Natural Carotenoids
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Biotechnologically produced carotenoids occupy an important place in the scientific research. Owing to their role as natural pigments and their high antioxidant properties, microbial carotenoids have been proposed as alternatives to their synthetic counterparts. Natural carotenoids can be obtained either by extraction from plants or via microbial production. To this end, many studies are focusing on their efficient and sustainable production from renewable substrates. Besides the development of an efficient upstream process, their separation and purification as well as their analysis from the microbial biomass confers another important aspect to be adressed.

natural carotenoids colorants separation of carotenoids analysis of carotenoids biotechnological production

1. Types and Chemistry of Carotenoids

Carotenoids are chemical compounds belonging to the group of terpenoids. Terpenoids are also called isoprenoids because their structure consists of eight units of isoprene (C5H8). There are two categories of carotenoids, both with biotechnological interest; the carotenes consist of hydrocarbons, and the xanthophylls with their oxygenated derivatives [1]. Figure 1 presents the chemical structures of the most common carotenes and xanthophylls produced by microorganisms. Carotenes include carotenoids such as α-, β- and γ-carotene, lycopene, torulene, neurosporene and others. The group of xanthophylls includes astaxanthin, zeaxanthin, lutein, torularhodin, canthaxanthin, violaxanthin and others.
Figure 1. Chemical structures of the most important carotenoids produced biotechnologically.
Natural carotenoids are biosynthesized via two major pathways, namely the 2-C-methyl-D-erythritol 4-phosphate (MEP) and the mevalonate (MVA) pathways. The two main terpenoid precursors generated from these pathways are dimethylallyl diphosphate (DMAPP) and isopentenyl diphosphate (IPP), respectively. Geranylgeranyl diphosphate (GGPP) is then generated from IPP isomerization, carried out by the addition of three IPP molecules to DMAPP, which is subsequently condensed to phytoene [2][3]. Finally, phytoene, which is the first carotenoid synthesized from the pathways, is desaturated and isomerized to lycopene [3][4]. The structure of all carotenoids can be derived from the structure of acyclic C40H56 (corresponds to the structure of lycopene) via hydrogenation, dehydrogenation, cyclization or oxidation [1]. The main characteristic of the carotenoid structure is the long hydrocarbon chain, consisting of conjugated double bonds. The delocalized π electrons from the conjugated double bonds system are the reason that carotenoids exhibit high antioxidant properties. In β-carotene, both ends are cyclized, while lycopene is characterized by two acyclic parts in its structure. The number of conjugated double bonds is also linked to the color of the carotenoid [5]. Molecules with a high number of conjugated double bonds absorb at higher wavelengths, resulting in a yellow-red color. A characteristic example is the formation of lycopene during the maturation of tomatoes from phytoene by phytoene desaturase. The conjugated bonds in the carotenoids’ structure have the ability to absorb visible light and are thus responsible for the molecule’s color. Phytoene is a colorless compound with three conjugated double bonds that is converted to phytofuene (pale yellow) with five conjugated double bonds, ζ-carotene (yellow) with seven conjugated double bonds, neurosporene (orange) with nine conjugated double bonds and finally to lycopene (red) with eleven conjugated double bonds [6].
The number of conjugated bonds in the molecule determines the color and the absorbance maxima. For instance, lycopene is an acyclic molecule of red color and because of the 11 conjugated double bonds, its maximum absorbance is located at 444, 470 and 502 nm. On the other hand, α-carotene, with 10 conjugated double bonds (one of them in the cyclic part), absorbs at 422, 445 and 473 nm, demonstrating an orange color [5].
The position of the side groups linked to the atoms where the double bonds are located divides carotenoids into trans or cis isomers. Trans carotenoids are also characterized as all-E and cis carotenoids as Z [7]. The all-E characterization refers to a structure where all double bonds are in trans formation, while the Z one differs depending on the double bond that is found in cis formation. Figure 2 illustrates the all-E isomer (trans) of lycopene and one of its cis isomers. Carotenoids occur predominantly in their all-E form; however the extent of antioxidant activities and bioavailability in the human body is highly dependent on the type of carotenoid under investigation [8]. Many studies evidence that Z-isomers (especially in the case of lycopene and astaxanthin) exhibit higher scavenging activities than their trans counterparts, while also presenting greater bioavailability [8][9][10]. Likewise, regarding their abundance, there is a wide distribution of carotenoid isomers in nature. For example, β-carotene is commonly found in all-E, as well as in its 9Z- and 13Z- isomers; lycopene also occurs as 5Z-, 9Z-, 13Z-, 15Z- and di-Z-, while 9Z-lutein and 13Z-lutein have been identified in tomatoes [9].
Figure 2. Examples of chemical structures of trans (All-E) and cis isomers (15Z-, 13Z- and 9Z-) of lycopene.
Chirality is another characteristic of most carotenoids due to the presence of chiral centers in their molecules. Astaxanthin and zeaxanthin are characteristic examples of chiral carotenoids, both with two chiral centers in 3 and 3′ carbon due to the presence of hydroxyl groups. These carotenoids have two enantiomers—the 3R,3′R and the 3S,3′S—and an optical inactive meso form of 3R,3′S [11].

2. Sources of Natural Carotenoids

Carotenoids are naturally occurring in plants, photosynthetic bacteria and algae but also in some heterotrophic bacteria and fungi [6][7]. Animals and humans obtain carotenoids from food, as they are unable to synthesize them. Nevertheless, the obtained carotenoids can be modified with metabolic reactions [6] for the synthesis of other carotenoids or their derivatives.

2.1. Plants

Plants constitute the prevalent source of natural carotenoids, as a wide spectrum of these compounds is found in fruits, flowers and vegetables but also in other plant tissues such as leaves, roots and seeds [12]. β-carotene is the predominant carotenoid extracted from plants, with carrots, spinach, tomatoes, sweet potatoes, broccoli and lettuce to be the richest sources. According to Stephen et al. [13], α- and β-carotene are the signature carotenoids of carrot, lycopene is for tomatoes, watermelon and papaya, lutein is for watercress and spinach and yellow bell peppers are rich in violaxanthin.
The utilization of waste fruits and vegetables for the sustainable recovery of carotenoids has been already demonstrated [14]. Another interesting approach has been recently introduced by Metličar et al. [15][16], proposing the exploitation of invasive alien plant species such as Japanese knotweed and Bohemian knotweed to extract carotenoids and xanthophylls.

2.2. Microorganisms

Besides plants, several microbial species, belonging to algae, bacteria and fungi, are able to accumulate intracellularly different types of carotenoids as metabolic products. Carotenoids production in non-photosynthetic microorganisms is connected to an evolutionary response to photo-oxidative damage caused by light and oxygen-rich habitats [17]. In the last few decades, many research groups have prioritized the investigation on the biotechnological production of carotenoids. It is only indicative that from the 750 naturally occurring carotenoids, more than 600 can derive from microorganisms [18][19].
Plant-derived pigments display difficulties with respect to characterization and standardization due to the effect of cultivation and climate conditions. Another important drawback lies in the stability and functionality of these pigments, particularly regarding exposure at high temperatures, pH variations and light [20]. Microorganisms evidence a prominent scientific potential due to the variation of their pigment color, the chemical profile of the pigment, the independence of seasonal restrictions and climate conditions, along with the capacity to scale up. In the framework of sustainability and circular economy, it is nowadays imperative to explore alternative sources of food additives that will not compete with food and feed and, in parallel, will respect the environment. Microbial carotenoids coincide entirely with the above mentioned purposes. The efficient productivities and high yields, complete process control and standardization of the product quality confer advantages of microbial carotenoids’ synthesis, directly related to the potential for large-scale production. Moreover, the utilization of low-cost and renewable resources (such as agro-industrial wastes and byproducts) as substrates for microbial growth could further mitigate the overall cost of production [21].

3. Biotechnological Production of Carotenoids

Table 1 refers to indicative research of the last five years on the biotechnological production of carotenoids. In fact, algae and fungi are the most popular choices among the most studied microbial strains for carotenoid production such as β-carotene, astaxanthin, torulene, zeaxanthin, torularhodin and lutein.
Microalgae are widely recognized as sources of diversified bioactive compounds such as pigments, phenolic compounds, fatty acids, proteins and vitamins, among others [17]. The microalgae Haematococcus pluvialis and Dunaliella salina have been extensively studied for astaxanthin and β-carotene production, respectively [17][22][23][24]. Spirulina is richer in β-carotene even compared to carrots [20]. Chlorella and Scenedesmus are also significant carotenoid producers, mainly of lutein [25][26]. The limitation of large-scale carotenoid production using microalgae lies in the high production costs and the high land requirements [21][27]. Bacteria and fungi introduce a prevalent advantage to this angle, as proper strain selection, substrate and fermentation/bioreactor design can lead to high product yields and productivities in completely controlled processes.
Yeasts have emerged as robust carotenoid producers, with the strains Rhodotorula sp. and Phaffia rhodozyma occupying most of the recently published works. Rhodotorula sp. together with the genera Rhodosporidium, Sporidiobolus and Sporobolomyces belong to a category known as “red yeasts”, describing their ability to intracellularly accumulate carotenoids [28]. Another important attribute of yeasts is their capability to synthesize carotenoids via the valorization of low-cost substrates as growth substrates, including cheese whey [21], molasses [29] and raw glycerol [30]. Red yeasts have been generally reported to produce mixtures of carotenoids, mainly β-carotene, γ-carotene, lycopene, torulene and torularhodin [21][28]. P. rhodozyma, a basidiomycetous yeast, is a well-known producer of astaxanthin and β-carotene [20][31]. The fungus Blakeslea trispora is industrially employed for β-carotene and lycopene production and its use as a food additive has already been approved [32][33].
Likewise, recent studies have been undertaken using some Archaea for carotenoid synthesis. Many Haloarchaea have developed the ability to accumulate pigments as a response to stress factors. To this end, Giani et al. [34] investigated the potential of the strain Haloferax mediterranei to synthesize carotenoids, and especially the C50 carotenoid bacterioruberin, when subjected to various concentrations of H2O2. Similarly Lizama et al. [35] explored different Haloarchaea strains, namely Halorubrum tebenquichense and Haloarcula sp., for their carotenoid profile and antioxidant capacity.
Finally, cyanobacteria are also able to produce carotenoids, still in lower amounts compared to other pigments such as phycocyanin [36]. Pagels et al. [36] recently reviewed the potential of these microorganisms, reporting the strains Cyanobium sp., Arthrospira platensis, Trichodesmium sp. and Lyngbya sp. as some characteristic examples of carotenoid-producing strains, also exhibiting antioxidant activities. The main carotenoids synthesized by these strains were β-carotene and zeaxanthin.
Table 1. Recent developments on natural carotenoids produced by microorganisms.

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