Exopolysaccharides from microalgae: Production in a biorefinery framework and potential applications
Graphical abstract
Introduction
Microalgae exopolysaccharides (EPS) are increasingly attracting interest owing to their physicochemical, functional, and industrial applications, and the growing market demand for natural polysaccharides. These bioactive compounds can be beneficial to health, biodegradable and versatile in product development (Santos and Amorim, 2018). EPS have biochemical properties with great potential for application in the biotechnology area because of their anticancer, antibacterial, antioxidant, and antiviral activities (Sed et al., 2017).
EPS are defined as extracellular polysaccharides that can be excreted by microalgae in the environment around them or be linked to the cell walls of these microorganisms. Some of the functions of EPS, include protecting the microalgal cells from biotic and abiotic stresses, mainly dehydration or toxic substances (Zhang et al., 2019b). Furthermore, EPS are related to the production of biofilms and cell adhesion and interaction (Liu et al., 2016). Many microalgae, especially the reds and cyanobacteria, produce EPS and can excrete large amounts of this compound (around 20 g L−1) (Michaud, 2018). Around 90,000 tons/year of algal polysaccharides are used in the pharmaceutical, cosmetic, and hydrocolloid industries. However, there is no saturation of this market and can integrate new products, for example, biopolymers and functional foods, obtained from microalgal EPS (Kraan, 2012; Michaud, 2018).
The cost of EPS can be reduced considerably through microalgae biomass production technologies and treatments under the biorefinery concept (Michaud, 2018). Biorefineries allow the sustainable processing of the biomass in various products (chemicals, biofuels, food, and feed) and bioenergy (Mitra and Mishra, 2019). Some strategies can be applied in biorefineries to integrate with a sustainable economy (circular bioeconomy), such as reducing costs and increasing yields by using flue gases and/or wastewater as nutrient sources. Furthermore, microalgal biomass can be fully used to obtain various compounds and coproducts with high value (Bongiovani et al., 2020; Rosero-Chasoy et al., 2021).
An option to increase the market value and potential applications of EPS are the use of nanotechnology techniques. The nanometer scale can bring to EPS different physicochemical properties and these structures can interact with cells and tissues at the molecular level (Dutta and Das, 2021). An EPS product can act more specifically as an bioactive compound though nanoencapsulation and its biodisponibility can also be increased (Roychowdhury et al., 2021). EPS as its antioxidant and anti-inflammatory characteristics, can be applied for the development of nanostructured scaffolds mixed with polymers that can be used as a smart dressing that speeds up the healing process (Morais et al., 2014).
In this context, this review article aims to address aspects related to EPS production from microalgae, focusing on strategies to improve production efficiency, environmentally friendly extraction techniques, and potential applications of these biocompounds. The application of nanobased structures and products with EPS in pharmaceutical, cosmeceutical, water treatment, and food industries will be also addressed. In addition, the integrated EPS obtention with the coproduction of compounds with a high value-added under the biorefinery concept, aiming to minimize costs and overcome the challenges of large-scale production will be encompassed.
Section snippets
Microalgal sources of exopolysaccharides: characteristics, cultivation strategies, and extraction methods
Microalgal EPS are mainly heteropolysaccharides formed from xylose, glucose, and galactose, and considerable amounts of monosaccharides such as fucose, methylated sugars, rhamnose, and iduronic acid (Michaud, 2018). In addition, they may contain non-sugar substituents, such as pyruvate, proteins, and sulfate (Table 1) (Delattre et al., 2016; Pereira et al., 2009). In general, their structure is complex and can contain from 9 to 12 different monosaccharides (Delattre et al., 2016). Although most
Production of exopolysaccharides in a biorefinery framework
Microalgal EPS are a by-product that can be obtained under the biorefinery concept, because after the biomass concentration they can be removed from the supernatants without the generation of residues. In addition, polysaccharides synthesized by most microalgal species are composite heteropolymers. Based on this, the bioactive compounds have a wide spectrum of molecular weights and ions that result in high value-added applications in several areas, for example pharmaceuticals, cosmetics,
Biological activity
Studies have reported different biological activities of EPS produced by microalgae (Table 1). Their antioxidant, anti-inflammatory, antitumor, and antimicrobial properties make microalgal EPS promising for pharmaceutical, cosmetic, and food applications.
EPS containing uronic acids and charged groups (pyruvate and sulfate) are characterized by an anionic nature and have been associated with several biological activities (De Philippis and Vincenzini, 1998; Sun et al., 2009; Tannin-Spitz et al.,
Current challenges and future prospects
Microalgal EPS production is limited by two main factors: production costs and reduced knowledge about these compounds produced by microalgae (Patel et al., 2013). The biomass production by the photosynthetic pathway is what generally increases the cost of production. Despite the high yield of polysaccharides, the amount of biomass produced does not make the product competitive compared to EPS extracted from plants or macroalgae (Delattre et al., 2016).
The alternatives to overcome this issue
Conclusion
Microalgae can produce EPS with structurally diverse and biological properties that vary according to species, cultivation, and extraction conditions. Moreover, the potential for expanding the use of these compounds was demonstrated with the production of nanostructures. However, although EPS are used industrially, microalgae represent only a small portion of the market. For greater industrial use of microalgal EPS, technological stages of production must be optimized to reduce large-scale
CRediT authorship contribution statement
M.G. Morais: Conceptualization, Writing – review & editing, Supervision. T.D. Santos: Conceptualization, Investigation, Writing – original draft, Writing – review & editing. L. Moraes: Conceptualization, Investigation, Writing – original draft, Writing – review & editing. B.S. Vaz: Conceptualization, Investigation, Writing – original draft, Writing – review & editing. E.G. Morais: Conceptualization, Investigation, Writing – original draft, Writing – review & editing. J.A.V. Costa:
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 would like to thank the Coordination for the Improvement of Higher Education Personnel (CAPES) – Finance Code 001, National Council for Scientific and Technological Development (CNPq), Ministry of Science, Technology and Innovation (MCTI), Research Support Foundation of the State of Rio Grande do Sul (FAPERGS), and Project CAPES-PRint FURG for their support of this study.
References (96)
- et al.
Biochemical characterization of Nostoc sp. Exopolysaccharides and evaluation of potential use in wound healing
Carbohydr. Polym.
(2021) Characterization and optimization of production of exopolysaccharide from Chlamydomonas reinhardtii
Carbohydr. Polym.
(2013)- et al.
Extracellular polysaccharide produced by Chlorella vulgaris – Chemical characterization and anti-asthmatic profile
Int. J. Biol. Macromol.
(2019) - et al.
The potential of microalgae and their biopolymers as structuring ingredients in food: a review
Biotechnol. Adv.
(2019) - et al.
New method for quantitative determination of uronic acids
Anal. Biochem.
(1973) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding
Anal. Biochem.
(1976)- et al.
Chlorella vulgaris α-L-arabino-α-L-rhamno-α, β-D-galactan structure and mechanisms of its anti-inflammatory and anti-remodelling effects
Int. J. Biol. Macromol.
(2020) - et al.
Enhancement of extracellular polymeric substances (EPS) production in Spirulina (Arthrospira sp.) by two-step cultivation process and partial characterization of their polysaccharidic moiety
Int. J. Biol. Macromol.
(2017) - et al.
A new exopolysaccharide produced by marine Cyanothece sp. 113
Bioresour. Technol.
(2007) - et al.
Autotrophic cultivation of Botryococcus braunii for the production of hydrocarbons and exopolysaccharides in various media
Biomass Bioenergy
(2007)
Exocellular polysaccharides from cyanobacteria and their possible applications
FEMS Microbiol. Rev.
Effects of growth conditions on exopolysaccharide production by Cyanospira capsulata
Bioresour. Technol.
Production, extraction and characterization of microalgal and cyanobacterial exopolysaccharides
Biotechnol. Adv.
Scope of green nanotechnology towards amalgamation of green chemistry for cleaner environment: a review on synthesis and applications of green nanoparticles
Environ. Nanotechnology, Monit. Manag.
The role of microalgae in the bioeconomy
New Biotechnol.
Engineering aspects of microbial exopolysaccharide production
Bioresour. Technol.
Production of exopolysaccharide by Botryococcus braunii CCALA 778 under laboratory simulated Mediterranean climate conditions
Algal Res.
Non-toxic nano approach for wastewater treatment using Chlorella vulgaris exopolysaccharides immobilized in iron-magnetic nanoparticles
Int. J. Biol. Macromol.
Quantitative assessment of extraction methods for bound extracellular polymeric substances (B-EPSs) produced by Microcystis sp. and Scenedesmus sp
Algal Res.
Synthesis and structural characterization of silver nanoparticles using bacterial exopolysaccharide and its antimicrobial activity against food and multidrug resistant pathogens
Process Biochem.
Efficient accumulation of high-value bioactive substances by carbon to nitrogen ratio regulation in marine microalgae Porphyridium purpureum
Bioresour. Technol.
Two-stage cultivation of microalgae for production of high-value compounds and biofuels: a review
Algal Res.
Protein measurement with the Folin phenol reagent
J. Biol. Chem.
Concomitant production of fatty acid methyl ester (biodiesel) and exopolysaccharides using efficient harvesting technology in flat panel photobioreactor with special sparging system via Scenedesmus abundans
Bioresour. Technol.
Anticoagulant activity of a sulfated polysaccharide from the green alga Arthrospira platensis
Biochim. Biophys. Acta
Optimization of growth and EPS production in two Porphyridum strains
Bioresour. Technol. Reports
Isolation and characterization of extracellular polymeric substances from micro-algae Dunaliella salina under salt stress
Bioresour. Technol.
Multiproduct biorefinery from Arthrospira spp. towards zero waste: current status and future trends
Bioresour. Technol.
Chromium and cobalt sequestration using exopolysaccharides produced by freshwater cyanobacterium Nostoc linckia
Ecol. Eng.
Microalgae biomass production for a biorefinery system: recent advances and the way towards sustainability
Renew. Sust. Energ. Rev.
Production and characterization of extracellular carbohydrate polymer from Cyanothece sp. CCY 0110
Carbohydr. Polym.
Recent advanced applications of nanomaterials in microalgae biorefinery
Algal Res.
Separation and fractionation of exopolysaccharides from Porphyridium cruentum
Bioresour. Technol.
Influence of sulphate on the composition and antibacterial and antiviral properties of the exopolysaccharide from Porphyridium cruentum
Life Sci.
Microbial co-culturing strategies for the production high value compounds, a reliable framework towards sustainable biorefinery implementation – an overview
Bioresour. Technol.
Isolation of an exopolysaccharide from a novel marine bacterium Neorhizobium urealyticum sp. nov. and its utilization in nanoemulsion formation for encapsulation and stabilization of astaxanthin
LWT
Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent
Methods Enzymol.
Response of Scenedesmus sp. to microwave treatment: enhancement of lipid, exopolysaccharide and biomass production
Bioresour. Technol.
Improvement of exopolysaccharide production by Porphyridium marinum
Bioresour. Technol.
Preparation of different molecular weight polysaccharides from Porphyridium cruentum and their antioxidant activities
Int. J. Biol. Macromol.
Immunomodulation and antitumor activities of different-molecular-weight polysaccharides from Porphyridium cruentum
Carbohydr. Polym.
Magnetophoretic removal of microalgae from fishpond water: feasibility of high gradient and low gradient magnetic separation
Chem. Eng. J.
Structural characteristics and biological effects of exopolysaccharide produced by cyanobacterium Nostoc sp
Int. J. Biol. Macromol.
Optimisation of culture parameters for exopolysaccharides production by the microalga Rhodella violacea
Bioresour. Technol.
Influences of drying methods on the structural, physicochemical and antioxidant properties of exopolysaccharide from Lactobacillus helveticus MB2-1
Int. J. Biol. Macromol.
Production and characterization of exopolysaccharides from Chlorella zofingiensis and Chlorella vulgaris with anti-colorectal cancer activity
Int. J. Biol. Macromol.
Characterization of exopolysaccharides produced by microalgae with antitumor activity on human colon cancer cells
Int. J. Biol. Macromol.
Transcriptome analysis reveals possible antitumor mechanism of Chlorella exopolysaccharide
Gene
Cited by (22)
Microalgae harvesting for wastewater treatment and resources recovery: A review
2023, New Biotechnology