Use of algae as food ingredient: sensory acceptance and commercial products

Introduction to algae as food source

The increasing worldwide population is projected to be around 9.7 billion in 2050 (Ehrlich and Harte, 2015; UN DESA, 2022), with massive demand for proteins either from animal-based foods (meat, poultry, fish, eggs, and dairy foods) or plant-based foods (fruits, vegetable, grains, nuts, and seeds) has driven researchers to investigate more sustainable food sources such as algal-based foods (Matos, 2020; Amorim et al., 2021). Current protein demand is approximately 202 million tonnes globally (Henchion et al., 2017), and according to the British nutrition foundation, the reference nutrient intake (RNI) for protein for adults is 0.75 g protein per kg body weight per day; this equates to 56 g/day and 45 g/day for men and women of average body weights (75 and 60 Kg), respectively.

Algae represent an interesting possibility to supply the growing need for protein demand as well as a source of bioactive compounds such as amino acids, polyunsaturated fatty acids, vitamins, and minerals for the enrichment of traditional algal foods (Matos, 2017). Like tofu, tempeh, lentils, chickpeas, and almonds, algae and its byproducts can efficiently be used for the development of new foods, providing rich biomass as substitutes for plant-based meat alternatives (Onwezen et al., 2021). When following a plant-based diet, there are some key nutrients and/or products that consumers should focus on, such as plant-based foods rich in protein, vitamins, and minerals (vitamin B₁₂, vitamin D, and calcium) as well as essential omega-3 fatty acids (De Farias Neves et al., 2019). Additionally, polysaccharides like carrageen, alginate, and agar-agar extracted from seaweed are all widely used as additives or adjuvants for the food industry as thickening agents for drinks, ice cream, cosmetics, and as gelling agents for jellies (Hung et al., 2021). Sodium alginate, for instance, can be mixed with soybean flour to make meat or fish analogue (Zhang et al., 2020).

Several recent studies found in the literature have proposed the use of whole algae or algae extract for the development of new foods, with investigations on the digestibility and bioaccessibility of algal biomass in different food matrixes. For example, 1) the sensory, physical, and chemical properties, antioxidant activity, and in vitro digestibility of microalgae biomass as an alternative ingredient in cookies was evaluated (Batista et al., 2017); 2) the nutritional, physical and sensory evaluations of Arthrospira platensis biomass for snack enrichment was investigated (Lucas et al., 2018); 3) the effect of Spirulina biomass on the technological and nutritional quality of bread wheat pasta was also investigated (Rodríguez Demarco et al., 2022); 4) the physical and antioxidant properties of gluten-free bread enriched with brown algae (Ascophyllum nodosum) was explored by Różyło et al. (2017); and 5) the biosorption of protein, minerals (Na, P, Ca, and Mg) and phenolic compounds of snack (extruded maize) enriched with Porphyra columbina was investigated by Cian et al. (2014). All these studies have shown the promising impact of consuming algae-based foods under in vitro experimental studies linked with the bioaccessibility of nutrients.

Other studies have reported that the addition of high concentration of algal biomass might result in negative effects on color and flavor of the final product, which depends on algae species and end product, decreasing consumers’ acceptance (Geada et al., 2021). For this reason, a concentration of a maximum 5% (w/w) of algal biomass has been generally utilized and incorporated in algal-food products (Batista et al., 2017).

Considering the skyrocketing growth of the healthy and plant-based food sector, it is not surprising that algae are being pursued as a functional ingredient. Previously widely used in animal feed, the high protein yield of certain microalgae lends them to be an attractive ingredient for a variety of foodstuffs (Matos, 2019).

In this mini-review, the technological and practical aspects of using algae as an ingredient for food development are briefly discussed, showing challenges related to sensory properties and product acceptance as food ingredients, by consumers. Examples of novel food products are also presented, giving an overview of companies and their foods enriched with microalgae and/or seaweed biomass.

Algae are a suitable source of nutritional compounds?

The term “algae” is a collective term for various water-dwelling eukaryotes that perform photosynthesis. The size of the algae is a suitable differentiating feature with microalgae, often unicellular organisms, only viewed under a microscope (<100 µm), while macroalgae can be seen with the naked eye (Moheimani et al., 2015). In Asian culture, food products containing seaweed have been used directly in traditional foods, such as established nori (e.g., Porphyra) for sushi or Ulva lactuca as sea lettuce (Fleurence, 2016). Further examples are wakame (Undaria pinnatifida), Kombu (Saccharina japonica), Irish moss (Chondrus crispus) and thongweed or sea spaghetti (Himanthalia elongate) (Parniakov et al., 2018), which provide texture and flavor to the food product (Taboada et al., 2013).

Microalgae are also increasingly used as ingredient for foods as a flavor active, texture enhancer or nutrients source (Coleman et al., 2022). Among the best-known microalgae species are Arthrospira platensis (Spirulina) and Chlorella vulgaris, which can act as a vegan protein source due to their high protein content (50%–60% of dry weight) with a complementary roll of essential amino acids and vitamin B₁₂ (Figure 1) (Matos, 2019). These microalgae have been listed in the EU Novel food catalogue for food applications by the European Food Safety Authority (EFSA, https://webgate.ec.europa.eu/fip/novel_food_catalogue/) (Enzing et al., 2014) and approved by the United States Food Drug Administration (FDA) as generally recognized as safe (GRAS) (21CFR73.530 for Spirulina and GRN 000986 for Chlorella) (Harp and Barrows, 2015).

FIGURE 1

FIGURE 1. Examples of commercialized microalgae available in the market (free-access photos assembled from Culture Collection of Algae (SAG) at Goettingen University). Biochemical content of some microalgae species with emphasizes to the protein content highlighted in green color. Data obtained from Matos et al. (2016).

It is important to highlight that microalgae are considered an unconventional food source and have to undergo a series of toxicological tests to prove their harmlessness (Becker, 2007). For example, Becker (2013) has suggested that approval of algal biomass for human consumption should follow some quality and safety standards, such as 1) proximate chemical composition, 2) evaluation of protein quality and quantity of essential amino acids, 3) determination of biogenic toxic substances (phycotoxins and other toxicants), 4) identification of non-biogenic toxic compounds (heavy metals, residues from harvesting and processing), 5) sanitary analyses including contamination by microbial pathogens, and 6) toxicological and safety evaluations.

To be able to use algae skillfully for food nutrition, their contents of proteins, dietary fibers, omega-3 fatty acids, pigments, vitamins, and trace elements must be considered, in addition to their flavor, bioaccessibility, and processability. The main value-adding uses of algae in foods are listed below:

• Algae are suitable for fish and shellfish substitutes because of their specific flavor, which ranges from umami, salty, grassy, and nutty to extend neutral (Turchini et al., 2009).

• Algae can make a significant contribution to the supply of omega-3 fatty acids and thus take over the role of fish meat in the diet. Long-chain fatty acids like eicosapentaenoic acid (EPA, C_20:5ω3) and docosahexaenoic acid (DHA, C_22:6ω3) are generally ingested via fish oil and can be replaced by directly some microalgae (Matos, 2016).

• Algae are a primary source of natural pigments such as carotenes (β-carotene, lycopene and astaxanthin) and xanthophylls (lutein and zeaxanthin), which have several positive physiological effects on human health (Maoka, 2020).

• Vitamin B₁₂, known as cobalamin, which is primarily found in animal products, is also produced by certain algae, notably Arthrospira platensis. This alga is, therefore interesting to prevent a possible deficiency as a result of a vegan diet (Grosshagauer et al., 2020).

• In terms of trace elements like minerals, algae contain zinc, iron, selenium, potassium, and calcium, which are all essential microelements for human consumption and metabolism (Demarco et al., 2022).

Challenges Surrounding algal usage and food acceptance

One of the main important aspects of using algae in food systems are related to the palatability of algal biomass in terms of sensory input induced by aroma, color, taste (salty, sweet, sour, bitter, and umami) and textural mouthfeel (Isleten Hosoglu, 2018). The main characteristics of aroma in algae biomass is derived from a complex mixture of different odor-active volatile chemical compounds as stated by Coleman et al. (2022). In particular, four classes of typical odor-active volatile chemicals in algae are known: 1) fatty acid-derived volatiles compounds (aldehydes, alcohols and ketones) originated from the lypoxygenase activity or autoxidation of polyunsaturated fatty acids; 2) sulfuric compounds such as dimethyl sulfuric (DMS, C₂H₆O₄S), dimethyl disulfide (DMDS, C₂H₆S₂) and methanethiol (CH₄S); 3) nitrogen-containing compounds such as trimethylamine (TMA, C₃H₉N) originated from the action of microbial activity that reduces osmolyte trimethylamine oxide (TMAO) into TMA; and 4) umami taste compounds related to the presence of specific free amino acids such as glutamate (Glu) and aspartate (Asp) as well as nucleotides, notably inosine monophosphate (IMP), guanosine monophosphate (GMP) and adenosine monophosphate (AMP).

Extraction of free amino acids and 5′-nucleotides from seven Dutch seaweed species analyzed by reversed-phase and mixed-mode HPLC as key contributors to the acceptance of umami taste seaweed has been investigated (Moerdijk-Poortvliet et al., 2022). Authors have identified that Phaeophyceae seaweed class showed the highest equivalent umami concentration (EUC), followed by Chlorophyceae and Rhodophyceae (≈9.5, 3.7, and 1.1 g/100 g respectively). In addition, glutamic acid always exceeded the taste activity values (TAV), while other umami compounds were species-specific, indicating that the correct determination of EUC values in algae can tailoring the appropriate seaweed species towards a product readily accepted as food source (Mouritsen et al., 2019). In contrast to seaweeds, there is little knowledge about the contribution of flavor in microalgae biomass, despite the ample attention received by these microorganisms in the past decade as a novel source of food. For this reason, the aroma and taste of eight different phototrophic microalage species were investigated and compared with five seaweeds to evaluate their potential as flavor ingredients in plant-based seafood alternatives (Coleman et al., 2022). According to the results, microalgae Rhodomonas salina, Tetraselmis chui, and Phaeodactylum tricornutum have a stronger seafood odor and taste features compared to seaweeds. The microalage species R. salina and T. chui have higher crab flavoring aroma, while P. tricornutum possesses the highest bitterness taste, which could be unwanted in plant-based products. T. chui also presents a slightly grassy odor, while Dunaliella salina is characterized by floral notes due to the presence of carotenoids-derived compounds (e.g., β-ionones).

Another notable study about aroma in microalgae was investigated by Isleten Hosoglu (2018), where the aroma characterization of five microalgae species (Crypthecodinium cohnii, Schizochytrium limacinum, Tetraselmis chuii, Chlorella vulgaris and Chlorella protothecoides) using solid-phase micro-extraction and gas chromatography-mass spectrometry/olfactometry was explored. The author remarkably stated that C. cohnii has a high level of sulfur compounds (dimethyl sulfide, ethanethiol), and ester and alcohol compounds associated with distinct ‘sulfur-cabbage, fruity, rosy, boiled potato’ aroma tastes. S. limacinum was characterized more by aldehydes and alcohol compounds linked with ‘mushroom, cucumber and fatty-grassy’ aroma attributes, while the other microalgae species showed moderate levels of ketone and terpene compounds with “woody and cereal-like” sensory qualities.

It is important to highlight that high protein content (28%–71% dry weight) of certain microalgae (Becker, 2007) could result in a high amount of free amino acids notably glutamic acid and aspartate, causing high umami taste desirable for the imparting flavor in plant-based seafood alternative (Coleman et al., 2022), whereas fishy off-flavors of microalgal biomass may be unwanted for certain food products (dairy foods, cookies, pasta, beverages, among others). In this way, advanced studies and investigations on the phytochemical compounds in microalgae are important to reveal the presence of volatile organic compounds that directly affect the sensorial properties of algal-based food products as well as its acceptance (Francezon et al., 2021).

Some authors have focused their research on evaluating the acceptance of algae as a food ingredient by consumers (Onwezen et al., 2021). For example, the motivational drivers and barriers of the adoption intention of Spirulina-enhanced food has been investigated (Moons et al., 2018), where health consciousness and the willingness to compromise on algal food taste are major motivational drivers of the adoption intention for sporting individuals, vegetarians, and foodies. Weinrich and Elshiewy (2019), for instance, have conducted a survey with 940 consumers from three different European countries (Germany: 315, Netherlands: 310, France: 315) to evaluate the preference and willingness to pay for meat substitutes based on microalgae biomass. Authors identified that consumers that see no need for meat in their diet have a higher probability to choose meat substitutes based on microalgae, while consumers with a strong habit for meat consumption show a negative relationship to choosing the meat substitutes based on microalgae. In general, consumers prefer products in which novel ingredients made from algae can be disguised due to their bitter taste and grassy odor (Onwezen et al., 2021). Disguising ingredients may increases familiarity with algae biomass due to its potential ability to mimic certain food ingredients such as seafood (Francezon et al., 2021). For example, the microalgae R. salina has the potential ability to act as flavoring agent in plant-based seafood because of its crab aroma, while Tetraselmis chui and Phaeodactylum tricornutum have strong seafood odor and a taste characterized by high umami and crab/shellfish flavor, which can be used to disguise flavor of animal-based seafood products (Coleman et al., 2022).

New food products derived from algal biomass

To track the newest news of food products enriched with algal biomass, the website Algae Planet accessed on https://algaeplanet.com/is a good reference that exhibits up-to-date information regarding algae industry. In Table 1, it is possible to visualize some examples of new food products under development based on either microalgae biomass or macroalgae also called kelp and/or seaweed.

TABLE 1

TABLE 1. New plant-based foods based on algal ingredients containing either microalgae or macroalgae (seaweed/kelp).

There is a great concern that current microalgae-based foods on the market often have a ‘grassy’ taste, intense green color and fishy odor that many consumers consider unpleasant. To use microalgae as a flavor ingredient, it is important that aroma and taste compounds are present in adequate concentrations. To minimize the off-flavors in algal food products, the appropriate selection of algal strain (Coleman et al., 2022), screening and optimization of culture conditions (Latsos et al., 2021), phytochemical studies and characterization of odorant compounds (López-Pérez et al., 2017) are some key steps towards the successful development of algal-food product.

A good example of algal food (ingredients) that tastes better is the honey yellow Chlorella powder produced by a Portuguese company (https://www.allmicroalgae.com/en/). The company also produces autotrophic organic Chlorella vulgaris with different characteristics (smooth-, honey- and white-Chlorella). The new Chlorella strain has a higher protein content (35%–40% per dry weight), and most importantly, from a consumer perspective, does not give food products the off-putting fishiness. To arrive at the new Chlorella strain, the researchers have applied random mutagenesis tool that induces mutations, generating proteins, enzymes and even entire genomes with improved properties. The new Chlorella strain developed by this company is then fully characterized from biochemical, technological, and sensorial perspectives to develop alternative food products such as cookies and biscuits (Gouveia et al., 2007; Batista et al., 2017), bread and pasta with improved nutritional value and organoleptic properties (Fradique et al., 2010; Diprat et al., 2020).

Kuehnle AgroSystems (KAS) (https://www.kuehnleagro.com/), a sustainable algae ingredients development company based in Honolulu, Hawaii, has announced the allowance of its patent for producing microalgal proteins and other products by culturing Chlamydomonas microalgae via dark fermentation (https://patentscope.wipo.int/search/en/detail.jsf?docId = WO2018006068). Unlike some microalgae, including Chlorella, the Chlamydomonas group of microalgae is distinguished by their soft and non-cellulosic cell wall that do not require added processing such as cell disruption to render its nutrients bioavailable (Fields et al., 2020). The company notes that the patented process covers the production of additional ingredients for adding color, flavor, and vital nutrients that can be used for plant-based meat and seafood, such as hematoproteins and selenoproteins, produced by members of the Chlamydomonadales (Kaur et al., 2009). Colors of the Chlamydomonas reinhardtii biomass produced by the dark fermentation process range from green and yellow to achlorophyllic color (in part from lutein/zeaxanthin), which is derived from a C. reinhardtii population of previously cryopreserved cells revived under mixotrophic conditions. The microalgal example also pertains to cell types of UV light-induced and chemically induced Chlamydomonas mutants (strain KAS 1602—variant derived from CC-125 or 137c) that lack carotenoids, providing different colors than the typical green (further descriptions about this patented process can be found in WO2018006068). The Chlamydomonas contains more than 60% of protein while delivering minerals, vitamins, antioxidants, and other components valued for foods, beverages, and nutraceuticals (Darwish et al., 2020).

Another distinguished foodstuff from microalgae is the microalgae-based cheese substitute, made from Sophie’s BioNutrients^® dairy-free microalgae milk (https://algaeplanet.com/sophies-closes-in-on-the-algal-bacon-cheeseburger/).

Sophie’s BioNutrients, a next-generation sustainable urban food technology company, together with Ingredion Idea Labs^® innovation center in Singapore, have collaborated to elaborate an algal-based cheese substitute that mimics natural Cheddar cheese. This product is developed using microalgae protein flour, and it is available as two types of products—a semi-hard microalgae dairy-free product and a dairy-free spread. Mohamed et al. (2013), for instance, have tested the quality in terms of chemical composition, physical properties and sensory acceptance of novel healthy processed cheese analogue enhanced with marine microalgae Chlorella vulgaris biomass. Cheese analogue is processed as a cheese-like product where milk fat, milk protein or both are partially or wholly replaced by non-milk-based components (Fox et al., 2017).

The bioproducts derived from Arthrospira platensis microalgae, notably protein and phycocyanin-pigment, have been used for many industrial applications (Lafarga et al., 2021), including for example the development soda beverage with blue-phycocyanin pigment (Jespersen et al., 2005), where authors studied the stabilities of three natural blue colorants (gardenia blue, phycocyanin and indigo) for use in confectionary and beverages under investigation of various pH toward heat and light exposition. Authors stated that phycocyanin was found to be insoluble in acidic solution (pH 3.0) and denatures at temperatures above 45°C at pH 5.0 and 7.0, causing degradation of −80% of the pigment as well as color change. Moreover, exploratory studies with the three blue colorants in model foods and beverages such as soft drinks, jelly gum, and sugar coating for soft candy showed that phycocyanin was a more versatile blue food colorant due to its inherent bright blue color in jelly gum and coated soft candy (De Amarante et al., 2020; Luzardo-Ocampo et al., 2021).

A new sophisticated coffee bean product called “Infinity Blue” was recently developed by The AAA Accelerator Group Europe AG, in Switzerland, and its biotech subsidiary Algatek Asturias, S.L., of Teverga Asturias Spain. The coffee bean production process for Infinity Blue has been registered for patent for coating the coffee beans with a soluble protein extracted from Arthrospira platensis biomass yielding a blue coffee bean that gives the consumer proteins not present in other coffee drinks. The coating also protects the coffee bean flavor, keeping the beans fresh for longer and locking in a premium coffee taste (https://algaeplanet.com/aaa-accelerator-and-algatek-introduce-infinity-blue-coffee/). Thinking in this soluble protein from A. platensis, Ramírez-Rodrigues et al. (2021) have investigated the techno-functional properties of a protein isolate from A. platensis biomass. Protein isolate was characterized in terms of protein content, structure (molecular mass, secondary structure, and thermal behavior) and functionality (emulsion capacity and stability) and was tested in two food prototypes, i.e., mayonnaise and fettuccine pasta. A. platensis protein isolate with sodium alginate (0.5%) produced stable emulsions (˃90%) during 14 days of storage and is comparable to the most commercially used protein in food products as a techno-functional additive.

Taking into account the potential of macroalgae as a potential source of protein, a Berkeley, California-based Umaro Foods (https://www.umarofoods.com/) has been showcasing an interesting and innovative plant-based bacon product. The company’s bacon benefits from two proprietary innovations. The first is the company’s own protein, UMARO^TM, which it extracts from ocean-farmed red seaweeds and that serves as a technological replacement for ‘heme’ group, the red protein molecule that makes plant-based meat “bleed” and provides the typical meat color. The second is the use of seaweed-based ingredients to encapsulate plant-based oils into a fat crisps and crunches just like animal fat. Meat and meat products have a central role in many food cultures, and transition towards to plant-based meat alternatives (PBMAs) have been identified as a key measure to promote health, while minimizing the impact of animal farming on the environment (Tso and Forde, 2021). Thus, an excellent review of research on plant-based meat analogue, including seaweed-based bacon, was discussed in detail in He et al. (2020), where driving forces for PBMA development, history of its progression, key technologies required for production, consumer attitudes and future research opportunities were summarized by the authors.

Another notable example of by-product made from red seaweed is the SEAFLOUR^TM produced by International Flavors & Frangances company (https://www.iff.com/sustainableseaweed). SEAFLOUR, also known as ‘seaweed flour’ is an ingredient with the properties to be a natural stabilizer that contains protein, fiber and minerals, offering food product stability, a high-suspension ability and excellent mouthfeel. This newly algal product is destined for plant-based beverage applications such as nut- and soy-based milk. The effect of seaweed flour incorporated in different foods has been previously tested such as 1) the effect of seaweed composite flour on the textural properties of dough and bread (Mamat et al., 2014); 2) the influence of seaweed composite flour on the physicochemical properties of muffin (Mamat et al., 2018); 3) the fermentation of seaweed flour with various fermenters to improve the quality of fish feed ingredients (Aslamyah et al, 2017), and 4) the fortification of seaweed flour on nutrition, iodine and glycemic index of pasta (Firdaus et al., 2017). All these studies have been shown the positive effect of adding seaweed flour in foodstuff as well as the significance of seaweed-based food for human health promotion (Lucas et al., 2019).

Conclusion

The search for novel foods and ingredients using algae either microalgae or seaweed biomass with remarkable nutritional, sensorial, and technological properties originated by sustainable food systems has grown exponentially in recent years. Few studies have investigated the chemical flavor compounds that impact the sensorial appeal of algal biomass, while other studies have focused their research on identifying the motivational drivers and barriers by the consumers in adopting a diet with algal biomass, where health consciousness and the willingness to compromise the algal-food taste are major concerns. New sophisticated microalgal-food products have been developed such as honey Chlorella yellow powder, sparkling water with distinct blue color from phycocyanin pigment, and coffee beans coated with soluble protein extracted from Arthrospira, while algal Cheddar cheese substitute, red seaweed as a substitute for bacon and conventional salmon are some novel algal-based food products, providing rich and nutritious biomass for human consumption. Future research on the influence of culture conditions that directly affect the synthesis of volatile compounds, free amino acids, and free nucleotides produced by different types of algae are necessary to bring closer readiness algal-based products with good sensory appeal for consumption.

Author contributions

APM: bibliographic investigations, writing—original draft, and writing—review and editing. GT: conceptualization, writing—original draft and writing—review and editing, supervising. EN: writing—review and editing, supervision. All authors contributed to the article and approved the submitted version.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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