# Algae as a Source of Natural Flavors in Innovative Foods

Nellie Francezon, Ariane Tremblay, Jean-Luc Mouget, Pamela Pasetto, Lucie Beaulieu

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## To cite this version:

Nellie Francezon, Ariane Tremblay, Jean-Luc Mouget, Pamela Pasetto, Lucie Beaulieu. Algae as a Source of Natural Flavors in Innovative Foods. Journal of Agricultural and Food Chemistry, 2021, 69, pp.11753-11772. 10.1021/acs.jafc.1c04409. hal-05261901

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# Algae as a Source of Natural Flavors in Innovative Foods

Nellie Francezon, Ariane Tremblay, Jean-Luc Mouget, Pamela Pasetto, and Lucie Beaulieu*

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Cite This: *J. Agric. Food Chem.* 2021, 69, 11753–11772

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**ABSTRACT:** As a result of their nutritive values, algae have been used as a food resource for centuries, and there is a growing interest to use them as enrichment ingredients in food products. However, food product acceptance by consumers is strongly linked to their organoleptic properties, especially the aroma, taste, and a combination of the two, flavor. With regard to edible algae, “fresh seashore”, “seafood-like”, “cucumber green”, and “earthy” are descriptors commonly used to define their aromas. Several families of molecules participate in the diversity and peculiarities of algal aromas: pungent sulfur compounds and marine halogenated components but also herbaceous fatty acid derivatives and fruity–floral terpenoids. In both macroalgae (seaweeds) and microalgae, these compounds are studied from a chemistry point of view (identification and quantification) and a sensorial point of view, involving sensorial evaluation by panelists. As a whole food, a food ingredient, or a feed, algae are valued for their nutritional composition and their health benefits. However, because the acceptance of food by consumers is so strongly linked to its sensorial features, studies have been performed to explore the aromas of algae, their impact on food, their evolution through processing, and their ability to produce selected aromas using biotechnology. This review aims at highlighting algal aromas from seaweed and microalgae as well as their use, their handling, and their processing in the food industry.

**KEYWORDS:** algae aromas, seaweed, microalgae, innovative food

## INTRODUCTION

Algae have been used as a food resource for centuries. Both phytoplankton (microalgae) and seaweed (macroalgae) have a long history of human consumption. Macroalgae are multicellular macroscopic aquatic plants, which belong to different taxons, Chlorophyta (green algae), Rhodophyta (red algae), and Phaeophyceae (brown algae). Their unicellular counterpart, microalgae, are distributed in a wider classification system, including genetically very different and non-exhaustively eukaryotic Chlorophyta, Euglenophyta, Bacillariophyta or diatoms, Haptophyta, Chrysophyta, and prokaryotic cyanobacteria (blue-green algae). The cyanobacteria *Spirulina*, nowadays marketed as Super Food in Occident, was already well-known by the ancient Aztec civilization and Chad populations.¹ Other cyanobacteria/microalgae, such as *Nostoc* spp., *Aphanotheca sacrum*, *Spirogyra*, and *Oedogonium*, were consumed as food or food supplement in Burma, Thailand, Vietnam, and India.¹ Seaweeds have a long tradition in Pacific (Indonesia, Philippines, Hawaii, and New Zealand) and Asian (China, Korea, and Japan) cultures, being a central ingredient in their daily cuisine.²

According to the Food and Agriculture Organization of the United Nations (FAO), the world production of algae has tripled from 2000 to 2018, reaching 32.4 million tonnes. This production is dominated by Asian and Southeast Asian countries, such as China (more than half of the worldwide production with 18.5 million tons), Indonesia, Korea, and Philippines. Some other countries around the world, such as Chile and Russia, were cited as major producers as well.³ Macroalgae represent the majority of the algae produced, with the main species being *Laminaria japonica* (Japanese kelp) at

11.5 million tons, *Eucheuma* spp. at 9.2 millions, *Gracilaria* spp. at 3.4 millions, *Undaria pinnatifida* (wakame) at 2.3 million, and *Porphyra/Pyropia* spp. (nori) at 2.0 million.³ On the other hand, microalgae farming was reported to an understated volume of 87 000 tonnes, with *Spirulina* being the most produced.

As a result of their healthy nutritive properties, algae raised interest as enrichment ingredients in processed foods but also as an improved diet for breeding. Their incorporation into food products would benefit from their high protein contents and their richness in minerals, vitamins, dietary fibers, and polyunsaturated fatty acids.² Whatever the nutritional value of food products, their acceptability depends upon consumer cognitive experiences and expectations and also organoleptic properties, of which the perception results from complex interactions of different senses. Indeed, for taste perception, there are four basic traditional tastes identified, bitterness, saltiness, sweetness, and sourness, with their appreciation relying on receptors on different parts of the oral cavity. Some algae can bring bitterness from some protein-derived peptides, saltiness from their high mineral contents (e.g., Na and K), and sweetness from their soluble sugars (e.g., mannitol). Furthermore, algae are known for being the representant of the fifth taste, the umami taste,⁴ mainly provided by the free

Received: July 21, 2021

Revised: September 18, 2021

Accepted: September 19, 2021

Published: October 1, 2021

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<table><caption>Table 1. Some of the Main Aroma Compounds of Algae, with Their Odor Threshold and Olfactory Descriptors<sup>11-13 a</sup></caption><thead><tr><th>Chemical family</th><th>Compound</th><th>Odor threshold</th><th>Aroma descriptors</th></tr></thead><tbody><tr><td rowspan="2">Sulfur compound</td><td>H<sub>3</sub>C-S-CH<sub>3</sub><br>dimethyl sulfide</td><td>0.3 - 10 µg/L</td><td>sulfur-cabbage, cooked-onions, boiled-potatoes, fishy</td></tr><tr><td>H<sub>3</sub>C-SH<br>methanethiol</td><td>0.02 - 4 µg/L</td><td>sulfurous, cabbage</td></tr><tr><td rowspan="6">Fatty unsaturated aldehyde</td><td>H<sub>3</sub>C-<br>hexanal</td><td>4 - 23 µg/L</td><td>fatty, green, grassy, fruity</td></tr><tr><td>H<sub>3</sub>C-<br>(2E)-octenal</td><td>3 - 4 µg/L</td><td>green leafy, also described as seaweed</td></tr><tr><td>H<sub>3</sub>C-<br>(2E)-nonenal</td><td>0.1 µg/L</td><td>fatty, green, waxy</td></tr><tr><td>H<sub>3</sub>C-<br>(2E,6Z)-nonadienal</td><td>0.01 µg/L</td><td>cucumber, green, fresh</td></tr><tr><td>H<sub>3</sub>C-<br>(2E,4E)-decadienal</td><td>0.07 - 10 µg/L</td><td>rich fatty, creamy aldehydic, sweet</td></tr><tr><td>H<sub>3</sub>C-<br>cubenol</td><td>100 - 250 mg/L *</td><td>spicy, fruity, green tea</td></tr><tr><td rowspan="7">Terpenoid</td><td>H<sub>3</sub>C-<br>geosmin</td><td>0.004 - 0.010 µg/L</td><td>earthy</td></tr><tr><td>H<sub>3</sub>C-<br>methyl-isoborneol</td><td>0.004 - 0.010 µg/L</td><td>earthy-musty</td></tr><tr><td>H<sub>3</sub>C-<br>α-ionone</td><td>0.4 - 3 µg/L</td><td>warm, woody, berry, violet-like, powdery nuance</td></tr><tr><td>H<sub>3</sub>C-<br>β-ionone</td><td>0.007 - 0.03 µg/L</td><td>characteristic violet-like, very woody, fruity</td></tr></tbody></table>
<table><caption>Table 1. continued</caption><thead><tr><th>Chemical family</th><th>Compound</th><th>Odor threshold</th><th>Aroma descriptors</th></tr></thead><tbody><tr><td rowspan="4">Halogenated compound</td><td>2-bromophenol</td><td>0.17 µg/L **</td><td>marine, fishy, sea-food</td></tr><tr><td>2,4-dibromophenol</td><td>4 µg/L **</td><td>phenolic, medicinal</td></tr><tr><td>2,6-dibromophenol</td><td>0.0005 µg/L **</td><td>iodine, seafood</td></tr><tr><td>2,4,6-tribromophenol</td><td>0.6 µg/L **</td><td>iodine, shrimp-like, seafood, sea-salt like</td></tr></tbody></table>

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amino acid glutamic acid. In addition, algae have very characteristic aromas, odors, or smells conveyed by volatile compounds. They are detected through respiration via the orthonasal olfaction route by the olfactory perception. “Flavor” is a perception involving the sense of smell through the retronasal olfaction route. First, the odor molecules are released from food or drink in the oral cavity, and then they travel to the nose and the olfactory receptors to be detected.⁵ Without retronasal olfaction, we would be unable to experience flavor, in the same way as food feels bland when we catch a cold. Therefore, flavor is considered as a combination of olfaction and taste.

From a long tradition in Asia to a recent trend in Western countries, several science-based and gastronomical developments involving algae have flourished.⁶,⁷ A dedicated word “phycogastronomy” was even created to promote algae cuisine.⁸ To further understand the contribution of algae into foods, this review aims at presenting the diversity and peculiarities of algal aromas from their harvest to their consumption, with a focus on the sense of smell. The impact of algae processing on the aromas, the influence of algae on food aromas, and the sensory challenge of their incorporation into food products will be discussed. Moreover, the progress of aroma production using living microalgae will be presented.

## ALGAL AROMA CHEMISTRY

The aroma and flavor diversity of algae depends upon the mixture of volatile compounds, their relative concentration, and their respective contribution to the overall sensory

perception. Some volatile compounds strongly define seaweed odors; they are “character-impact compounds”. Some others participate in the richness and complexity of aromas. Several classes of molecules, covering a wide range of scents, are represented in algae. They are described in detail hereafter with their occurrence in various algal species. Another key element in olfactory impact of a molecule is its odor threshold. Odor threshold is the minimum concentration of which 50% of a human panel can detect the presence of an odor or odorant without characterizing the stimulus. The lower the odor threshold, the more impact the compound has in the whole aroma. Some odor thresholds found in the literature are presented in Table 1 for some volatile compounds found in algae. Moreover, an aroma wheel dedicated to algal aromas is proposed in this review (Figure 1). Inspired by the early work of Sugisawa et al. on the green seaweed *Ulva pertusa*⁹ and Larssen et al. on marine oils,¹⁰ this aroma wheel was elaborated from all of the descriptors used for algae aromas collected in this literature review. It could be a useful tool for sensory evaluation of algae.

**Sulfur Compounds.** Sulfur compounds are very characteristic of algal smells, conveying a vast array of odors, from a “fresh seashore” atmosphere to offensive sulfuric odor of decaying seaweeds. Dependent upon their concentrations and their structural peculiarities, sulfur compounds can be overpowering odoriferous components. One of the most widespread sulfur molecules in algae is dimethyl sulfide (DMS). Its odor, described as “sulfur–cabbage” with “cooked onions” and “boiled potatoes” notes, also has a very “fresh seashore” smell in small amounts. The very volatile DMS has a

<footnote>a*, in ethanol; **, in water.</footnote>
<figure><img src="image_13.png" /><figcaption>**Figure 1.** Algal aroma wheel.⁹,¹⁰</figcaption></figure>

low odor threshold,¹⁴ which makes it a great contributor to algal aromas, even at low concentrations (Table 1). Released in the marine environment by algae, DMS contributes to the global sulfur cycle and climate regulation. DMS is produced by enzymatic reaction from its precursor, dimethyl sulfoniopropane (DMSP). DMSP accumulates in algal cells and is responsible for osmoregulation.¹⁵ Its degradation in DMS is a natural process in living algae but also a marker of cell death, because enzymatic degradation of DMSP occurs after lysis of the cells. Although this degradation is a natural process, DMS release can be caused by crushing the algae⁹ or even being artificially produced by thermal decomposition. Among seaweeds, DMS is ubiquitous; however, some phyla are greater producers, such as green macroalgae (Chlorophyta), characterizing their odor profile to a great extent.¹⁶ For example, for *Enteromorpha* sp., the DMS content can reach 5.8 mg/L and the DMSP content can reach 450 mg/L, whereas brown and red seaweeds contain from 10 µg/L to 1 mg/L.¹⁶ A very high level of DMSP (6977 mg/L) was reported in the green seaweed *Ulva lactuca*.¹⁷ Karsten et al. reported green seaweeds *Acrosiphonia arcta*, *Ulva lactuca*, and *Enteromorpha bulbosa* having the highest DMSP content, 150–300 times higher than other seaweeds. However, some representatives of red algae, such as *Polysiphonia*,¹⁸ have a significative amount of DMSP in their cells, equaling the green algae content. Another red alga, *Porphyra* sp., better known as nori, possesses DMS and other sulfuric compounds.¹⁶

Among microalgae, the DMS precursor is abundantly produced by Prymnesiophyceae and Dinophyceae.¹⁵,¹⁹ It is worth mentioning that DMSP production in unicellular algae was evidenced for the first time with obtaining a DMSP crystal from the dinoflagellate microalgae *Cryptothecodinium cohnii*.¹⁹ Benthic diatoms are considered intermediate DMSP producers, with the amount varying with their growth phase. Kasamatsu et al. evidenced that the DMSP content of *Navicula* sp. and *Nitzschia* sp. gradually increased during the stationary growth phase.²⁰ DMS was also detected as the highest volatile organic compound (VOC) in five microalgae strains, ranging

from 0.7 mg/L for *C. cohnii* (dinophyceae) to 0.3–0.2 mg/L for *Chlorella vulgaris*, *C. protothecoides*, *Tetraselmis chuii*, and *S. limacinum*.²¹ Contrarily, cyanobacteria are not specific emitters of DMS,¹⁵ because none was detected in the headspace of living strains of *Spirulina*, *Anabaena*, and *Nostoc*.²² However, other sulfuric compounds, alkane thiols, such as methanethiol and isopropylthiol, are known malodorous VOCs produced by cyanobacteria.²³ Methanethiol is a degradation product of methionine and can be further degraded to sulfides. It possesses a “cabbage-like” note and participates in flavor intensity.¹⁴ More complex sulfuric compounds are cyclic polysulfides. They are rare in nature,²⁴ but their unusual structure and their pungent unpleasant sulfur odor are worth mentioning, especially because they were identified in algae. Two members of the *Dictyopteris* genus (*D. plagiogramma* and *D. australis*) have been reported to contain a cyclic disulfide 3-hexyl-4,5-dithiacycloheptanone, naturally derived from an acyclic trisulfide.²⁵ Another sulfured odoriferous macroalga, *Chara globularis*, produced two compounds with a 1,2-dithiolane ring system.²⁶ The red algae *Chondria californica* display a wide range of cyclic sulfured compounds with antibacterial activity.²⁷ Original cyclic structures were elucidated, from trithiolane to a 12-membered heterocycle with eight sulfur atoms. To the best of our knowledge, no microalga was reported to produce cyclic polysulfide.

**Unsaturated Fatty Aldehydes.** Fatty aldehydes are long-chain aldehydes derived from polyunsaturated fatty acids (PUFAs), by either auto-oxidation or enzymatic degradation by lipoxygenase. Aldehydes contribute notably to algae aromas because their odor threshold is very low.²⁸ They convey desirable fresh-green to fatty-green odor for the $C_6-C_9$ aldehydes and typical marine-seaweed smell for $C_{15}-C_{17}$ aldehydes.⁹ The diversity of the number of carbon atoms and the degree of saturation lead to a wide range of green aroma variations, hexanal (grassy, green), (2E)-octenal (seaweed), (2E)-nonenal (fatty-green, waxy), (2E,6Z)-nonadienal (cucumber), and (2E,4E)-decadienal (fatty rich, sweet),¹⁶ and also contribute to other notes (woody, fatty, nutty, floral, citrus, waxy, and sweet).²⁸ A range of other compounds, including carboxylic acids, alcohols, and ketones, are derived from the same PUFA degradation phenomenon, having different impacts on algal aromas as a result of their odor threshold value and volatility.²⁹

Algae share these volatile compounds with terrestrial plants, because the green odor of green leaves was described to come from $C_6$ volatile compounds, including (Z)-3-hexenol, also called “leaf alcohol”, and (E)-2-hexenal, “leaf aldehyde”.³⁰ Among seaweeds, fatty aldehydes are very characteristic of green seaweed aromas. Sensory evaluation by gas chromatography–sniffing (GC–sniffing) of green seaweed *Ulva pertusa* volatile compounds revealed that, while representing 54% of the total volatile composition, aldehydes contributed to 77% of the total odor.⁹

Studies on several microalgae revealed that unsaturated-fatty-acid-derived aldehydes highly contributed to their aroma profiles, especially for those with a high lipid content. Microalgae are quite rich in PUFAs, very long-chain PUFAs, such as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), in marine microalgae mostly, whereas freshwater *Chlorella* contain mostly shorter PUFAs, such as α-linolenic acid. *Botryococcus braunii* and *Rhodomonas* sp. microalgae with high contents of PUFAs and total lipids were reported to contain high levels of aldehydes (71.2 and 33.9 µg/g,
respectively) compared to others, such as marine *Tetraselmis chuii* and *Nannochloropsis oculata*, with low lipid contents.²⁸ *Chlorella vulgaris* was reported with short-chain aldehydes and ketones, having very characteristic $C_5$ compounds. Microalgae *Cryptothecinium cohnii* and *Schizochytrium limacinum*, which have been used to produce DHA, were demonstrated to contain high amounts of saturated and unsaturated aldehydes.²¹ In comparison, a few aldehydes were detected in *C. protothecoides*, *C. vulgaris*, and *Tetraselmis chuii*.

Other classes of compounds can be produced from the lipid degradation process, such as alcohols, ketones, and alkenes. A long-chain polyene, (6Z,9Z,12Z,15Z)-henicosapentaene, was identified from brown algae *Undaria pinnatifida* and *Sargassum thunbergii*.³¹,³² This compound was described with a subtle marine aroma, very characteristic of dried wakame. Other very odoriferous polyenes, short-chain polyenes "dictyopterenes", are characteristic molecules from brown algae of the *Dictyopteris* genus. Associated with an "ocean smell",¹⁶ these molecules (dictyopterene A, dictyopterene B, dictyopterene C', and dictyopterene D') are major compounds in the essential oils of *D. prolifera* and *D. undulata*³³ and Hawaiian *D. plagiogramma* and *D. australis*.³⁴ Dictyopterene D' is also known as ectocarpene, because it was first isolated from the brown alga *Ectocarpus siliculosus*. Produced by the lipoxygenase pathway from unsaturated fatty acids,³⁵ the dictyoperenes are $C_{11}$ and $C_8$ polyunsaturated open-chain or cyclic hydrocarbons, which act as pheromones in the reproduction cycle of brown algae.³⁶ Pohnert and Boland described, in a complete review, the 12 pheromones and structural isomers identified to date in brown algae as well as the species that produce them.³⁷ These peculiar compounds are also produced by unicellular algae, especially by diatoms. The diatoms *Skeletonema costatum* and *Lethodesmium undulatum*, under optimized growing condition cultures (intense light), produce ectocarpene.³⁸ Other cultures of the species of these genera were tested, but no ectocarpene could be isolated, even if their smell was characteristic of it.³⁸ Ectocarpene and dictyopterene C' were reported to have a caraway seed fragrance with a pungent note.³⁹ One should note that ectocarpene was detected in the emitted odor of ripening mango and pineapple.⁴⁰

**Terpenoids and Norisoprenoids.** Terpenoids are a wide family of secondary metabolites, with compound categories related to their carbon number. Among them, monoterpenes ($C_{10}$) and sesquiterpenes ($C_{15}$) are odoriferous volatile compound classes, mainly found in terrestrial plant essential oils. Other classes, such as diterpenes ($C_{20}$), sesterterpenes ($C_{25}$), triterpenes ($C_{30}$), and tetraterpenes ($C_{40}$), are non-volatile compounds, which play key roles in the metabolism of living organisms. Isoprene, composed of five carbons, is the simplest terpenoid. It is also the precursor of all of the other compounds in this wide family. Being very volatile, isoprene is not usually detected in VOC extracts but can be measured in *vivo* using headspace gas chromatography/mass spectrometry in algae.¹¹ Although isoprene contributes to ocean-atmosphere chemical equilibrium, it participates in aroma production in algae as a building block for monoterpenes, sesquiterpenes, and other terpenoid derivatives. Monoterpenes have more impact than sesquiterpenes on algal aromas because they are more volatile and have a lower odor threshold.¹⁴

Several very common monoterpenes from terrestrial plants were reported in microalgae, such as α-pinene, δ-limonene, eucalyptol,³⁹ linalool, and geraniol in *Chlorella vulgaris*⁴² and sylvestrene and thujone in *Spirulina platensis*,⁴³ but also in

macroalgae, such as α-pinene, δ-limonene, carvone, α-terpineol, terpinolene, cadinene, 1,8-cineol, linalool, ocimene, geraniol, myrcene, and cadinol.¹⁶ Even if they do not represent characteristic algal aromas, they play their part in the mixture, giving floral, fruity, or woody notes. The sesquiterpene cubenol is present in a high content in some brown algae, such as wakame (*Undaria pinnatifida*) and kombu (*Laminaria japonica*). Its content can even reach 95% of the essential oil extracted from the kelp *Dictyopteris divaricate*.³³ Finally, as very characteristic terpenes from algae, the earthy-muddy-moldy-musty geosmin and methylisoborneol are worth mentioning. The sesquiterpenoid geosmin is a characteristic compound of actinobacteria and cyanobacteria. While its earthy odor is associated with the poetic "smell of rain" or the smell of wet soil, it is also known as a malodorous aquatic pollutant. Indeed, together with the monoterpenoid methyl-isoborneol, they are responsible for the undesirable off-flavor of water and seafood, with very low odor thresholds (4–10 ng/L).²³ More than 20 cyanobacterial strains were studied by Persson, and an earthy-musty odor was quasi-systematically used to define the algal odor, which was attributed to methylisoborneol and geosmin.⁴⁴ Methylisoborneol was also detected in cyanobacteria *Nostoc*, *Anabaena*, and *Spirulina*.²² Cyanobacteria are probably the only algae able of producing such compounds.²³

In the terpenoid family, other volatile compounds can be produced from the degradation of tetraterpene carotenoids. Carotenoids are pigments present in algae at different levels. In algae, the most prominent carotenoid is β-carotene. Its high level can be found in almost every phylum (except in *Cryptophyta* and *Dinophyta*), leading to a wide range of xanthophyll derivatives.⁴⁵ Its isomer α-carotene and derivatives have a distribution limited to *Rhodophyta* (macrophytic type), *Cryptophyta*, *Euglenophyta*, *Chlorarachniophyta*, and *Chlorophyta*.⁴⁵ The cleavage of carbon-carbon double bonds on the polyene chain of carotenoids results in various odoriferous volatile compounds, called norisoprenoids. These norisoprenoids are 9–13 carbon compounds, with an aromatic cycle originating from the cyclic ends of the carotenoid. Dioxygenases are responsible of these cleavages.⁴⁶ Notable odoriferous norisoprenoids in algae are α- and β-ionones, which display floral, violet-like scents with a woody note for the β isomer. They are well-known and valuated in terrestrial plant essential oils. α-Ionone is a specific degradation product of α-carotene extremity cleavage, whereas β-ionone can result from both α- and β-carotene end cleavage. Another derivative of ionone, such as 3-hydroxy-β-ionone, can be produced from the degradation of other carotenoids. Another norisoprenoid, β-cyclocitral, participates in the odoriferous profile of algae, having a fruity tropical aroma with a tobacco-like note. These compounds have a low odor threshold, making them great contributors to algal aroma. A review on algae volatile compounds¹⁶ reported the presence of β-ionone as a characteristic odor compound in brown seaweeds as well as β-cyclocitral and dihydroactinidiolide (in nori-type red algae). Indeed, they were reported as potent flavor compounds in wakame *Undaria pinnatifida*.⁴⁷ Among microalgae, ionones and β-cyclocitral were measured in *Chlorella*, *Tetraselmis*, *Botryococcus*, and *Rhodomonas*, with the latter containing a remarkable concentration of α-ionone (1400 ± 290 ng/g).²⁸ This concentration of α-ionone might be explained by the high α-carotene content of *Rhodomonas* which belongs to the *Cryptophyta* phylum, known to be devoid of β-carotene and a
high producer of the α isomer.⁴⁵ *Dunaliella salina* and *Dunaliella bardawil* are green microalgae that can produce high levels of β-carotene in controlled photobioreactor cultures.⁴⁸,⁴⁹ α- and β-ionone as well as β-cyclocitral were detected in the *D. salina* aroma profile,⁵⁰ but it is still unclear whether living microalgae produce norisoprenoids or if it is a result of carotenoid cleavage during extraction processes.⁵¹ The same observation was made for the steam-distilled essential oil of the green alga *Capsosiphon fulvescens*, whose major compound is β-ionone.²⁹ However, these observations led to the hypothesis that a high content of norisoprenoids could be obtained from high-content carotenoid algal species if a suitable treatment process is applied. Additionally, cyanobacteria were reported to contain notable levels of norisoprenoids as well. *Nostoc*, *Spirulina*, and *Anabeaena* strains contained 1.15–2.72% β-ionone and 0.20–1.34% β-cyclocitral.²²

**Halogenated Compounds.** Halogenated compounds are very specific to marine organisms. Contrary to terrestrial plants, algae can produce these compounds thanks to their direct access to halides in the seawater and their specific enzyme system of vanadium haloperoxidases.⁵² Therefore, the contribution of halogenated volatile compounds is characteristic of the sea-like flavors. A lot of halogenated volatile molecules have been reported in algae, and *ortho*-substituted halogen compounds are known to interact strongly with human odor receptors, resulting in high odor intensity.⁵³ However, little information is available on their real contribution to seaweed aromas as a result of the restriction of the use of halogen-containing compounds as flavoring agents.¹⁶ Volatile halogenated compounds are known to contribute to taints in foodstuffs as contamination originating from their extensive use as sanitizers and pesticides.⁵⁴ However, the marine environment is a natural producer of organohalogens, especially algae.

Green, brown, and red macroalgae produce a wide range of halogenated compounds, but red seaweeds (Rhodophyceae) stand out for the incredible diversity and abundance of their halogenated secondary metabolites. The essential oil of *Asparagopsis taxiformis*, a highly appreciated red alga in Hawaii for its flavor and aroma, has been reported to contain at least 42 bromine and iodine compounds, ranging from simple haloforms, such as CH₃Br, to more complex halogenated aldehydes and ketones.⁵⁵ Halogenation of compounds can indeed occur on a wide range of secondary metabolites, such as short-chain hydrocarbons, terpenes, and phenols, via the action of haloperoxidases.¹² Vanadium haloperoxidases are key enzymes involved in the biosynthesis of organohalogens. There are three of them, with different specificities: the chloroperoxidases, which can oxidize three different halides (chloride, bromide, and iodide), the bromoperoxidases for bromide and iodide, and the iodoperoxidases (VIPO), specific to iodide. Brominated and chlorinated sesquiterpenes were reported in the red algal genus *Laurencia* as well as several furanones.⁵⁶ Bromophenols are produced by Bacillariophyceae, Cyanophyceae, Rhodophyceae, and Chlorophyceae.¹² Bromophenols, for example, impart a very marine seafood-like aroma, especially monobromophenols. Dibromophenols have a more phenolic medicinal aroma. At a higher concentration, they can be associated with off-flavors (see the Impact of an Algal Diet on Seafood Aromas section). *Laminaria digitata*, a brown seaweed, is known to accumulate high amounts of iodine (known for its odor of sea air)⁵⁷ and to produce methyl

iodine.⁵⁵ Four iodides, 2-iodopropane, 1-iodopropane, 1-iodopentane, and 1-iodooctane, were also isolated from *Laminaria* spp.⁵⁸ Fluoride- and iodide-containing compounds are quite unusual compared to chlorinated and brominated compounds in marine organisms.⁵⁹ This explains the little information on their contribution to the aromas of food.¹² Contrary to seaweeds, microalgae are predominant producers of halomethanes, such as red *Porphyridium purpureum*, green *Dunaliella tertiolecta*, diatoms *Porosira glacialis*, *Nitzschia* sp., *Odontella mobiliensis*, *Phaeodactylum tricornutum*, and *Thalassiosira weissflogii*, and prymnesiophytes *Isochrysis galbana* and *Phaeocystis* sp.⁶⁰⁻⁶² In addition, cyanobacterial blooms revealed the massive contribution of cyanobacteria to the overall emission of halomethanes.⁶³ In contrast, only a few structurally more complex volatile organohalogens have been reported from phytoplankton.⁶²

## AROMA BIOTECHNOLOGIES USING MICROALGAE

Microalgae biotechnology is nowadays widely developed to produce non-volatile high-value-added molecules. For example, green algae *Dunaliella salina* is industrially grown worldwide (about 3000 tons/year) for the production of β-carotene, along with *Haematococcus pluvialis* (about 700 tons/year) for astaxanthin and *Cryptothecodinium cohnii* and *Shizochytrium* for ω-3 fatty acid DHA.¹ Many advantages are associated with microalgae biotechnology: these organisms are robust, versatile, and able to grow fast, possibly in harsh conditions, and their photoautotrophic nature avoids furnishing carbonated substrates for their growth. In comparison to their macroalgae counterpart, microalgae can grow in photo-bioreactors, with controlled conditions. However, their greatest advantage, as for other microorganisms, is their capacity of producing compounds of interest, under mild reaction conditions, that are considered as “natural”⁶⁴ with regio- and stereoselectivity, avoiding further complex purification processes. Indeed, stereochemistry is a key element in odoriferous compounds, because two isomers can smell totally different. For example, D-limonene [or (+)-limonene] produced by the *Citrus* family displays a sweet citrusy scent, whereas its enantiomer L-limonene [or (−)-limonene], found in conifers, smells terpenic and piney. Microorganisms offer two options for the production of targeted compounds: the *de novo* synthesis, involving the catabolism of macromolecules (proteins, fats, and carbohydrates) in smaller molecules, and the biotransformations/bioconversions, which are modifications of a compound to a structurally similar compound.⁶⁵

Production of volatile compounds useful to the food flavoring can be achieved with intact or genetically modified plants. However, the low yields obtained cannot compete with the synthetically tailored molecules. Flavors are considered as food additives by the U.S. food regulation. As for all food additives, growing concerns by consumers about the natural origin of these added compounds encouraged the development of natural alternatives using biotechnology. Biotransformation of volatile compounds has been widely studied for microorganisms (bacteria, yeasts, and molds), and very efficient models were developed.⁶⁶⁻⁶⁸ Thus, research investigated opportunities in genetic engineered microalgae. Some of them were successfully modified to enhance the production of targeted compounds. *D. salina* and *H. pluvialis*, already industrially used for their natural carotenoid high production capacity, were genetically modified to increase their production of violaxanthin, zeaxanthin, and astaxanthin.⁶⁹,⁷⁰ Several others
had been studied (e.g., *Chlamydomonas reinhardtii*, *Nannochloropsis* sp., *Phaeodactylum tricornutum*, *Porphyridium* sp., and *Chlorella* sp.).<sup>71</sup> To date, none of them is dedicated to the production of a specific volatile compound.

**Biotransformation of Ionones.** The two isomers α- and β-ionone are odoriferous compounds with pleasant violet scents and extremely low odor thresholds (0.4–3.2 µg/L for α-ionone and 0.03–0.007 µg/L for β-ionone.<sup>72–74</sup> They are of commercial importance, valued in several fields, including cosmetics and perfumeries. For instance, α-ionone worldwide use ranges from 100 to 1000 tons per year.<sup>72</sup> Ionones are produced by the breakdown of carotenoids either enzymatically or chemically. The latter includes photo-oxygenation, auto-oxidation, and thermal degradation, and the former involves carotenoid cleavage by dioxygenases and other enzymes,<sup>73</sup> which can be used either exogenously or directly into the carotenoid-producing cells.

Yeasts and molds are yet better producers of ionones than microalgae. For example, a lycopene-overproducing *Escherichia coli* strain produced unprecedented yields of α-ionone (480 mg/L) and β-ionone (500 mg/L).<sup>75</sup> Coupled with an efficient purification process, it led to industrially viable ionone production.<sup>72,76</sup> Studies have investigated generally recognized as safe (GRAS) microorganisms, which can reach food regulations and safety, such as the yeasts *Saccharomyces cerevisiae* or *Yarrowia lipolytica*.<sup>31,77,78</sup> Even if effective, these bioengineered models require the addition of several exogenous enzyme genes through plasmids in the host genome to reconstruct the α-ionone pathway. It implied to first stimulate the mevalonate pathway to produce lycopene and carotene and then to cleave them to obtain ionones. Some algae, such as *Dunaliella salina* and *Dunaliella bardawil*, are naturally high producers of carotenoids;<sup>48,49</sup> therefore their use as new models can be raised. Unfortunately, as recently demonstrated by Liang et al., β-ionone and β-cyclopitral (another product of carotenoid cleavage) inhibit the growth of *Dunaliella*.<sup>79</sup> Therefore, it was demonstrated that it does not seem feasible to further engineer *Dunaliella* cells to produce high levels of β-ionone. In the same way, growth inhibition of other microalgae, *Anabaena*, *Synechococcus*, *Nannochloris*, and *Cyanidium*, was reported in the presence of some norisoprenoids.<sup>80</sup> Moreover, several cyanobacteria (*Microcrystis*, *Calothrix*, *Plectonema*, *Nostoc*, *Phormidium*, and *Synechocystis*) were investigated for the activity of their carotenoid cleavage oxygenase, but none was highlighted yet as an interesting biotechnological model.<sup>73</sup>

**Biotransformation of Monoterpenes.** Specificities of microorganism enzymes, such as oxyfunctionalization (integration of oxygen in a selective manner), are of great importance for aroma biotechnology. Whereas tons of low-value terpene hydrocarbons from plant essential oils are discarded each year, it would be possible to convert them into their oxygenated metabolites with higher aromatic value.<sup>64</sup> Studies on microalgae abilities of transforming common monoterpenes, such as (R)-(+)-carvone, *D*-(+)-limonene, (+)-β-pinene, thymol, (+)-linalool, (−)-menthone, (+)-pulegone, (−)-fenchone, and (−)-piperitone, were assessed on *Chlorella* sp., *Oocystis* sp., *Synechococcus* sp., and *Chlamydomonas* sp.<sup>81–83</sup> Some microalgae were able to reduce double bonds and ketone groups and to oxidize in a site- and regioselective manner.

**Biotransformation of Vanillin.** The most famous single flavor, vanillin, is a principal target for flavor biotechnology.<sup>64</sup>

Indeed, vanillin obtained biotechnologically from microorganisms is labeled “natural vanillin” according to U.S. and European legislation,<sup>84</sup> and it has been available on the market for more than a decade. This “biovanillin” can compete with the dominating synthetic vanillin, surfing on the wave of natural products. Microbial bioproduction of vanillin has been widely investigated; several native or modified bacterial and fungal strains have been reported to produce vanillin from eugenol, isoeugenol, or ferulic acid precursors.<sup>84–89</sup> Research on vanillin biosynthesis in microalgae and cyanobacteria has not yet been widely explored. However, a study on the green alga *Haematococcus pluvialis* immobilized cells revealed the possibility of producing vanillin from ferulic acid.<sup>90</sup> This microalga has already been a biotechnological target, being the producer of the carotenoid astaxanthin. The concept of producing several different added-value compounds from the same microalga has already been raised, from the observation that biofuel single production from microalgae might not be industrially profitable.<sup>91</sup>

<figure><img src="image_14.png" /></figure>

## ALGAL AROMAS IN FOOD PRODUCTS

**Influence of Food Processing on Algae Aromas.** With their very high moisture content, algae are perishable food that require preservation processes to improve their shelf life. Most of the research studying the impact of treatments on algae concerns the preservation of nutritional properties, such as the protein and amino acid contents, the lipid loss, or the microbial spoilage.<sup>92,93</sup> Few works explored the impact of preservation of algal aromas, even though the sensory characteristic of a food product, especially odor, is of capital importance for consumer acceptance.

As they grow in a salted environment, seaweed can easily be stored in saline water at low temperatures after harvest. The influence of storage conditions on the odor of *Palmaria palmata* was studied: frozen seaweed was compared to fresh seaweed preserved in artificial seawater. Algae in seawater were described as seaside, fresh, seaweed, and iodized, whereas frozen algae (thawed for evaluation) were associated with green odors (cut grass, tea, or hay).<sup>94</sup> Even if seaweed preserved in seawater may undergo microbial alteration, it seemed to preserve its original aroma. Indeed, the freezing process causes cell lysis, which, during thawing, induces the liberation of intracellular enzymes, such as lipoxygenases. These enzymes would then easily produce volatile compounds from fatty acids (ketones, alcohols, and aldehydes) with characteristic green aromas.<sup>94</sup> Similarly, the crushing of algae resulted in a modification of algal aromas with the release of enzymes.<sup>95</sup> This could develop the green aromas of algae as well as a sulfur-cabbage smell with the release of DMS from its precursor, depending upon the seaweed species. Indeed, Nayyar and Skonberg demonstrated a species specificity on the aroma changes while studying the storage temperature and time for two seaweeds *P. palmata* and *Gracilaria tikvahiae*.<sup>96</sup>

A traditional method for preserving seaweed is drying. Being the preferred method for stabilizing seaweed for long-term storage, drying retards microbial growth, helps preserve desirable qualities, and reduces storage volume. Several drying techniques are commonly used in algal processing: solar drying, hot air drying, freeze drying, vacuum drying, and spray drying.<sup>97</sup> Commonly marketed as dried products, seaweeds are then directly rehydrated for consumption or used as ingredients in dishes. Drying pretreatment can be used, such as blanching, which limits component degradation and lowers
energy consumption. For instance, no significant change of flavor or aroma of the seaweed *Kappaphycus alvarezii* was reported when blanched before drying.⁹⁸ Some drying parameters, such as the temperature, can affect specific compounds (lipids, proteins, pigments, and phenolic compounds)⁹⁹ and, thus, sensory properties. However, a comparison between freeze drying and air drying in the temperature range of 25–70 °C resulted in equally nutritious products with similar flavor and aroma properties.⁹⁹ Volatile compounds and odors of seven 46–48 °C dried seaweeds were reported with preserved “seaweed”, “hay”, “marine”, and “seafood” odors.¹⁰⁰ Semi-drying [moisture content (MC) of 20%] was compared to drying (MC of 6%) on *P. palmata* and resulted in a fading of the characteristic marine flavors and a development of “hay” and sweet odors.¹⁰¹ Traditionally in Japan, the best quality kombu (*Saccharina japonica*) is sun-dried and aged in cellars for 1–10 years.⁴ This process, known to improve umami taste, can fade the strong undesirable marine aroma. Similar maturation techniques were reported in Iceland.¹⁰¹ The drying process has indeed an impact on the composition of volatile compounds of algae. For example, fresh wakame essential oil is composed of a high content of the terpenoid cubenol (88%),¹⁰² conveying a fruity tone. After traditional drying and salting, the essential oil of processed wakame was devoid of cubenol but presented a much heavier molecule, (6Z,9Z,12Z,15Z,18Z)-henicosahexaene, as the major compound and major aroma contributor.³¹

Fermentation is an ancient technique for the preservation of perishable foods, notably food with a high moisture content. It also improves the taste and texture of food as well as their safety (reducing harmful metals, such as Cd and Hg)¹⁰³ and shelf life. As a wet product, seaweeds are commonly dried, but fermentation is an option for innovation in novel seaweed products. Fermentation can be used to refine sensory properties of seaweeds, by attenuating some undesirable odors. Indeed, lactic acid bacteria fermentation was reported to soften the strong sea smell of sugar kelp (*Saccharina latissima*), originating from DMS and other sulfides.¹⁰³ Fermentation of *Laminaria japonica* with *Aspergillus oryzae* helps remove off-flavors by reducing the odor intensity of the seaweed.¹⁰⁴ Fermentation also changes the taste of algae because it induces the release of amino acids.¹⁰⁵ Finally, the cooking of algae was investigated for evaluating the change of *Ulva rigida* aromas.¹⁰⁶ It appeared that the main sensory modifications took place during the first minutes of cooking and at medium cooking temperatures, with a decrease of the “seaside and seaweed” characteristic volatile compound contents and an increase of the “cooked fish, salty dry fish, and crustacean” characteristics.

Preserving the original aromas, controlling the changes at each step of processing, selecting desirable aromas, and being able to guarantee reproducibility are some useful impacts of the studies on the evolution of algal aromas from harvest to dishes.

**Impact of an Algal Diet on Seafood Aromas.** Food quality and taste are directly linked to their environment. Pollution, intensive farming, and feed grade are known to alter nutritional and organoleptic properties of food. By extension, the characteristics of the feed can greatly influence the aroma of food. Highlighted for their excellent nutritional composition (e.g., their high protein or polyunsaturated fatty acid contents), algae arouse interest in the enrichment of cattle feeding.¹⁰⁷ However, the marine and sea-like aromas of algal biomass are

not suitable for every meal. Several studies have evaluated the sensory impact of an algal diet to processed meat, and typical aroma of beef, chicken, and lamb meats was reported to be negatively altered.¹⁰⁸⁻¹¹¹ The fishy or rancid taints described in these meats were attributed to volatile lipid oxidation-derived compounds. Indeed, an algal diet rich in PUFAs influences the fatty acid composition of meat, of which, after cooking, will release unusual flavors.¹¹⁰ Eggs were reported to have a fishier aroma when enrichment with DHA from a microalgae diet was too high.¹¹² Although increasing PUFA levels in meat is nutritionally beneficial, it cannot compete with sensory quality for the consumer.¹⁰⁸ However, a low dosage might be of interest because recent studies reported no adverse impact of an algal diet (*Spirulina*, *Laminaria* spp., and *Cryptothecodinium cohnii*) on chicken, rabbit, and duck meat flavor.¹¹³⁻¹¹⁵

These algal diet “off-flavors” for meat may be more suitable to fish and seafood,¹¹⁶ although the risk of a taste negatively influenced by the abundance of algae in the diet also exists. Indeed, volatile compounds, such as (E)-2-nonenal, (E,Z)-2,6-nonadienal, and 3,6-nonadien-l-ol, derived from polyunsaturated fatty acids EPA and DHA display a characteristic aroma of cucumber and watermelon to the sweet smelt (*Plescoglossus* spp.), very appreciated by Koreans and Japanese.¹¹⁷,¹¹⁸ The flavor of freshwater-farmed barramundi (*Lates calcarifer*) fed with marine algae *Ulva ohnoi* was improved, having a rich and complex seafood aroma.¹¹⁹ Moroney et al. reported that 5% of *Ulva rigida* in the diet of farmed salmon improved the quality of the fillet without sensory alteration.¹²⁰ Another example of diet-acquired off-flavor is the iodine-like strong smell of saltwater seafood. Conveyed by a high concentration of bromophenols, this taint was reported in shrimp and fish.¹²,¹²¹ Microalgae, including *Bacillariophyceae*, *Cyanophyceae*, *Rhodophyceae*, and *Chlorophyceae*,¹² which are the primary producers of bromophenols, constitute the feed for marine crustaceans, molluscs, worms, and fish, and, therefore, influence their flesh aromas. At low concentrations, bromophenols impart very characteristic marine/seafood aromas, described as iodine-, shrimp-, crab-, and sea-salt-like.¹²² They are widely distributed in wild marine fish and seafood (contrary to their very low occurrence in freshwater fish) and, therefore, take a great part in their characteristic marine aromas.¹²³ It was also demonstrated that the bland flesh of cultured prawns was linked to the lack of these compounds.¹²⁴ Consequently, it was suggested that the parsimonious use of bromophenols in the diet of farmed species might improve the flavor of their meat.¹²³ Whitfield et al. tried to create a prawn feed enriched with bromophenols, but bromophenols were lost during the feed preparation process.¹²⁴ It appears that a bromophenol naturally rich microalgae diet, contained in the algal biomass, would be the best alternative to enhance cultured fish and seafood flavors.

A traditional diet-oriented cultivation is oyster refinement, a practice that aims to fatten oysters and improve their taste.¹²⁵ Refinement with different algal diets influences the sensory properties of oysters. These differences originated in the fatty acid profile of microalgae, which accumulate in lipids of oysters and then generate diverse volatile compounds through oxidation. Indeed, from 50 volatiles identified in the aromas of fresh oysters, 86% of them were related to fatty acid oxidation, including 66% related to ω-3 polyunsaturated fatty acid oxidation.¹²⁶ *Skeletonema costatum* and *Tahitian isochrysis*, commonly used microalgae in oyster-refining ponds, were
studied for their impact on the final aroma of oysters.¹²⁵⁻¹²⁷
Specific aroma compounds were identified, with 6-methyl-5-hepten-2-one (ether odor) being *S. costatum* characteristic and 3-nonyne (cucumber and marine odor), 6-(E)-nonen-1-ol (green and fresh odor), and 4-ethylbenzaldehyde (aniseed odor) being attributed to *T. isochrysis*.¹²⁷

Conversely, marennine, the water-soluble blue-green pigment produced by the diatom *Haslea ostrearia*, which is responsible for the greening of the gills of oysters in refining ponds of France, seems to have no direct impact on aromas of the oyster,¹²⁸ even if organoleptic properties of “green oysters” are well-appreciated by connoisseurs.¹²⁶ Indeed, apart from the color, their organoleptic properties could result from changes in the microorganism communities that the oysters feed on in refining ponds during the greening phenomenon (the so-called “verdissement en claires”). Marennine displays different biological activities, such as antioxidant,¹²⁹ allelopathic,¹³⁰ antibacterial, and antiviral.¹³¹,¹³² Furthermore, it has been experimentally demonstrated that marennine can inhibit the growth of some microalgae encountered in oyster ponds,¹³⁰,¹³³ which could allow for *H. ostrearia* to outcompete them, thus resulting in the changes in phytoplankton communities observed during the greening in ponds.¹³⁴⁻¹³⁶

Finally, the most notorious off-flavors of fish are the earthy—muddy taints conveyed by geosmin and 2-methylisoborneol (MIB). Produced by cyanobacteria and actinomycetes, these compounds cause alterations of the taste of water and freshwater fish flesh. Reported in several fish species, such as channel catfish and trout,¹³⁷⁻¹³⁹ geosmin and MIB represent a significant problem for fish farming and commercial fishing.¹³⁸ However, this earthy—muddy taint does not originate from the diet but rather from the environment, because fish do not feed from this phytoplankton. The major route of uptake of geosmin and MIB by fish is passive absorption from water through the gills. From the gills, compounds are transported into the blood, then to tissues, such as muscles, and finally concentrated in lipid-rich tissues.¹⁴⁰ The human odor detection thresholds of geosmin and MIB in fish flesh were evaluated between 0.2 and 1.5 µg/kg,¹³⁸ which make them very potent tainting agents. These off-flavor compounds can be removed from fish flesh by holding living fish in clean water for some days. The duration of depuration may vary upon the water temperature and fish fat content.¹⁴⁰

**Algae Incorporation into Innovative Foods and Impact on Flavor.** Incorporating microalgae or macroalgae (seaweed) into food formulations has numerous benefits. The antioxidant and antimicrobial properties of algae constituents can improve the conservation of foodstuffs.¹⁴¹,¹⁴² Algae also constitute a source of proteins, vitamins, and minerals,⁵⁴,¹⁴³⁻¹⁴⁷ and seaweed can be a food flavor and texture enhancer.²,¹⁴⁸ Fortifying products having already a high consumer acceptance with algae could allow for spreading their health benefits to a greater part of the population.¹⁴⁹ However, algae-containing innovative food products should be subjected to a flavor characterization to ensure their acceptability before their release on the market. This is usually achieved by sensory analysis. Recently, some work, summarized in Table 2, has been accomplished on algae incorporation into food products, taking the flavor into account. Emphasis has been placed on works about the aroma impact of algae in foods, but some results on flavor and taste are also presented, because flavor is a combination of aroma and taste and these concepts are interrelated.

**Dairy Products.** Dairy products are one of the most tested food categories for the incorporation of food ingredients for functional food development, with the most common added ingredients being probiotics and prebiotic carbohydrates.¹⁵⁰,¹⁵¹ Nevertheless, there are some recent examples of algae incorporation in dairy, mainly for antioxidants and nutrient enrichment purposes, which include a sensory analysis.

Most algae-containing dairy products are made with microalgae. The impact of microalgae *Chlorella vulgaris* and *Arthrospira platensis* (also named *Spirulina platensis*) addition to the sensory characteristics of fermented milks was reviewed.¹⁵² Some flavor defects can emerge from microalgae incorporation, being generally proportional to the concentration. These defects are due to compounds generated by the oxidation of polyunsaturated acids.¹⁵² This can also be caused by some minerals acting like prooxidants and provoking metallic unpleasant tastes.¹⁵³ More recently, the impact of *A. platensis* supplementation of yogurt at four different concentrations was assessed. Yogurt with the lowest concentration (0.25%) was the most acceptable among the tested formulations.¹⁵⁴ A yogurt was fortified with a lipid extract from *Pavlova lutheri* at 0.25 and 0.50% (w/v); these products exhibited poor acceptability. Hedonic analysis revealed a negative correlation between the “liking of flavor” and the concentration, and the formulations containing the lipid extract exhibited a fishy taste.¹⁵⁵ There is also a recent example of cheese supplemented with microalgae. A feta-type cheese was enriched with 0.5, 1.0, and 1.5% *A. platensis* powder. Sensory analysis revealed that the 0.5 and 1.0% algae formulations were acceptable; with the highest concentration being bitter and with low odor scores.¹⁵⁶

The impact of macroalgae-containing dairy products on their sensory characteristics are less documented than their microalgae counterparts. O'Sullivan et al. studied the impact of the incorporation of three seaweed extracts in milk and yogurt. The addition of all seaweed extracts did not have a significant effect on the odor of milk. The water extract of *A. nodosum* at 0.25 and 0.50% concentration appeared to be the most acceptable in both milk and yogurt. Contrarily, ethanolic extracts were reported with an overall negative impact on sensory acceptance of milk and yogurt. Indeed, some milks containing ethanolic extracts exhibited a fishy taste. In yogurt, all of the ethanolic extracts negatively correlated to flavor and the *A. nodosum* ethanolic extracts negatively correlated to odor.¹⁵⁷,¹⁵⁸

Besides seaweed extracts, whole seaweeds have also been incorporated into dairy products. Powdered dried seaweeds of five species were incorporated into yogurt and quarks at 0.5% to study their influence on the sensory characteristics of these products. *Saccharina latissima* had the lowest seaweed odor and flavor scores aside from the control without algae. This seaweed was judged the most appropriate for yogurt and quark supplementation. In opposition, *Porphyra umbilicalis*, *Ulva lactuca*, and *Undaria pinnatifida* had the most intense effect on the flavor quality of yogurt and quark, being responsible for the highest seaweed odor and flavor scores. Therefore, the incorporation of these seaweeds had a detrimental effect on the sensory characteristics of the yogurt.¹⁵⁹ The detrimental incorporation of *P. umbilicalis* and *U. lactuca* was also pointed out in semi-hard cheese (Ibérico cheese).¹⁶⁰ Cheeses containing these seaweeds exhibited a strong seaweed odor and had lower odor quality scores. In dairy products, incorporating seaweeds with marked odors and flavors lead
<table><caption>Table 2. continued</caption><thead><tr><th>food group</th><th>product</th><th>algae species</th><th>form</th><th>concentration(s) tested</th><th>type(s) of evaluation(s)</th><th>main results</th><th>reference</th></tr></thead><tbody><tr><td></td><td></td><td>Diacronema vulgatum</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td></td><td> pasta</td><td>Arthrospira platensis</td><td>fresh biomass</td><td>5, 10, and 15% (w/w)</td><td>trained panelists from the academic staff; 7-point hedonic scale for flavor, appearance, texture, and overall acceptability</td><td>strange flavor was detected in the 15% formulation; 10% formulation was preferred for its flavor and appearance</td><td>164</td></tr><tr><td></td><td> bread</td><td>Asphyllum nosum</td><td>not precise</td><td>1.25, 2.50, 3.75, and 5% (w/w)</td><td>untrained panelists; samples rated over appearance, aroma, flavor, aftertaste, texture, and overall acceptability</td><td>all bread samples were acceptable</td><td>165</td></tr><tr><td></td><td> bread</td><td>Palmaria palmata</td><td>protein hydrolysate</td><td>4%</td><td>semi-trained consumers; 6-point hedonic scale for appearance, texture, flavor, and general acceptability</td><td>breads containing P. palmata hydrolysate had significantly lower flavor scores than those without algae (bitter taste)</td><td>166</td></tr><tr><td></td><td> bread</td><td>Arthrospira platensis</td><td>not precise</td><td>10% flour replacement</td><td>experienced panelists; external and internal characteristics, odor, and flavor properties were assessed; volatile aroma compound analysis by solid-phase microextraction and gas chromatography mass spectrometry</td><td>panelists suggested lowering the algae concentration to increase the acceptability; 5-nonadecen-1-ol was the predominant volatile in the dough and bread with A. platensis; but was not detected in the conventional formulation</td><td>167</td></tr><tr><td></td><td> bread</td><td>Tetraselmis Nannochloropsis</td><td>not precise</td><td>2.0 and 1.0% (w/w) flour replacement</td><td>semi-trained panelists; 9-point hedonic scale for firmness, flavor, overall visual appearance, and overall acceptability and 5-point hedonic scale for purchase intention; volatile analysis by solid-phase micro-extraction and gas chromatography mass spectrometry (GC-MS)</td><td>aroma scores of bread containing macroalgae were lower than the control, and flavor scores were not different; for crackers, the aroma scores were not different, and the flavor scores were higher than the control; increased emission of compounds, such as P-cymene and (Z)-2-heptenal, was noted for the formulations with algae</td><td>168</td></tr><tr><td></td><td> crackers</td><td>Tetraselmis Nannochloropsis</td><td></td><td>2.5% (w/w) flour replacement</td><td>untrained panelists; sensory attributes: color, smell, taste, texture, and global appreciation</td><td>for the taste and smell, the 2% formulation was not significantly different from the control</td><td>169</td></tr><tr><td></td><td> crostini</td><td>Arthrospira platensis</td><td>biomass dried at a low temperature</td><td>2, 6, and 10% (w/w)</td><td>consumers assessed the appearance, smell, flavor, texture, overall impression (9-point hedonic scale), and purchase intention (5-point hedonic scale)</td><td>no significant differences between the control and algae-enriched doughnuts for the smell and flavor</td><td>170</td></tr><tr><td></td><td> doughnuts</td><td>Arthrospira platensis</td><td>dried biomass</td><td>2.59 and 5.41%</td><td>untrained panelists; sensory characteristics: color, smell, taste, texture, and global appreciation; buying intention was also assessed</td><td>2% A. platensis cookies had the most appreciated taste</td><td>171</td></tr><tr><td></td><td> cookies</td><td>Arthrospira platensis</td><td>freeze-dried powder</td><td>2 and 6% (w/w)</td><td></td><td></td><td></td></tr><tr><td></td><td></td><td>Chlorella vulgaris</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td></td><td></td><td>Tetraselmis succinea</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td></td><td></td><td>Phaeocystum triornutum</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td></td><td> cookies</td><td>Chlorella</td><td>defatted by-product</td><td>3, 6, 9, and 12% flour substitution</td><td>semi-trained panelists; 9-point hedonic rating for color and appearance, texture, taste, flavor, and overall acceptability</td><td>acceptable score for the aroma was obtained up to 9% defatted</td><td>172</td></tr><tr><td></td><td> breadsticks</td><td>Himanthalia elongata</td><td>not precise</td><td>6.08 and 10.33%</td><td>untrained panelists; 5-point hedonic scale for aroma, appearance, texture, flavor, and overall acceptability</td><td>taste and aroma for formulations were slightly lower than the control but were still acceptable</td><td>173</td></tr><tr><td></td><td> biscuits</td><td>Caulerpa racemosa</td><td>powder</td><td>1, 5, and 10%</td><td>semi-trained panelists; 9-point hedonic rating for color, appearance, texture, flavor, and overall acceptability</td><td>sensory scores, including flavor, declined when increasing the seaweed concentration, flavor score of the 1% formulation was close to the score of the control</td><td>174</td></tr><tr><td></td><td> cookies</td><td>Sargassum fulvelum</td><td>powder</td><td>5% flour substitution</td><td>9-point hedonic scale for appearance, flavor, texture, and overall acceptability</td><td>formulations with H. fusiforme, E. linza, and S. fulvelum had the flavor scores the closest to the control; no fishy smell differences were observed between the control and cookie containing H. fusiforme; most preferred seaweed was H. fusiforme</td><td>175</td></tr><tr><td></td><td></td><td>Enteromorpha linza</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td></td><td></td><td>Codium fragile</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td></td><td></td><td>Hizikia fusiforme</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td> extruded corn and rice flour snacks</td><td> Arthrospira sp.</td><td>ground biomass</td><td>2.6%</td><td>assessment of flavor, color, texture, taste, and overall acceptability (9-point hedonic scale) and purchase intention (5-point hedonic scale)</td><td>taste and flavor appreciation were not different from the control</td><td>176</td></tr><tr><td> extruded corn flour snacks</td><td> Arthrospira sp.</td><td>powder</td><td>2, 4, 6, and 8% algae and 8%</td><td>sensory evaluation using a 5-point hedonic scale for shape, color, aroma, taste, and crispiness</td><td>aroma and taste scores were slightly lower than the control and decreased with increasing concentrations of algae</td><td>177</td></tr></tbody></table>
<table><caption>Table 2. continued</caption><thead><tr><th>food group</th><th>product</th><th>algae species</th><th>form</th><th>concentration(s) tested</th><th>type(s) of evaluation(s)</th><th>main results</th><th>reference</th></tr></thead><tbody><tr><td rowspan="10">fish, meat, and poultry</td><td>fish cutlets</td><td>Kappaphycus al-<br/>verezi</td><td>powder</td><td>algae + 2%<br/>baking powder</td><td>ranking test (preference test) and quantitative descriptive analysis; descriptors: brown, compactness, firmness, hardness, fish-like, ily, spicy, salty, pungent, and overall quality</td><td rowspan="10">no significant differences for the aroma attribute; formulation containing 7.5% algae was chosen for profiling and flavor attributes ("pungent", "salty", "spicy", "ily", and "fish-like") were not different from the control</td><td rowspan="10">178</td></tr><tr><td>fish cakes</td><td>Sacharina latissi-<br/>ma</td><td>dried seaweed</td><td>5, 7.5, 10, 12.5, and 15%</td><td>untrained panelists; choice of preference between two formulations: with seaweed or with steamed parsley (control), with assessment of taste and appearance using a 7-category scale</td><td rowspan="10">two formulations were equally attractive to consumers for the flavor, and most panelists liked their taste "moderately" or "strongly"</td><td rowspan="10">6</td></tr><tr><td>carp burgers</td><td>Chlorella minatis-<br/>sima<br/>Iochrysis galbana</td><td>powder</td><td>0.5, 1.0, and 1.5% (w/v)</td><td>panel recruited among the researchers and industry, 5-point hedonic scale for taste, body and texture, color, appearance, and odor</td></tr><tr><td>frankfurters</td><td>Himanthalia elon-<br/>gata<br/>Himanthalia elon-<br/>gata<br/>Palmaria palmata</td><td>powder</td><td>5%</td><td>trained panelists; sensory descriptors: off-flavor, texture, and overall acceptability; use of an unstructured scale</td></tr><tr><td>frankfurters</td><td>Porphyrna umbili-<br/>calis<br/>Undaria pinnatifi-<br/>da</td><td>powder</td><td>1% (w/v)</td><td>panelists were regular frankfurter consumers; sensory acceptance test (hedonic attributes): color, liking of appearance, liking of aroma, liking of flavor, liking of texture, and overall acceptability; ranking descriptive analysis (intensity of sensory attributes): tenderness, juiciness, salt taste, meat flavor, off-flavor, and seaweed flavor; volatile compound extraction and analysis (thermal desorption and GC-MS)</td></tr><tr><td>breakfast saus-<br/>ages</td><td>Laminaria japoni-<br/>ca</td><td>powder</td><td>1, 2, 3, and 4%</td><td>sensory attributes: color, flavor, juiciness, tenderness, and overall acceptability; 10-point descriptive scale</td></tr><tr><td>beef patties</td><td>Himanthalia elon-<br/>gata</td><td>ground<br/>blanched<br/>seaweed</td><td>10, 20, 30, and 40%</td><td>sensory evaluation on 20 and 40% formulations; 5-point hedonic scale for aroma, appearance, texture, flavor, and overall acceptability</td></tr><tr><td>pork patties</td><td>Laminaria japoni-<br/>ca</td><td>powder</td><td>1, 3, and 5%</td><td>sensory attributes: color, flavor, juiciness, tenderness, and overall acceptability; 10-point descriptive scale</td></tr><tr><td>restructured<br/>poultry<br/>steaks</td><td>Himanthalia elon-<br/>gata</td><td>powder</td><td>3%</td><td>trained panelists; sensory descriptors: flavor, texture, and overall acceptability; use of an unstructured scale</td></tr><tr><td>broccoli soups</td><td>Arthrospira sp.<br/>Chlorella sp.<br/>Tetraselmis sp.</td><td>freeze-dried<br/>biomass</td><td>0.5, 1.0, 1.5, and 2.0% (w/v)</td><td>semi-trained panelists; 9-point hedonic scale for flavor and overall acceptance; 5-point hedonic scale for purchase intention</td></tr><tr><td>other</td><td>Ulva sp.<br/>Laminaria ochro-<br/>leuca<br/>Undaria pinnatifi-<br/>da<br/>Himanthalia elon-<br/>gata</td><td>powder</td><td>2.2%</td><td>5-point scale of damage incidence and severity for off-colors, off-flavors, off-odors, lumpiness and phase separation; 5-point hedonic scale of acceptability for visual appearance, aroma, flavor, texture, and overall quality</td></tr></tbody></table>
<table><caption>Table 2. continued</caption><thead><tr><th>food group</th><th>product</th><th>algae species</th><th>form</th><th>concentration(s) tested</th><th>type(s) of evaluation(s)</th><th>main results</th><th>reference</th></tr></thead><tbody><tr><td></td><td></td><td>Palmaria palmata<br>Clondruss crispus<br>Porphyra sp.<br>Chlorella vulgaris<br>Arthrospira sp.</td><td></td><td></td><td></td><td></td><td></td></tr></tbody></table>

to less acceptable formulations than those with more subtle seaweed taste and aroma, such as *Saccharina*. The concentration is also a critical factor. As shown for microalgae, lower concentrations are more acceptable to consumers.

**Cereal Products.** Pasta products are widely consumed around the world and have a good consumer value. They are easy to cook, and dry pasta is shelf-stable.¹⁸⁸ For these reasons, they represent an appropriate vehicle for algae supplementation. Prabhasankar et al. aimed to prepare a seaweed-containing food product to make it appealing for people who do not normally eat algae. Wakame (*U. pinnatifida*) powder was incorporated into pasta. Formulations containing up to 10% wakame were acceptable according to the sensory analysis. Pasta with 10% wakame had a mild seaweed flavor and a taste similar to the control.¹⁶¹ In pasta, this type of seaweed can be added at relatively high concentrations without negatively impacting the flavor. More studies on different types of seaweed need to be conducted, given the relative few publications and species yet tested. Concerning microalgae added in formulation, some studies were also conducted using fresh pasta. Two varieties of *C. vulgaris* (green and orange) and *Arthrospira maxima* (0.5 and 2.0%) were used as well as *Isochrysis galbana* and *Diacronema vlkianum* (0.5, 1.0, and 2.0%).¹⁶²,¹⁶³ Formulations containing *C. vulgaris* or *A. maxima* did not differ from the control regarding odor and flavor. However, for all species tested but orange *C. vulgaris*, a strange flavor was noticed in the 2.0% formulations.¹⁶²,¹⁶³ On the other hand, fresh *A. platensis* biomass was added at 5, 10, and 15% (w/w) in fresh pasta before drying. Pasta with 10% *A. platensis* was preferred for its flavor and appearance.¹⁶⁴

Algae addition in bread can enhance its nutritional qualities. For instance, a high-fiber bread was developed using *A. nodosum*, a brown seaweed containing alginate, a dietary fiber. Concentrations tested ranged between 1.25 and 5% (w/w). Although the control (without seaweed) had higher flavor, aftertaste, and overall acceptability, all enriched bread samples were reported to be acceptable, regarding aroma, flavor, and aftertaste.¹⁶⁵ On the other hand, bread containing a protein hydrolysate from *P. palmata* exhibited significantly lower flavor scores than their counterparts without algae. They were described as bitter by the panelists.¹⁶⁶ The bitterness could be due to the peptide content and the buckwheat flour.¹⁸⁹,¹⁹⁰

There are also examples of microalgae addition in bread. Sensory characteristics of bread with *A. platensis* at a concentration of 10% of the total flour content were evaluated at different storage times and temperatures. Globally, aroma and smell scores were lower for the *Arthrospira*-enriched bread compared to the control without algae, but the difference between the control and enriched bread tended to decrease during the storage. Panelists judged the bread consumable but suggested lowering the *Arthrospira* concentration to increase its acceptability. The volatile compound analysis before and after baking revealed that breads with *Spirulina* exhibited a completely different volatile compound profile compared to the control, which means that adding the microalgae to the bread has an impact on the aroma. For instance, 5-nonadecen-1-ol was the predominant volatile in the dough with *A. platensis* and remained in the bread but was not detected in the conventional dough and bread. However, in this study, the volatile compounds found were only identified and not associated with any aroma.¹⁶⁷

Baked goods, such as biscuits, cookies, or crackers, are widely consumed worldwide and could be fortified with algae.
Some of these have the advantage of having a lower moisture content than bread, which improves their shelf life.¹⁹¹ Lafarga et al. prepared functional breads and crackers containing *Tetraselmis* or *Nannochloropsis*. For bread, there were no differences in flavor between the formulations, but microalgae addition caused a decrease in the aroma score compared to the control. On the other hand, the aroma scores of the algae-containing crackers were not significantly different from the control without algae. Moreover, the flavor score was higher in the crackers enriched with macroalgae compared to the control. Microalgae addition changed the volatile profile of the breads and crackers. An increased emission of compounds, such as *p*-cymene and (Z)-2-heptenal, was noted. The compound *p*-cymene is responsible for the fresh, citrus, terpenic, woody, and spicy odors, while (Z)-2-heptenal has fatty, oily, and fruity aromas.¹⁶⁸ Crostini, a leavened bakery product, was prepared using *A. platensis*. No significant differences were found between the 2% formulation and the control regarding taste and smell, while these scores decreased for the 6 and 10% formulations.¹⁶⁹ Although in that study the lower algae concentration was preferred, it is not always the case. Indeed, higher concentrations of *A. platensis* have been reported acceptable on a sensory basis: up to 5.41% in cassava doughnuts formulations¹⁷⁰ and up to 6% in cookies.¹⁷¹ *Chlorella* incorporation in cookies was also successful, with acceptable sensory scores for aroma and taste. Concentration of 2% *Chlorella vulgaris*¹⁷¹ and up to 9% defatted *Chlorella* meal¹⁷² were reported satisfactory in cookie formulations. Nonetheless, every species of microalgae is not suitable for baked good enrichments. Some of them, such as *Tetraselmis suecica* and *Phaeoactylum tricornutum*, were not further studied as a result of their fishy odor in preliminary tasting sessions.¹⁷¹

With regard to incorporation of seaweed in baked goods, the brown alga *H. elongata* was incorporated into breadsticks at 6.08 and 10.33% concentrations. The taste and aroma for the seaweed-containing formulations were slightly lower than the control, and all of the breadsticks containing algae were still acceptable.¹⁷³ Biscuits were enriched with sea grapes (*Caulerpa racemosa*), a tropical green seaweed, at flour substitution levels up to 10%. A decline in sensory scores, including flavor, was observed with an increased seaweed concentration, but the flavor score of the 1% sea grape formulation was close to the control.¹⁷⁴ The concentration but also the seaweed species can have an impact on flavor. Different seaweed species from the Korean coast were compared to the preparation of cookies. The best flavor score was obtained for the control, followed by *Hizikia fusiforme*, *Enteromorpha linza*, and *Sargassum fulvellum*. No fishy smell differences were observed between the control and cookie containing *H. fusiforme*, and the most disliked formulation regarding the fishy taste was the formulation containing *Codium fragile*. It was demonstrated that the fishy smell was the parameter the most strongly correlated with overall acceptance.¹⁷⁵ Baked goods are a good vehicle for algae supplementation. In most studies, relatively high concentrations (often higher than for bread) could be added without negatively impacting the flavor.

Studies were also conducted with snacks made with extruded flour enriched with algae. A snack consisting of extruded rice and corn flour, which was enriched with *Arthrospira* sp. at a concentration of 2.6% to enhance its nutritional qualities, was prepared.¹⁷⁶ The sensory analyses conducted revealed that the taste and flavor appreciation were not significantly different from the control without algae. In another study using higher

*Arthrospira* sp. concentrations (up to 8%), the aroma and taste scores of enriched corn extrudates slightly decreased when increasing the concentration of algae.¹⁷⁵

*Fish, Meat, and Poultry*. Algae can be incorporated in fish for preservation as a result of their bioactive properties, such as antioxidant activity, but also for the nutritional enrichment.¹⁷⁸,¹⁹² Powdered *Kappaphycus alverezii* was added to fish cutlets at concentrations ranging up to 15%. There was no significant difference in the aroma attribute according to the panelists. The formulation containing 7.5% algae was chosen for profiling, and flavor attributes (“pungent”, “salty”, “spicy”, “oily”, and “fish-like”) were not different from the control.¹⁷⁸ The addition of *Saccharina latissima* in fish cakes also had a positive impact on the flavor. The alga-enriched cake was equally attractive compared to the control, and panelists liked the taste “moderately” or “strongly”.⁶ Microalgae were also incorporated into fish products. Three species (*Chlorella minutissima*, *Isochrysis galbana*, and *Picochlorum* sp.) were added to carp burgers at 0.5, 1.0, and 1.5% (w/v). The 0.5 and 1.0% formulations showed no differences from the control regarding the odor, taste, and aftertaste.¹⁷⁹ It is noteworthy that algae incorporation in fish has the advantage of not inducing an unpleasant fishy flavor, as reported above for other types of products.

Algae generally contain a high concentration in minerals; therefore, they can be used in meat for sodium replacement. Their dietary fiber content can improve meat texture by enhancing water- and fat-binding properties.¹⁹³ There are some studies reporting seaweed addition in sausages. Frankfurters containing 5% *H. elongata* had higher off-flavors, which negatively affected their overall acceptability. These off-flavors could be limited by selecting a seaweed with a lower flavor intensity and/or modifying the seasoning.¹⁸⁰ Four types of seaweeds (*H. elongata*, *U. pinnatifida*, *P. umbilicalis*, and *P. palmata*) at 1% (w/w) were tested in reformulated frankfurters.¹⁸¹ All formulations containing seaweeds had lower “liking of aroma” than the control, while the “liking of flavor” attribute was similar to the control for all formulations, except *P. palmata*, which had a lower score. Sausages containing *H. elongata* and *U. pinnatifida* were the closest to the control for the seaweed flavor. All sausages containing seaweed also exhibited a higher off-flavor intensity than the control, in particular, *P. palmata*. *H. elongata* was the most accepted seaweed for sausage incorporation. The volatile profile of the frankfurters revealed a lot of diversity between the formulations, especially relating to the abundance levels of different compounds. The terpenes and esters had the highest levels in *H. elongata*, while ketones, phenylpropanes, and phenols were the predominant classes in the sausages containing *P. umbilicalis*. Alcohols, aldehydes, and sulfur compounds were the most abundant classes in *P. palmata* frankfurters, and the formulation containing *U. pinnatifida* did not have a predominant class of volatiles. However, there is still work needed to be done to evaluate the impact of individual volatile compounds on the sensory properties.¹⁸¹ The seaweed concentration also has an impact on the meat flavor. Breakfast sausages containing *Laminaria japonica* (sea tangle) at 0, 1, 2, 3, and 4% were prepared. The highest flavor scores during the sensory evaluation were obtained with 1 and 2% concentrations. It is thus possible that the savory taste of the sea tangle favorably impacts the flavor at these levels.¹⁸²

Seaweed addition in patties was also studied. Blanched *H. elongata* was added at five different concentrations in beef
patties (0, 10, 20, 30, and 40%). The 20 and 40% seaweed concentrations were selected for the sensory evaluation. Patties containing seaweeds scored slightly lower than the control regarding the aroma attribute but exhibited higher scores for the taste, and those containing 40% seaweed had the highest overall acceptability. No seaweed aroma was detected, which could be attributed to the blanching process.¹⁸³ These results agree with those of Choi et al., who prepared reduced-fat pork patties using *L. japonica* powder at 1, 3, and 5%. Flavor scores of formulations containing 1 and 3% seaweed had similar flavor scores and a higher overall acceptability than the control without algae.¹⁸⁴

Studies about algae addition in poultry and its impact on flavor are scarce. To our knowledge, there is one study where restructured poultry steaks were prepared with powdered *H. elongata* (3%) added to the chicken and blended. Seaweed significantly affected most of the parameters of the sensory evaluation. The panelists were able to detect a non-meat flavor in formulations containing seaweed. The flavor acceptability score was inferior to the control but was still acceptable with scores higher than 5 out of 10.¹⁸⁵

*Other Products.* Broccoli soups were prepared using *Arthrospira* sp., *Chlorella*, sp., or *Tetraselmis* sp. at concentrations ranging from 0.5 to 2.0% (w/v). There were no differences in flavor compared to the control for *Arthrospira* and *Tetraselmis* at 0.5%, while *Chlorella* incorporation, even at 0.5%, had an adverse effect on flavor.¹⁸⁶ In another study, quality changes during storage in fresh green smoothies supplemented with nine edible micro- and macroalgae at 2.2% were investigated. Algae addition led to a mild marine taste in the smoothies. On the day of processing, no off-flavors and odors were detected. *C. crispus* and *Chlorella* had the lowest overall quality scores, mostly as a result of their strong marine odor and flavor. After 17 days of storage at 5 °C, off-flavors were noticed, mostly for *Chlorella* and brown macroalgae, but *Ulva* kept an acceptable overall quality up to 24 days.¹⁸⁷

Impact of algae on aromas must be attentively monitored to achieve aroma harmony in common food products while benefiting from their nutritional enrichment. Several factors should be considered when incorporating algae to food to ensure a good flavor acceptability. The concentration, the type of product, and the algae species have an impact on flavor. In some products, such as pasta and baked goods, higher concentrations are tolerated, but in others, especially dairy, low concentrations are preferred. In addition, some algal aromas can be enhanced or attenuated by controlled processing of the raw materials. Studies on algal aromas, in accordance with preferences of consumers, are a promising avenue in the development of innovative food containing algae. Indeed, more studies need to be conducted regarding the flavor profile of the products using instrumental analysis and associating it with sensory analysis. This could allow for identifying the molecules responsible for good and bad flavors. This fundamental knowledge could help to produce better and accepted innovative foods containing algae.

## AUTHOR INFORMATION

### Corresponding Author

*Lucie Beaulieu* — *Institut sur la Nutrition et les Aliments
Fonctionnels (INAF), Département des Sciences des Aliments,
Université Laval, Québec City, Québec G1V 0A6, Canada*;

● orcid.org/0000-0001-8120-1039;

Email: lucie.beaulieu@fsaa.ulaval.ca

## Authors

**Nellie Francezon** — **Institut sur la Nutrition et les Aliments**
*Fonctionnels (INAF), Département des Sciences des Aliments,
Université Laval, Québec City, Québec G1V 0A6, Canada;*
*Institut National de Recherche pour l'Agriculture,*
*l'alimentation et l'Environnement (INRAE), 49070*
*Beaucouzé, France*

**Ariane Tremblay** — **Institut sur la Nutrition et les Aliments**
*Fonctionnels (INAF), Département des Sciences des Aliments,
Université Laval, Québec City, Québec G1V 0A6, Canada*

**Jean-Luc Mouget** — **Mer-Molécules-Santé (MMS), FR CNRS**
*3473 IUML, Le Mans Université, 72085 Le Mans, France*

**Pamela Pasetto** — **Institut des Molécules et Matériaux du Mans (IMMM), UMR CNRS 6283, Le Mans Université,**
*72085 Le Mans, France*

Complete contact information is available at:

https://pubs.acs.org/10.1021/acs.jafc.1c04409

## Funding

Nellie Francezon postdoctoral position received grants from the Région Pays de la Loire, Recherche, Formation & Innovation (RFI) "Food for Tomorrow", and Institut sur la Nutrition et les Aliments Fonctionnels (INAF). This work takes part in a project that has received funding from the European Union's Horizon 2020 Research and Innovation Program under Grant Agreement 734708/GHaNA/H2020-MSCA-RISE-2016 (Jean-Luc Mouget coordinator).

## Notes

The authors declare no competing financial interest.

## ACKNOWLEDGMENTS

The authors thank Eric Tamigneaux for providing pictures of *P. palmata* for this review.

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