 2018. The interactions of algae-
bacteria symbiotic system and its effects on nutrients removal from synthetic
wastewater. Bioresour. Technol. 247:44-50. doi.org/10.1016/j.biortech.2017.09.074.
41. Kączkowski J. 2017. Podstawy biochemii. Warsaw: PWN.
pt

42. Kalin, M., W. N. Wheeler, and G. Meinrath. 2005. The removal of uranium from
mining waste water using algal/microbial biomass. J. Environ. Radioact. 78 (2):151-
ce

177. doi.org/10.1016/j.jenvrad.2004.05.002.
43. Kim, H.-W., J.-H. Choi, Y.-S. Choi, D.-J. Han, H.-Y. Kim, M.-A. Lee, S.-Y. Kim, and
C.-J. Kim. 2010. Effects of Sea Tangle (Lamina japonica) powder on quality
Ac

characteristics of breakfast sausages. Korean J. Food Sci. Anim. Resour. 30 (1):55-61.

doi.org/10.5851/kosfa.2010.30.1.55.
44. Kim, K.-H., D. Yu, S.-H. Eom, H.-J. Kim, D.-H. Kim, H.-S. Song, D.-M. Kim, and
Y.-M. Kim. 2017. Fucofuroeckol-A from edible marine alga Eisenia bicyclisto restore
antifungal activity of fluconazole against fluconazole-resistant Candida albicans. J.
Appl. Phycol. 1-5. doi.org/10.1007/s10811-017-1232-1.
45. Lalic, L. M., and K. Berkovic. 2005. The influence of algae addition on
physicochemical properties of cottage cheese. Milchwissenschaft. 60 (2):151-154.
46. Libudzisz Z. 2008. Bakterie fermentacji mlekowej. In Mikrobiologia techniczna, ed.
Z. Libudzisz, K. Kowal, and Z. Żakowska, vol. 2, 25-58.Warsaw: PWN.

15
47. Lima, R. L., K. M. S. Pires-Cavalcante, D. B. Alencar, F. A. Viana, A. H. Sampaio,
and S. Saker-Sampaio. 2016. In vitro evaluation of antioxidant activity of methanolic
extracts obtained from seaweeds endemic to the coast of Ceará, Brazil. Acta
Scientiarum – Technol. 38 (2):247-255. doi.org/10.4025/actascitechnol.v38i2.27275.
48. López-López, I., S. Bastida, C. Ruiz-Capillas, L. Bravo, M. T. Larrea, F. Sánchez-
Muniz, S. Cofrades, and F. Jiménez-Colmenero. 2009a. Composition and antioxidant
capacity of low-salt meat emulsion model systems containing edible seaweeds. Meat
Sci. 83 (3):492-498. doi.org/10.1016/j.meatsci.2009.06.031.
49. López-López, I., S. Cofrades, A. Yakan, M. T. Solas, and F. Jiménez-Colmenero.
2010. Frozen storage characteristics of low-salt and low-fat beef patties as affected by
Wakame addition and replacing pork backfat with olive oil-in-water emulsion. Food
Res. Int. 43 (5):1244-1254. doi.org/10.1016/j.foodres.2010.03.005.
50. López-López, I., S. Cofrades, C. Ruiz-Capillas, and F. Jiménez-Colmenero. 2009b.
Design and nutritional properties of potential functional frankfurters based on lipid
formulation, added seaweed and low salt content. Meat Sci. 83 (2):255-262.

t
doi.org/10.1016/j.meatsci.2009.05.014.

ip
51. Mallick, N. 2002. Biotechnological potential of immobilized algae for wastewater N,
P and metal removal: a review. Biometals. 15 (4):377-390.

cr
52. McKay, L. L. and K. A. Baldwin. 1990. Applications for biotechnology: present and
future improvements in lactic acid bacteria. FEMS Microbiol. Rev. 7 (1-2):3–14.
doi.org/10.1016/0378-1097(90)90694-L.

us
53. Mendes, A., T. Lopes da Silva, and A. Reis. 2007. DHA Concentration and
Purification from the Marine Heterotrophic Microalga Crypthecodinium cohnii CCMP
316 by Winterization and Urea Complexation. Food Technol. Biotechnol. 45 (1):38-
an
44.
54. Mohsenpour, S. F., and N. Willoughby. 2013. Luminescent photobioreactor design for
improved algal growth and photosynthetic pigment production through spectral
M

conversion of light. Bioresour. Technol. 142:147–153.

doi.org/10.1016/j.biortech.2013.05.024.
55. Muñoz, R., and B. Guieysse. 2006. Algal–bacterial processes for the treatment of
ed

hazardous contaminants: a review. Water Res. 40 (15):2799-2815.

doi.org/10.1016/j.watres.2006.06.011.
56. Murillo-Álvarez, J. I., and G. Hernández-Carmona. 2007. Monomer composition and
sequence of sodium alginate extracted at pilot plant scales from three commercially
pt

important seaweeds from México. J. Appl. Phycol. 19 (5):545–548.

doi.org/10.1007/s10811-007-9168-5.
ce

57. Nagle, N., and P. Lemke. 1990. Production of methyl ester fuel from microalgae.
Appl. Biochem. Biotechnol. 24 (1):355-361. doi.org/10.1007/BF02920259.
58. Narayanan, N., P. K. Roychoudhury, and A. Srivastava. 2004. L(+) lactic acid
Ac

fermentation and its product polymerization. Electron. J. Biotechnol. 7 (2):167-179.

doi.org/10.2225/vol7-issue2-fulltext-7.
59. Neves, A. R., W. A. Pool., J. Kok, O. P. Kuipers, and H. Santos. 2005. Overview on
sugar metabolism and its control in Lactococcus lactis- The input from in vivo NMR.
FEMS Microbiol. Rev. 29 (3):531–554.
60. Ohta, S., Y. Shiomi, A. Kawashim, O. Aozasa, T. Nakao, T. Nagate, K. Kitamura, and
H. Miyata. 1995. Antibiotic effect of linolenic acid from Chlorococcum strain HS-101
and Dunaliella primolecta on methicillin-resistant Staphylococcus aureus. J. Appl.
Phycol. 7 (2):121–127. doi.org/10.1007/BF00693057.

16
61. Pina-Pérez, M. C., A. Rivas, A. Martínez, and D. Rodrigo. 2017. Antimicrobial
potential of macro and microalgae against pathogenic and spoilage microorganisms in
food. Food Chem. 235:34-44. doi.org/10.1016/j.foodchem.2017.05.033.
62. Ponnampalam, E. N., V. F. Burnett, S. Norng, D. L. Hopkins, T. Plozza, and J. L.
Jacobs. 2016. Muscle antioxidant (vitamin E) and major fatty acid groups, lipid
oxidation and retail colour of meat from lambs fed a roughage based diet with flaxseed
or algae. Meat Sci. 111:154-160. doi.org/10.1016/j.meatsci.2015.09.007.
63. Prabhasankar, P., P. Ganesan, and N. Bhaskar. 2009a. Influence of Indian brown
seaweed (Sargassum marginatum) as an ingredient on quality, biofunctional and
microstructure characteristics of pasta. Food Sci. Technol. Int. 15 (5):471-479.
doi.org/10.1177/1082013209350267.
64. Prabhasankar, P., P. Ganesan, N. Bhaskar, A. Hirose, N. Stephen, L. R. Gowda, M.
Hosokawa, and K. Miyashita. 2009b. Edible Japanese seaweed, wakame (Undaria
pinnatifida) as an ingredient in pasta: Chemical, functional and structural evaluation.
Food Chem. 115 (2):501-508. doi.org/10.1016/j.foodchem.2008.12.047.

t
65. Rafiquzzaman, S. M., M. U. Ahmad, J. M. Lee, E.-Y. Kim, Y.-O. Kim, D.-G. Kim,

ip
and I.-S. Kong. 2016. Phytochemical Composition and Antioxidant Activity of Edible
Red Alga Hypnea musciformis from Bangladesh. J. Food Process. Preserv. 40

cr
(5):1074-1083. doi.org/10.1111/jfpp.12688.
66. Rosaline, D., S. Sakthivelkumar, K. Rajendran, and S. Janarthanan. 2016. Detection of
antibacterial activity and its characterization from the marine macro-algae Sargassum

us
wightii (Greville ex J. Agardh 1848). Indian J. Geo-Marine Sci. 45 (10):1365-1371.
67. Sarojini, Y., B. Sujatha and P. Santha Rao. 2016. The variation in distribution of total
phenols and antioxidant activity in five species of marine macro algae. Der Pharm.
an
Lettre. 8 (1):30-37.
68. Sasaki, K., K. Ishihara, C. Oyamada, A. Sato, A. Fukushi, T. Arakane, M. Motoyama,
M. Yamazaki, and M. Mitsumoto. 2008. Effects of fucoxanthin addition to ground
M

chicken breast meat on lipid and colour stability during chilled storage, before and
after cooking. Asian-Australas. J. Anim. Sci. 21 (7):1067-1072.
doi.org/10.5713/ajas.2008.70670.
ed

69. Senthil, A., B. S. Mamatha, and M. Mahadevaswamy. 2005. Effect of using seaweed
(eucheuma) powder on the quality of fish cutlet. Int. J. Food Sci. Nutr. 56 (5):327-335.
doi.org/10.1080/09637480500224205.
70. Shin, Y. J., H. Y Song, Y. B. Seo, and K. B. Song. 2012. Preparation of red algae film
pt

containing grapefruit seed extract and application for the packaging of cheese and
bacon. Food Sci. Biotechnol. 21 (1):225–231.
ce

71. Singh, R. N., and S. Sharma. 2012. Development of suitable photobioreactor for algae
production – a review. Renew. Sustain. Energy Rev. 16 (4):2347-2353.
doi.org/10.1016/j.rser.2012.01.026.
Ac

72. Siriwardhana, N., K. W. Lee, S. H. Kim, J.-H. Ha, G.-T. Park, and Y. J. Jeon. 2004.
Lipid peroxidation inhibitory effects of Hizikia fusiformis methanolic extract on fish
oil and linoleic acid. Food Sci. Technol. Int. 10 (2):65-72.
doi.org/10.1177/1082013204043883.
73. Soares, F., C. Fernandes, P. Silva, L. Pereira, and T. Gonçalves. 2016. Antifungal
activity of carrageenan extracts from the red alga Chondracanthus
teedei var. lusitanicus. J. Appl. Phycol. 28 (5):2991-2998. doi.org/10.1007/s10811-
016-0849-9.
74. Stiles, M. E., and W. H. Holzapfel. 1997. Lactic acid bacteria of foods and their
current taxonomy. Int. J. Food Microbiol. 36 (1):1-29. doi.org/10.1016/S0168-
1605(96)01233-0.

17
75. Suraiya, S., J. M. Lee, H. J. Cho, W. J. Jang, D. -G. Kim, Y. -O. Kim, and I. -S. Kong.
2018. Monascus spp. fermented brown seaweeds extracts enhance bio-functional
activities. Food Biosci. 21: 90-99. doi.org/10.1016/j.fbio.2017.12.005.
76. Suresh, B., and G. A. Ravishankar. 2004. Phytoremediation- a novel and promising
approach for environmental clean-up. Crit. Rev. Biotechnol. 24 (2-3):97-124.
doi.org/10.1080/07388550490493627.
77. Uchida M., and M. Murata. 2004. Isolation of a lactic acid bacterium and yeast
consortium from a fermented material of Ulva spp. (Chlorophyta). J. Appl. Microbiol.
97:1297-1310. doi.org/10.1111/j.1365-2672.2004.02425.x.
78. Uchida, M., M. Murata, and F. Ishikawa, 2007. Lactic acid bacteria effective for
regulating the growth of contaminant bacteria during the fermentation of Undaria
pinnatifida (Phaeophyta). Fish. Sci. 73:694-704. doi.org/10.1111/j.1444-
2906.2007.01383.x
79. Uchida, M., T. Miyoshi, G. Yoshida, K. Niwa, M. Mori, and H. Wakabayashi 2014a.
Isolation and characterization of halophilic lactic acid bacteria acting as a starter

t
culture for sauce fermentation of the red alga Nori (Porphyra yezoensis). J. Appl.

ip
Microbiol. 116:1506-1520. doi.org/10.1111/jam.12466.
80. Uchida, M., T. Miyoshi, M. Kaneniwa, K. Ishihara, Y. Nakashimada, and N. Urano.

cr
2014b. Production of 16.5 % v/v ethanol from seagrass seeds. J. Biosci. Bioeng.
118:646-650. doi.org/10.1016/j.jbiosc.2014.05.017.
81. Uchida, M., H. Kurushima, K. Ishihara, Y. Murata, K. Touhata, N. Ishida, K. Niwa,

(Pyropia yezoensis). J.
doi.org/10.1016/j.jbiosc.2016.10.003.
Biosci.
us
and T. Araki. 2017. Characterization of fermented seaweed sauce prepared from nori
Bioeng. 123 (3):327-332.
an
82. Uchida M., H. Kurushima, N. Ishida, T. Araki, K. Ishihara, Y. Murata, K. Touhata,
and N. Ishida. 2018. Preparation and characterization of fermented seaweed sauce
manufactured from low-quality nori (dried and fresh fronds of Pyropia yezoensis).
M

Fish. Sci. 84 (3):589-596. doi.org/10.1007/s12562-018-1184-7.

83. Vaishampayan, A., R. P. Sinha, D.-P. Hader, T. Dey, A. K. Gupta, U. Bhan, and A. L.
Rao. 2001. Cyanobacterial biofertilizers in rice agriculture. Bot. Rev. 67 (4):453-516.
ed

doi.org/10.1007/BF02857893.
84. Wang, T., R. Jónsdóttir, H. G. Kristinsson, G. Thorkelsson, C. Jacobsen, P. Y.
Hamaguchi, and G. Ólafsdóttir. 2010. Inhibition of haemoglobin-mediated lipid
oxidation in washed cod muscle and cod protein isolates by Fucus vesiculosus extract
pt

and fractions. Food Chem. 123 (2):321-330. doi.org/10.1016/j.foodchem.2010.04.038.

85. Wee, Y.-J., J.-N. Kim, and H.-W. Ryu. 2006. Biotechnological production of lactic
ce

acid and its recent application. Food Technol. Biotechnol. 44 (2):163-172.

86. Welman, A. D. and I. S. Maddox. 2003. Exopolysaccharides from lactic acid bacteria:
perspectives and challenges. Trends Biotechnol. 21 (6):269–274.
Ac

87. Yun, J.-S., Y.-J. Wee, and H.-W. Ryu. 2003. Production of optically pure L(+)-lactic
acid from various carbohydrates by batch fermentation of Enterococcus faecalis
RKY1. Enzyme Microb. Technol. 33 (4):416–423. doi.org/10.1016/S0141-
0229(03)00139-X.
88. Zaremba, M. L., and J. Borowski. 1997. Bakteriologia lekarska. In Mikrobiologia
lekarska. 113-398. Warsaw: PZWL.
89. Zhu, L., Y. K. Nugroho, S. R. Shakeel, Z. Li, B. Martinkauppi, and E. Hiltunen. 2017.
Using microalgae to produce liquid transportation biodiesel: What is next? Renew.
Sustain. Energy Rev. 78:391-400. doi.org/10.1016/j.rser.2017.04.089.

18
Table 1. Biological properties of algae.
Properties of algae Algae species Microorganisms Source

Antioxidant Tetraselmis suecica, Goiris et al. 2012

Botryococcus braunii,
Neochloris oleoabundans,
Isochrysis sp.,
Chlorella vulgaris,
Phaeodactylum
tricornutum

Pterocladia capillacea Fleita, El-Sayed, and

t
ip
Rifaat 2015

Spirulina platensis

cr
Afify et al. 2017

Hypnea musciformis Rafiquzzaman et al.

Caulerpa cupressoides,
us 2016

Lima et al. 2016

an
Ulva fasciata,
Amansia multifida,
M

Cryptonemia crenulata,
Dictyota dichotoma,
ed

Sargassum vulgare

Amansia multifida, Alencar et al. 2014

pt

Meristiella echinocarpa.
ce

Ulva fasciata, Sarojini, Sujatha,

Enteromorpha compressa, and Santha Rao
Ac

Caulerpa sertularioides, 2016

Gracilaria corticata,
Hypnea musciformis

Antibacterial Chlorococum HS-101 Staphylococcus aureus Ohta et al. 1995

Dunaliella primolecta (MRSA)

Rhodomela confervoides Staphylococcus aureus, Han et al. 2005

19
 Pseudomonas
aeruginosa.

Himanthalia elongata, Listeria monocytogenes Gupta, Rajauria, and

Laminaria sachharina, Salmonella abony, Abu-Ghannam 2010
Laminaria digitata Enterococcus faecalis,
Pseudomonas aeruginosa

Pterocladia capillacea Staphylococcus aureus, Fleita, El-Sayed, and

Escherichia coli Rifaat 2015

Sargassum wightii Staphylococcus aureus, Rosaline et al. 2016

Bacillus subtilis,

t
ip
Enterococcus faecalis,
Pseudomonas

cr
aeruginosa, Erwinia sp.,

Proteus us
Enterobacter aerogenes,
vulgaris,
an
Escherichia coli

Antiviral Spirulina platensis Wirus Herpes simplex Hayashi et al. 1996

M

type 1, HMV, measles

virus, mumps virus,
ed

influenza virus A, and

HIV-1
pt

Eisenia bicyclis Murine norovirus (MNV) Eom et al. 2015

Antifungal Eisenia bicyclis Candida albicans Kim et al. 2017

ce

Chondracanthus teedei Aspergillus fumigatus, Soares et al. 2016

Ac

var. lusitanicus Alternaria infectoria

20
Table 2. Classification od lactic acid bacteria depending on the fermentation type (Felis and
Pot 2014; Libudzisz 2008; Stiles and Holzapfel 1997; Yun, Wee, and Ryu 2003).

Obligatory Facultatively Obligatory

homofermentative heterofermentative homofermentative
Lb. acidophilus Lb. acetotolerans Lb. acidifarinae
Lb. amylophilus Lb. acidipiscis Lb. antri
Lb. bavaricus Lb. agilis Lb. brevis
Lb. bulgaricus Lb. algidus Lb. buchneri
Lb. catenaformis Lb. alimentarius Lb. fermentum

t
Lb. delbrueckii Lb. bifermentans Lb. florum

ip
Lb. equi Lb. casei Lb. fructivorans

cr
Lb. farciminis Lb. ceti Lb. hilgardii
Lb. gasseri Lb. coryniformis Lb. ingluviei
Lb. helveticus
Lb. hominis
Lb. curvatus
Lb. paracasei us
Lb. kunkeei
Lb. ozensis
an
Lb. johnsonii Lb. pentosus Lb. panis
Lb. mali Lb. plantarum Lb. parabrevis
M

Lb. salivarius L. rhamnosus Lb. rapi

Lb. uvarum Lb. sakei Lb. reuteri
ed
pt
ce
Ac

21
 Ac
ce
pt
ed

22
M
an
us
cr
ip
t
 Ac
ce
pt
ed

23
M
an
us
cr
ip
t