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org/JAFC Review

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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ABSTRACT: As a result of their nutritive values, algae have been used as a food resource for centuries, and there is a growing
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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
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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
11.5 million tons, Eucheuma spp. at 9.2 millions, Gracilaria spp.
at 3.4 millions, Undaria pinnatifida (wakame) at 2.3 million,
phytoplankton (microalgae) and seaweed (macroalgae) have a and Porphyra/Pyropia spp. (nori) at 2.0 million.3 On the other
hand, microalgae farming was reported to an understated
long history of human consumption. Macroalgae are multi-
volume of 87 000 tonnes, with Spirulina being the most
cellular macroscopic aquatic plants, which belong to different
produced.
taxons, Chlorophyta (green algae), Rhodophyta (red algae),
As a result of their healthy nutritive properties, algae raised
and Phaeophyceae (brown algae). Their unicellular counter-
interest as enrichment ingredients in processed foods but also
part, microalgae, are distributed in a wider classification
as an improved diet for breeding. Their incorporation into
system, including genetically very different and non-exhaus-
food products would benefit from their high protein contents
tively eukaryotic Chlorophyta, Euglenophyta, Bacillariophyta
and their richness in minerals, vitamins, dietary fibers, and
or diatoms, Haptophyta, Chrysophyta, and prokaryotic
polyunsaturated fatty acids.2 Whatever the nutritional value of
cyanobacteria (blue-green algae). The cyanobacteria Spirulina,
food products, their acceptability depends upon consumer
nowadays marketed as Super Food in Occident, was already
cognitive experiences and expectations and also organoleptic
well-known by the ancient Aztec civilization and Chad
properties, of which the perception results from complex
populations.1 Other cyanobacteria/microalgae, such as Nostoc
interactions of different senses. Indeed, for taste perception,
spp., Aphanotheca sacrum, Spirogyra, and Oedogonium, were
there are four basic traditional tastes identified, bitterness,
consumed as food or food supplement in Burma, Thailand, saltiness, sweetness, and sourness, with their appreciation
Vietnam, and India.1 Seaweeds have a long tradition in Pacific relying on receptors on different parts of the oral cavity. Some
(Indonesia, Philippines, Hawaii, and New Zealand) and Asian algae can bring bitterness from some protein-derived peptides,
(China, Korea, and Japan) cultures, being a central ingredient saltiness from their high mineral contents (e.g., Na and K), and
in their daily cuisine.2 sweetness from their soluble sugars (e.g., mannitol).
According to the Food and Agriculture Organization of the Furthermore, algae are known for being the representant of
United Nations (FAO), the world production of algae has the fifth taste, the umami taste,4 mainly provided by the free
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 Received: July 21, 2021
production with 18.5 million tons), Indonesia, Korea, and Revised: September 18, 2021
Philippines. Some other countries around the world, such as Accepted: September 19, 2021
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

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Table 1. Some of the Main Aroma Compounds of Algae, with Their Odor Threshold and Olfactory Descriptors11−13 a

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Table 1. continued
a
∗, in ethanol; ∗∗, in water.
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 develop-
ments 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
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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 pertusa9 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 character-
istic 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
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Figure 1. Algal aroma wheel.9,10
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 sulfoniopro-
pionate (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), character-
izing 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 Crypthecodinium cohnii.19
Benthic diatoms are considered intermediate DMSP pro-
ducers, 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
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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 C6−C9
aldehydes and typical marine-seaweed smell for C15−C17
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 (sea-
weed), (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 C6 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 chromatog-
raphy−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,
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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 C5 compounds. Microalgae
Crypthecodinium cohnii and Schizochytrium limacinum, which
have been used to produce DHA, were demonstrated to
contain high amounts of saturated and unsaturated alde-
hydes.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. undulata33 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
C11 and C8 polyunsaturated open-chain or cyclic hydro-
carbons, 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
(C10) and sesquiterpenes (C15) are odoriferous volatile
compound classes, mainly found in terrestrial plant essential
oils. Other classes, such as diterpenes (C20), sesterterpenes
(C25), triterpenes (C30), and tetraterpenes (C40), 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.41 Although isoprene contributes to ocean−atmos-
phere 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, D-limonene,
eucalyptol,39 linalool, and geraniol in Chlorella vulgaris42 and
sylvestrene and thujone in Spirulina platensis,43 but also in
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macroalgae, such as α-pinene, D-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
Crytophyta 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 Chlor-
ophyta.45 The cleavage of carbon−carbon double bonds on the
polyene chain of carotenoids results in various odoriferous
volatile compounds, called norisoprenoids. These norisopre-
noids 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, Botryo-
coccus, 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
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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-cyclo-
citral.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 character-
istic 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 Bromo-
phenols, 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
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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 Thalas-
siosira 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 Crypthecodinium 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 carbo-
nated 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 pro-
cesses. 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 modifica-
tions 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 micro-
organisms (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
J. Agric. Food Chem. XXXX, XXX, XXX−XXX
Journal of Agricultural and Food Chemistry
had been studied (e.g., Chlamydomonas reinhardtii, Nanno-
chloropsis sp., Phaeodactylum tricornutum, Porphyridium sp., and
Chlorella sp.).71 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.72−74 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.72 Ionones are
produced by the breakdown of carotenoids either enzymati-
cally or chemically. The latter includes photo-oxygenation,
auto-oxidation, and thermal degradation, and the former
involves carotenoid cleavage by dioxygenases and other
enzymes,73 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).75 Coupled with an efficient
purification process, it led to industrially viable ionone
production.72,76 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.31,77,78 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 carotenes;48,49 therefore their use
as new models can be raised. Unfortunately, as recently
demonstrated by Liang et al., β-ionone and β-cyclocitral
(another product of carotenoid cleavage) inhibit the growth of
Dunaliella.79 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 norisopre-
noids.80 Moreover, several cyanobacteria (Microcrystis, Calo-
thrix, 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.73
Biotransformation of Monoterpenes. Specificities of
microorganism enzymes, such as oxyfunctionalization (inte-
gration 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.64
Studies on microalgae abilities of transforming common
monoterpenes, such as (R)-(+)-carvone, D-(+)-limonene,
(+)-β-pinene, thymol, (+)-linalool, (−)-menthone, (+)-pule-
gone, (−)-fenchone, and (−)-piperitone, were assessed on
Chlorella sp., Ooscystis sp., Synechococcus sp., and Chlamydo-
monas sp.81−83 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.64
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Indeed, vanillin obtained biotechnologically from micro-
organisms is labeled “natural vanillin” according to U.S. and
European legislation,84 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.84−89 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.90 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.91
■ 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.92,93 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).94 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.94 Similarly, the crushing of algae
resulted in a modification of algal aromas with the release of
enzymes.95 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.96
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.97 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
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Journal of Agricultural and Food Chemistry
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 com-
pounds) 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
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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
Crypthecodinium 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 polyunsatu-
rated 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, Rho-
dophyceae, 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, bromo-
phenols 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
J. Agric. Food Chem. XXXX, XXX, XXX−XXX
Journal of Agricultural and Food Chemistry
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 pig-
ment 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 encoutered 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 miner-
als,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 accept-
ability before their release on the market. This is usually
achieved by sensory analysis. Recently, some work, summar-
ized 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.
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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 concen-
tration. 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 concen-
trations 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
J. Agric. Food Chem. XXXX, XXX, XXX−XXX
 Table 2. Examples of Algae Incorporation in Diverse Food Types and Its Impact on Flavor
food concentration(s)
group product algae species form tested type(s) of evaluation(s) main results reference
dairy yogurt Arthrospira pla- powder 0.25, 0.50, 0.75, panel recruited among the research staff and industry; 9-point hedonic flavor and taste not different from the control at 0.25% 154
tensis and 1.00% scale for color and appearance, body and texture, flavor, and overall
acceptability
yogurt Pavlova lutheri lipid extract 0.25 and 0.50% naive untrained panel; hedonic scale for color, flavor, texture, negative correlation between the “liking of flavor” and the 155
(w/v) acceptability, and intensity descriptors for thickness, odor, off-odor, concentration; a fishy taste was noticed
sour taste, yogurt flavor, off-flavor, and fishy taste
feta cheese Arthrospira pla- powder 0.5, 1.0, and 1.5% trained panelists; 5-point hedonic scale for appearance, color, syneresis, 0.5 and 1.0% formulations were acceptable, while the 1.5% 156
tensis odor, texture, consistency, spreadability, flavor, saltiness, bitterness, formulation showed bitterness and low odor scores
mouthfeel, and pleasantness
milk Ascophyllum no- aqueous ex- 0.25 and 0.50% naive panelists; sensory analysis descriptors (color, fishy taste, odor, seaweed extracts did not have a significant effect on the odor; 80% 157
dosum tract flavor, off-flavor, texture, and overall acceptability) and degree of ethanol A. nodosum extract at 0.5% and F. vesiculosus extract at
80% ethanol liking 0.25% negatively correlated with the flavor indicator and
extract positively correlated with the off-flavor indicator; fishy taste
negatively influenced the taste of milk; aqueous extract was
Fucus vesiculosus 60% ethanol more acceptable than ethanolic extracts
extract
yogurt Ascophyllum no- aqueous ex- 0.25 and 0.50% naive panelists; sensory analysis descriptors (color, odor, flavor, aqueous extract was the most acceptable; A. nodosum ethanolic 158
Journal of Agricultural and Food Chemistry

dosum tract off-flavor, texture, thickness, and overall acceptability) and degree of extracts were negatively correlated with odor and flavor; F.
80% ethanol liking vesiculosus extract at 0.5% was negatively correlated with flavor
extract
Fucus vesiculosus 60% ethanol
extract
yogurt and Himanthalia elon- powder 0.5% trained assessors; sensory analysis characteristics were odor quality, highest seaweed odor and flavor scores and lower odor and flavor 159
quark gata seaweed odor, yogurt odor, buttery odor, flavor quality, seaweed quality were obtained with P. umbilicalis, U. lactuca, and U.

J
Porphyra umbili- flavor, acid flavor, bitter flavor, sweet flavor, salty flavor, texture pinnatifida; S. latissima had the lowest seaweed odor and flavor
calis quality, and texture uniformity scores besides the control without algae
Saccharina latissi-
ma
Ulva lactuca
Undaria pinnatifi-
da
semi-hard Himanthalia elon- dehydrated 1.0% trained panelists; characteristics tested were odor quality, seaweed cheeses containing P. umbilicalis and U. lactuca exhibited a strong 160
cheese gata seaweed odor, flavor quality, seaweed flavor, acid flavor, bitter flavor, sweet seaweed odor and had lower odor quality scores
Porphyra umbili- pieces flavor, salty flavor, umami flavor, and texture quality
calis (2 mm)
pubs.acs.org/JAFC

Laminaria ochro-
leuca
Ulva lactuca
Undaria pinnatifi-
da
cereal pasta Undaria pinnatifi- powder 5, 10, 20, and semi-trained panelists who are regular eaters of wakame; sensory pasta with up to 10% wakame was acceptable; panelists 161
da 30% attributes: appearance, strand quality, mouth feel, and overall quality complained of saltiness for formulations with 20 and 30%
seaweed
fresh pasta green Chlorella freeze-dried 0.5 and 2.0% untrained panelists; sensory attributes: color, odor, flavor, and texture algae-containing pasta did not differ from the semolina control for 162
vulgaris biomass odor and flavor; strange flavor was detected in 2.0% green C.
orange Chlorella vulgaris and A. maxima pasta by some panelists
vulgaris
Arthrospira maxi-
ma
fresh pasta Isochrysis galbana freeze-dried 0.5, 1.0, and 2.0% untrained panelists; sensory attributes: color, odor, flavor, and texture fish flavor was noticed in 2.0% formulations, which led to a lower 163
Review

biomass global appreciation

J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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 Table 2. continued
food concentration(s)
group product algae species form tested type(s) of evaluation(s) main results reference
Diacronema vlkia-
num
pasta Arthrospira pla- fresh biomass 5, 10, and 15% trained panelists from the academic staff; 7-point hedonic scale for strange flavor was detected in the 15% formulation; 10% 164
tensis (w/w) flavor, appearance, texture, and overall acceptability formulation was preferred for its flavor and appearance
bread Ascophyllum no- not precise 1.25, 2.50, 3.75, untrained panelists; samples rated over appearance, aroma, flavor, all bread samples were acceptable 165
dosum and 5% (w/w) aftertaste, texture, and overall acceptability
bread Palmaria palmata protein hydro- 4% semi-trained consumers; 6-point hedonic scale for appearance, texture, breads containing P. palmata hydrolysate had significantly lower 166
lysate flavor, and general acceptability flavor scores than those without algae (bitter taste)
bread Arthrospira pla- not precise 10% flour re- experienced panelists; external and internal characteristics, odor, and panelists suggested lowering the algae concentration to increase 167
tensis placement flavor properties were assessed; volatile aroma compound analysis by the acceptability; 5-nonadecen-1-ol was the predominant volatile
solid-phase microextraction and gas chromatography mass spec- in the dough and bread with A. platensis, but was not detected in
trometry the conventional formulation
bread Tetraselmis not precise 2.0 and 1.0% semi-trained panelists; 9-point hedonic scale for firmness, flavor, overall aroma scores of bread containing macroalgae were lower than the 168
Nannochloropsis (w/w) flour re- visual appearance, and overall acceptability and 5-point hedonic scale control, and flavor scores were not different; for crackers, the
placement for purchase intention; volatile analysis by solid-phase micro- aroma scores were not different, and the flavor scores were
crackers Tetraselmis 2.5% (w/w) flour extraction and gas chromatography mass spectrometry (GC−MS) higher than the control; increased emission of compounds, such
as p-cymene and (Z)-2-heptenal, was noted for the formulations
Journal of Agricultural and Food Chemistry

Nannochloropsis replacement
with algae
crostini Arthrospira pla- biomass dried 2, 6, and 10% untrained panelists; sensory attributes: color, smell, taste, texture, and for the taste and smell, the 2% formulation was not significantly 169
tensis at a low (w/w) global appreciation different from the control
temperature
doughnuts Arthrospira pla- dried biomass 2.59 and 5.41% consumers assessed the appearance, smell, flavor, texture, overall no significant differences between the control and algae-enriched 170
tensis impression (9-point hedonic scale), and purchase intention (5-point doughnuts for the smell and flavor
hedonic scale)

K
cookies Arthrospira pla- freeze-dried 2 and 6% (w/w) untrained panelists; sensory characteristics: color, smell, taste, texture, 2% A. platensis cookies had the most appreciated taste 171
tensis powder and global appreciation; buying intention was also assessed
Chlorella vulgaris
Tetraselmis sueci-
ca
Phaeoactylum tri-
cornutum
cookies Chlorella defatted by- 3, 6, 9, and 12% semi-trained panelists; 9-point hedonic rating for color and appearance, acceptable score for the aroma was obtained up to 9% defatted 172
product flour substitu- texture, taste, flavor, and overall acceptability Chlorella
tion
breadsticks Himanthalia elon- not precised 6.08 and 10.33% untrained panelists; 5-point hedonic scale for aroma, appearance, taste and aroma for formulations were slightly lower than the 173
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gata texture, flavor, and overall acceptability control but were still acceptable
biscuits Caulerpa racemo- powder 1, 5, and 10% semi-trained panelists; 9-point hedonic rating for color, appearance, sensory scores, including flavor, declined when increasing the 174
sa texture, flavor, and overall acceptability seaweed concentration; flavor score of the 1% formulation was
close to the score of the control
cookies Sargassum fulvel- powder 5% flour substi- 9-point hedonic scale for appearance, flavor, texture, and overall formulations with H. fusiforme, E. linza, and S. fulvellum had the 175
lum tution acceptability flavor scores the closest to the control; no fishy smell differences
Enteromorpha were observed between the control and cookie containing H.
linza fusiforme; most preferred seaweed was H. fusiforme
Codium fragile
Hizikia fusiforme
extruded corn Arthrospira sp. ground bio- 2.6% assessment of flavor, color, texture, taste, and overall acceptability taste and flavor appreciation were not different from the control 176
and rice mass (9-point hedonic scale) and purchase intention (5-point hedonic
flour snacks scale)
extruded corn Arthrospira sp. powder 2, 4, 6, and 8% sensory evaluation using a 5-point hedonic scale for shape, color, aroma and taste scores were slightly lower than the control and 177
flour snacks algae and 8% aroma, taste, and crispiness decreased with increasing concentrations of algae
Review

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 Table 2. continued
food concentration(s)
group product algae species form tested type(s) of evaluation(s) main results reference
algae + 2%
baking powder
fish, fish cutlets Kappaphycus al- powder 5, 7.5, 10, 12.5, ranking test (preference test) and quantitative descriptive analysis; no significant differences for the aroma attribute; formulation 178
meat, verezii and 15% descriptors: brown, compactness, firmness, hardness, fish-like, oily, containing 7.5% algae was chosen for profiling, and flavor
and spicy, salty, pungent, and overall quality attributes (“pungent”, “salty”, “spicy”, “oily”, and “fish-like”)
poultry were not different from the control
fish cakes Saccharina latissi- dried seaweed 5% (w/w) untrained panelists; choice of preference between two formulations: two formulations were equally attractive to consumers for the 6
ma with seaweed or with steamed parsley (control), with assessment of flavor, and most panelists liked their taste “moderately” or
taste and appearance using a 7-category scale “strongly”
carp burgers Chlorella minutis- powder 0.5, 1.0, and 1.5% panel recruited among the researchers and industry; 5-point hedonic formulations containing 1.5% algae scored lower than the control 179
sima (w/v) scale for taste, body and texture, color, appearance, and odor for the organoleptic characteristics, including odor (except
Isochrysis galbana Picochlorum, which showed no odor differences), taste, and
aftertaste; formulations containing 0.5 and 1.0% of microalgae
Picochlorum sp. showed no differences from the control
frankfurters Himanthalia elon- powder 5% trained panelists; sensory descriptors: off-flavor, texture, and overall higher off-flavors in the formulation with algae, which led to a 180
gata acceptability; use of an unstructured scale lower acceptability
frankfurters Himanthalia elon- powder 1% (w/w) panelists were regular frankfurter consumers; sensory acceptance test all formulations had lower “liking of aroma” than the control; 181
Journal of Agricultural and Food Chemistry

gata (hedonic attributes): color, liking of appearance, liking of aroma, there were no significant differences to the control for the “liking
Palmaria palmata liking of flavor, liking of texture, and overall acceptability; ranking of flavor”, except for P. palmata, which had a lower score;
descriptive analysis (intensity of sensory attributes): tenderness, sausages with H. elongata and U. pinnatifida were the closest to
juiciness, salt taste, meat flavor, off-flavor, and seaweed flavor; volatile the control seaweed scores; P. palmata sausages had the higher
compound extraction and analysis (thermal desorption and off-flavor intensity; H. elongata was the most accepted seaweed
Porphyra umbili- GC−MS) predominant compound classes were terpenes and esters (H.
calis elongata), ketones, phenylpropanes, and phenols (P. umbilicalis),

L
Undaria pinnatifi- and alcohols, aldehydes, and sulfur compounds (P. palmata); no
da predominant classes for U. pinnatifida
breakfast saus- Laminaria japoni- powder 1, 2, 3, and 4% sensory attributes: color, flavor, juiciness, tenderness, and overall highest flavor scores were obtained with 1 and 2% formulations 182
ages ca acceptability; 10-point descriptive scale
beef patties Himanthalia elon- ground 10, 20, 30, and sensory evaluation on 20 and 40% formulations; 5-point hedonic scale aroma attribute score was lower for the seaweed patties, but the 183
gata blanched 40% for aroma, appearance, texture, flavor, and overall acceptability taste score was higher compared to the control; no seaweed
seaweed aroma was detected, probably as a result of blanching; patties
containing 40% seaweed had the highest acceptability
pork patties Laminaria japoni- powder 1, 3, and 5% sensory attributes: color, flavor, juiciness, tenderness, and overall there were no differences in flavor for low-fat pork patties 184
ca acceptability; 10-point descriptive scale containing seaweed compared to the control (regular-fat pork
patties), and reduced-fat pork patties without seaweed had a
lower flavor score compared to the control; patties with 1 and
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3% had the highest overall acceptability

restructured Himanthalia elon- powder 3% trained panelists; sensory descriptors: flavor, texture, and overall non-meat flavor was detected in formulations containing seaweed; 185
poultry gata acceptability; use of an unstructured scale flavor acceptability of the seaweed-containing chicken was
steaks acceptable, but the score was lower than the control
other broccoli soups Arthrospira sp. freeze-dried 0.5, 1.0, 1.5, and semi-trained panelists; 9-point hedonic scale for flavor and overall flavor scores were affected by the concentration, the species, and 186
Chlorella sp. biomass 2.0% (w/w) acceptance; 5-point hedonic scale for purchase intention an interaction between these two factors; there were no
differences for flavor compared to the control for 0.5%
Tetraselmis sp. Arthrospira and 0.5% Tetraselmis soups; Chlorella had an adverse
effect of flavor, even at 0.5%
green Ulva sp. powder 2.2% 5-point scale of damage incidence and severity for off-colors, off-flavors, mild marine taste was noticed in smoothies containing algae; C. 187
smoothies Laminaria ochro- off-odors, lumpiness and phase separation; 5-point hedonic scale of crispus and Chlorella had the lowest overall quality scores, mostly
leuca acceptability for visual appearance, aroma, flavor, texture, and overall as a result of their strong marine odor and flavor; off-flavors
quality were detected after 17 days of storage, but the formulation with
Undaria pinnatifi- Ulva still kept an acceptable overall quality until 24 days of
da storage
Himanthalia elon-
Review

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to less acceptable formulations than those with more subtle

reference
seaweed taste and aroma, such as Saccharina. The concen-
tration 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 supplementa-
tion. 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
main results

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
type(s) of evaluation(s)

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
concentration(s)

due to the peptide content and the buckwheat flour.189,190

tested

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
form

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
Palmaria palmata

Chlorella vulgaris
Chondrus crispus
algae species

Arthrospira sp.

its acceptability. The volatile compound analysis before and

Porphyra sp.

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-
Table 2. continued

1-ol was the predominant volatile in the dough with A. platensis

product

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
group
food

Baked goods, such as biscuits, cookies, or crackers, are

widely consumed worldwide and could be fortified with algae.
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Journal of Agricultural and Food Chemistry
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 vulgaris171 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 concen-
trations (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
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Arthrospira sp. concentrations (up to 8%), the aroma and taste
scores of enriched corn extrudates slightly decreased when
increasing the concentration of algae.177
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 enrich-
ment.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% concen-
trations. 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
J. Agric. Food Chem. XXXX, XXX, XXX−XXX
Journal of Agricultural and Food Chemistry
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 concen-
trations 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
O https://doi.org/10.1021/acs.jafc.1c04409
pubs.acs.org/JAFC Review
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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