ReviewProducing fucoxanthin from algae – Recent advances in cultivation strategies and downstream processing
Introduction
Fucoxanthin is a brown-colored xanthophyll carotenoid abundant in brown macroalgae (such as Dictyota, Fucus, Laminaria, Sargassum, and others), diatoms, haptophytes, and Chrysophyceae species (Mao et al., 2020, Sahin et al., 2019). These unicellular microalgae, diatoms, and Chrysophyceae sp. exhibit a characteristic golden-brown color due to their high fucoxanthin content (Gao et al., 2017). Fucoxanthin serves a significant role as the light-harvesting pigments for photosynthesis in the protein-pigment network of fucoxanthin-chlorophyll a/c-binding proteins complexes (FCPs). FCPs enable the harvesting of blue-green light under water and efficiently quench the excess energy, providing algae with outstanding light harvesting and photoprotection capabilities.
Fucoxanthin has recently garnered much attention for use in various industries, including cosmetic, food, nutraceutical, and pharmaceutical industries (Kanamoto et al., 2021). In addition, fucoxanthin can also be employed as a feed additive in aquaculture and poultry industries (Xia et al., 2013). This is because fucoxanthin possesses multiple biological activities which benefit human health, including anti-allergic, anti-angiogenic, anti-cancer, anti-diabetic, anti-hypertension, anti-inflammatory, anti-malarial, anti-obesity, anti-osteoporotic, anti-oxidant activities as well as protective effects on the bones, brain blood vessels, eyes, liver, and skin (Peng et al., 2011, Sahin et al., 2019, Sivagnanam et al., 2015). The antioxidant activity of fucoxanthin is related to its unique structure, which is composed of an allenic bond, a 5–6 monoeposide and oxygenic functional groups, including carbonyl, carboxyl, epoxy and hydroxyl groups (Nie et al., 2021b). Fucoxanthin has the ability to scavenge reactive oxygen species on mouse macrophage RAW 264.7 cells (Murakami et al., 2000), kidney fibroblasts (Heo et al., 2008), human hematoma HepG2 cells (Zeng et al., 2018), and human hepatic L02 cells (Wang et al., 2018c). The antioxidant activity of fucoxanthin also contributed to its other bioactivities, including cardiovascular-protective, hepato-protective, neuro-protective and skin-protective.
Supplied by Algatechnologies Inc., FucovitalTM was the first fucoxanthin health food product approved by the US Food and Drug Administration (Kanamoto et al., 2021). Currently, commercially available fucoxanthin is mainly from marine seaweeds such as Eisenia bicyclis, Fucus vesiculosus, Hijikia fusiformis, Saccharina japonica and Undaria pinnatifida where some are the most common edible macroalgae in East and Southeast Asia and some European countries. Studies showed that fresh macroalgae generally have higher fucoxanthin content as compared with dried algae which might be due to the loss of fucoxanthin during the drying process (Kanazawa et al., 2008). Furthermore, to minimize the generation of waste, Kanazawa and coworkers have proposed and studied the potential of commercial production of fucoxanthin from the waste part of kombu (Kanazawa et al., 2008). Table 1 presented fucoxanthin content in macroalgae in fresh or dried form. However, fucoxanthin production via macroalgae is not economically favorable due to several reasons, including low fucoxanthin content, poor product quality, low growth rate, and seasonal dependence (Li et al., 2019, Lu et al., 2018).
With the characteristics of rapid growth rate and high fucoxanthin content, microalgae such as Isochrysis spp. (7.5–23.3 mg/g), Nitzschia spp. (12–32.8 mg/g), Phaeodactylum tricornutum (10.9–59.2 mg/g), Tisochrysis lutea (2.1–79.4 mg/g) and others serve as a source of fucoxanthin production with immense potential. Furthermore, researchers have demonstrated fucoxanthin-producing microalgae can accumulate valuable co-metabolites, such as lipid in Isochrysis spp. (Kim et al., 2012b), Nitzschia spp. (Mao et al., 2020, Sahin et al., 2019), and T. lutea (Gao et al., 2020) as well as omega-3 polyunsaturated fatty acids in Isochrysis spp. (Sun et al., 2019), Odontella aurita (Xia et al., 2018), P. tricornutum (Derwenskus et al., 2020, Gao et al., 2017, Wang et al., 2018a, Yuan et al., 2020, Zhang et al., 2018) and Thalassiosira weissflogii (Marella & Tiwari, 2020).
The pathway of fucoxanthin biosynthesis in microalgae remains unclear, though researchers proposed that fucoxanthin can be synthesized from either diadinoxanthin or neoxanthin as shown in Fig. 1 (Guo et al., 2016). Diadinoxanthin and diatoxanthin constitute the Diadinoxanthin Cycle (Torzillo et al., 2012). They are photoprotective pigments that play significant roles in the short-term protective mechanism. The increase in light intensity initiates the de-epoxidation of diadinoxanthin to diatoxanthin, resulting in decreased accumulation of fucoxanthin. On the other hand, Violaxanthin Cycle consisting of violaxanthin (the precursor of neoxanthin), antheraxanthin and zeaxanthin is essential for the rapid adaption of algae to a wide variation of light intensity. Violaxanthin is converted to zeaxanthin upon high light via antheraxanthin intermediate, causing a reduced level of fucoxanthin and neoxanthin.
Most related literature reviews have focused on the bioactivities of fucoxanthin (Bae et al., 2020, Kumar et al., 2013, Maeda, 2015, Peng et al., 2011), while the upstream microalgal production (especially culture conditions and pilot-scale studies) and downstream processing (especially pretreatment and emerging extraction technologies) of fucoxanthin have been rarely discussed in the literature. As this information is valuable for future commercial-scale production of fucoxanthin, this review aims to bridge the gap by providing an overview of the upstream and downstream processing of microalgae-based fucoxanthin production. In upstream cultivation of fucoxanthin-accumulating algae, topics such as culture conditions, heterotrophic and mixotrophic cultivation, utilization of low-cost byproducts as a nutrient medium, and pilot-scale studies were discussed. On the other hand, in the downstream processing, different pretreatment and extraction technologies were explored as well as the underlying mechanisms were presented.
Section snippets
Culture conditions for fucoxanthin-accumulating microalgae
Among different factors affecting microalgae cultivation, temperature and pH usually do not affect the accumulation of fucoxanthin from microalgae, but play a role in biomass production. Most fucoxanthin-accumulating microalgae, such as Isochrysis spp., Nitzschia spp., P. tricornutum, T. lutea and others are mesophilic, where they grow well at a moderate temperature of 20–30 °C, except for O. aurita which has an optimum cultivation temperature of −1.5–6 °C (Marella and Tiwari, 2020, Mohamadnia
Heterotrophic and mixotrophic cultivation
Other than the conventional photoautotrophic mode, there are various cultivation modes, such as heterotrophic cultivation and mixotrophic cultivation. Although most fucoxanthin-producing microalgae can grow photoautotrophically, commercial-scale production of fucoxanthin will be limited by the inability to achieve high cell densities due to the “self-shading” effect causing light limitation (Lu et al., 2018). Eliminating the requirement of light illumination, heterotrophic cultivation mode
Utilization of low-cost substrate for sustainable production of fucoxanthin
To achieve a low-cost and sustainable production of fucoxanthin, researchers have attempted to utilize low-cost substrates, such as wastes from agriculture and food industries, including palm oil mill effluent (POME), soybean residue (okara), spent yeast and others to substitute conventional nitrogen and phosphorus source for fucoxanthin biosynthesis from P. tricornutum (Kim, 2019, Nur et al., 2019, Yuan et al., 2020).
Consisting of a mixture of both organic and inorganic nitrogen and phosphorus
Open culture systems - open pond systems
For commercial-scale production of microalgae, open pond systems such as open tank and raceway ponds are widely employed due to their low capital and operating cost as well as easy to build and simple operation (Ishika et al., 2017). Furthermore, Torzillo et al. showed that microalgal culture of P. tricornutum in an open pond system has higher fucoxanthin content when compared with tubular photobioreactors as low-light acclimatization in the pond culture induced fucoxanthin accumulation (
Pretreatment process for macroalgae
As mentioned previously, fresh macroalgae are preferred for fucoxanthin extraction, instead of dried macroalgae. Pretreatment technologies are usually employed to improve the extraction efficiency of fucoxanthin from macroalgae, where cutting and grinding increases the surface area to volume ratio for extraction, washing minimizes the salt content of macroalgal extract, and freezing helps preserve the sensitive biomolecules during transportation (Kanazawa et al., 2008). In addition, heat
Challenges and future prospects
The biorefinery approach of utilizing low-cost byproducts as a nutrient medium for cultivation of fucoxanthin-accumulating microalgae (Kim, 2019, Nur et al., 2019, Yuan et al., 2020) or fucoxanthin recovery from the waste part of brown macroalgae (Kanazawa et al., 2008) demonstrated good examples of circular economy, which recycle materials in a closed-loop and minimize waste output. Furthermore, researchers have always studied the possibility of co-production of fucoxanthin with lipids which
Conclusion
This paper has systematically reviewed and provided insights on the fundamentals of fucoxanthin upstream fermentation and downstream processing technologies, facilitating the future development of its industrial-scale production. Flat plate photobioreactors emerged as potential photobioreactors for the commercial production of fucoxanthin. Microalgae strains with tolerance towards a wide range of salinity are preferred for open pond cultivation systems. Novel and innovative “green” solvent
CRediT authorship contribution statement
Yoong Kit Leong: Investigation, Writing – original draft. Chun-Yen Chen: Validation, Resources. Sunita Varjani: Investigation, Writing – review & editing. Jo-Shu Chang: Conceptualization, Funding acquisition, Project administration, Writing – review & editing.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
The authors acknowledge the financial support received from Taiwan’s Ministry of Science and Technology (MOST) under grant number 110-2221-E-029-005, 110-3116-F-006 -003, 110-2221-E-029 -004 -MY3, 110-2621-M-029 -001, 110-2221-E-006 -029 -MY3, and 109-2622-E-110 -011.
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