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Cite This: J. Agric. Food Chem. 2018, 66, 11544−11549
Marine Poly- and Oligosaccharides as Prebiotics Roya R. R. Sardari and Eva Nordberg Karlsson*
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Biotechnology, Department of Chemistry, Lund University, Post Office Box 124, 221 00 Lund, Sweden ABSTRACT: The marine environment can increase the global production of biomass. Interest in marine macroalgae and microorganisms has increased tremendously as a result of international agendas and market trends promoting sustainability as well as healthy food. Macroalgae and marine microorganisms contain unique poly- and oligosaccharides with different substitutions, e.g., sulfation or carboxylation. There is great potential to find prebiotic compounds from these marine-derived saccharides. However, the exact composition and substituent distribution needed for the activity is to a large extent unexplored. In depth investigations of these compounds will provide us with novel insights on the specific structures required for the observed functions. KEYWORDS: marine, prebiotics, dietary fiber, macroalgae, polysaccharide, gut microbiota
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INTRODUCTION Sustainable production of agricultural resources for food and food additives is facing significant challenges as a result of the increasing world population and limitations in cultivable land. Thus, there is a need to explore alternative production sites and food sources that have high capacity as well as low fertilization need. The seas and oceans (that make up 71% of the surface of the earth) have always been a resource for food and contain complex ecosystems, making up valuable biodiversity.1,2 From this system, algae biomass can be used directly or as components in food and non-food applications. Macroalgae contain different kinds of poly- and oligosaccharides, which can be used as food products and additives and which in many cases show health-promoting properties.2−4 Macroalgae (seaweeds) are already used today as food in Asia, where most of the global production takes place (28.3 million tonnes in 20145), but is only used to a limited degree in Europe and the U.S., despite significant production potential. Macroalgae are aquatic organisms with high photosynthetic ability that belong to the lower plants, and it has been reported that they have higher productivity rates than terrestrial biomass, such as corn and switchgrass.6 Macroalgae are classified as green algae (Chlorophyta and Charophyta, with the latter in mainly freshwater species), red algae (Rhodophyta), and brown algae (Phaeophyta), in accordance with their respective thallus color, which is derived from natural pigments and chlorophylls. Many potential health-promoting activities in macroalgae, such as prebiotic, antibacterial, antioxidant, and anti-inflammatory properties, have been linked to their poly- and oligosaccharides.4,7 In addition, marine microorganisms are named the lung of the planet as a result of the production of more than 50% of the Earth’s oxygen. Typical marine microorganisms are bacteria (in the phyla Actinobacteria, Firmicutes, Cyanobacteria, and Proteobacteria), fungi (Ascomycota, Basidiomycota, and Chytridiomycota), including yeasts (originating from several genera in both Ascomycota and Basidiomycota), microalgae, and diatoms [in phyla classified under Heterokonta and in Dinoflagellata (classified under Alveolata)]. The marine © 2018 American Chemical Society
microorganisms are living in different places of the oceans and produce unique molecules, of which some have broad applications in the pharmaceutical industry.8 The aging population and lifestyle-related diseases have created a demand for more knowledge about and better access to healthy food and food additives. Prebiotics (first identified and named by Gibson and Roberfroid9) are non-digestible food ingredients that stimulate growth and/or activity of health-promoting bacteria (probiotics) in the digestive system in humans and animals. In this way, prebiotic compounds modulate the gut microbiota to a more health-promoting species distribution that, e.g., results in release of bioactive, immuno-stimulating compounds. The marine environment can both increase the global biomass production and supply resources (i.e., marine macroalgae and microorganisms) rich in prebiotic and bioactive compounds,3,10 which is in line with the United Nations global sustainability goals for 2030 (e.g., eliminating hunger, securing access to food, reducing food waste, achieving improved nutrition, and promoting sustainable farming and water use).11 This makes it worthwhile to highlight marine macroalgae as a source of prebiotic poly- and oligosaccharides and to also pay attention to marine microorganisms as producers of interesting exopolysaccharides that can further increase the product potential from marine environments. The importance of the exact poly- and oligosaccharide structures for the prebiotic function and/or bioactivity (both prebiotic properties and bioactivity are often reported for the same type of polymer) is however to a large extent unexplored, and more research is needed to highlight the importance of substituents and the exact molecular structures needed for specific functions. Received: Revised: Accepted: Published: 11544
August 14, 2018 October 10, 2018 October 11, 2018 October 11, 2018 DOI: 10.1021/acs.jafc.8b04418 J. Agric. Food Chem. 2018, 66, 11544−11549
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Figure 1. Microbial genera from Firmicutes and Actinobacteria found in the GI tract with proposed probiotic properties.9,14
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PREBIOTICS AND THE HUMAN GASTROINTESTINAL (GI) TRACT The microbiota of the human GI tract is a complex system that has been the subject of many reviews. Recently, Thursby and Juge12 highlighted that improved techniques for analysis via whole-genome shotgun metagenomics (e.g., MetaHit and the Human Microbiome Project) led to identification of 2172 species isolated from humans, including 386 strict anaerobes, with the latter most likely found in the large intestine.12,13 The different species identified in humans were classified into 12 different phyla, of which more than 90% belonged to Proteobacteria, Firmicutes, Actinobacteria, and Bacteroidetes. Some of these species play very important roles in human health, such as providing nutrients, protecting against pathogens, and modulating the host metabolism and immune system by secretion of metabolites. The species distribution, diversity, and metabolic outputs of the gut microbiota thus affect the host in a way that can be either beneficial or harmful. Several microbial species from Firmicutes and Actinobacteria have, for example, been proposed to play beneficial (probiotic) roles (Figure 1).14 The distribution of species in the gut can be influenced by the intake of prebiotics. To be classified as prebiotics, the compounds should survive the small intestinal digestion but be substrates for gut microbiota in a way that is favorable for the host health. The prebiotic activity of a compound is evaluated on the basis of three criteria: (1) compound resistance against digestibility in the upper GI tract, (2) microbial fermentation
of the compound by gut bacteria, and (3) increased growth of beneficial gut bacteria (probiotics), leading to stimulation of the host metabolism in a beneficial way.15 The probiotic species use the prebiotics in their metabolism and secrete metabolites [e.g., short-chain fatty acids (SCFAs)] that interact with human intestinal and immunomodulating cells. The presence of country-specific microbial species signatures in human GI tracts show that the composition of the gut microbiota is influenced by our diet as well as by other, less known, host-specific factors.12,13 Hence, important strategies to obtain a favorable balance and more growth of the beneficial species are to use foods and food ingredients with prebiotic properties shown to influence the microbiota (at least during the period of intake).3,9 The fermentation rate of the prebiotic compounds is also of importance. A slower fermentation rate may, for example, be desirable, leading to less discomfort (e.g., less flatulence). The fermentation rate may be affected (often slowed down) by substituents on the prebiotic compounds. Most of the polysaccharides used in our diet today originate from terrestrial plant cell walls16 that are either digestible or non-digestible (dietary fibers). Various dietary fibers [host non-digestible polysaccharides (degree of polymerization (DP) of >20) or oligosaccharides (DP of 2−19)] are promising as prebiotics and originate from many different sources,3,9,16,17 including species from marine environments. The glycosidic bonds joining the monosaccharides in the dietary fibers can be hydrolyzed by enzymes, produced by microorganisms in the 11545
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Figure 2. Schematic phylogenetic tree (not drawn to scale) of marine macroalgae. The figure is giving examples of some well-known species and major polysaccharides occurring in brown, red, and green algae. The Charophyta group of green algae is not shown in the chart, because the majority of these species thrive in freshwater. The total polysaccharide content in macroalgae range from approximately 10 to 75% of the seaweed dry weight, but both total and species-specific polysaccharides show seasonal variation. Generally, species of brown algae contain alginic acid, fucoidan (sulfated fucose), and laminaran (β-1,3-glucans). Species of red algae contain differing amounts of carrageenans, agars, xylans, floridean starch (amylopectin-like glucan), and water-soluble sulfated galactans. Green algae contain sulfated polysaccharides (galactans and xylans). Some examples of reported prebiotic effects are given next to polysaccharides used for trials on prebiotic effects. ML = mixed linkage.
(e.g., alginate) or sulfated (e.g., fucoidan and ulvan);7 i.e., they carry substituents that may affect their fermentability. The most common and known algae polysaccharides are alginates, laminarins, and fucoidans (from brown algae), carrageenans and agar (from red algae), and ulvans (from green algae) (Figure 2), but even for these compounds, the exact composition, substituent distribution, and distribution of glycosidic linkage types differ between species and varies between seasons. Frequently, the main components in the polymer are identified (for example, via monosaccharide composition), but the exact structures, the substituents, and the linkage connecting them to the backbone may be undefined. In addition, the purity of the molecules may vary. Purification protocols of macroalgae polysaccharides are often separated into the preparation of biomass (a first step that includes cleaning with water, drying, and milling processes) and extraction of the polysaccharide fraction using solvents, which may be followed by further purification by, e.g., chromatographic or membrane filtration techniques.19 In the extraction, dried, milled biomass is treated with a mixture of water and organic solvents (mainly ethanol, methanol, chloroform, and acetone). The solvent selection is dependent upon the targeted polysaccharide), but the aim is to enrich the polysaccharides and remove lipids, proteins, phenols, mannitol, and chlorophyll. Solvent extraction may be combined with novel techniques, such as microwave-assisted extraction, ultrasound-assisted extraction, and enzyme-assisted extraction. The desired polysaccharide can then be further purified by ionexchange chromatography, size-exclusion chromatography, affinity chromatography, or membrane filtration.19
GI tract, leading to production of oligo- or monosaccharides that can be further used by other species in the microbiota.4 Prehydrolysis (either enzymatic or by acids before intake) can also create oligosaccharides (shorter often soluble dietary fibers) that stimulate certain types of probiotics. These probiotics are unable to perform the first degradation of the polysaccharides but metabolize predigested oligosaccharides. Use of different combinations of compounds, substituted to different degrees and with different glycosidic bonds, will hence influence both which microbial species that are stimulated and the fermentation rate at which the species grow.
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MARINE MACROALGAL POLYSACCHARIDES The cell wall of macroalgae differ from cell walls of terrestrial plants because it has a lower proportion of fibrous polysaccharides compared to the matrix polysaccharides to provide flexibility and strength against the currents and wave motions.10 Some amounts of fibrous (crystalline) polysaccharide, interpreted as cellulose, has over the years been reported to be present in red, green, and brown algae (Figure 2). Crystalline glucans are, for example, reported from marine green algae of the genus Valonia (classified under Ulvophyceae). Recently, non-cellulosic crystalline structures that consist of mixed linkage glucans (MLGs) have been shown in brown algae (Phaeophyceae)18 that may replace cellulose in these species. Matrix polysaccharides are more abundant, and their composition depends upon the type of algae as well as the season. Some of the matrix polysaccharides are carboxylated 11546
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Table 1. Marine Microorganism-Derived EPSs and Pigments, Also Including Some Food Products That Are Available Today on the Market8,29−31 EPS, components (mol mass, yield) (producing microorganism) glucose, mannose (7 kDa, 0.2 g/L) (Aspergillus versicolor) homoglucan (nd, 22.34 g/L) (Cyanothece sp.) heteroglycan (0.13 MDa, nd) (Keissleriella sp. YS 4108) glucose, galactose (nd, 9.23 g/L) (Hahella chejuensis) mannose, glucose (0.4 MDa, nd) (Geobacillus thermodenitrificans) mannose, glucose, galacturonic acid (5.7 MDa, nd) ( Pseudoalteromonas sp. CAM025) (nd, 14 g/L) (Weissella cibaria) galactose, uronic acids (18.7 MDa, 0.13 g/L) (Cyrodinium impudicum) heteroglycan (sulfated) (2.3 MDa, nd) (Porphyridium sp.) heteroglycan (sulfated) (80 kDa, nd) (Rhodothermus marinus)
pigment (producing microorganism) β-carotene (Dunaliella salina, Synechococcus spp., Nannochloropsis gaditan) zeaxanthin (Paracoccus sp., Zeaxanthinibacter enoshimensis) violaxanthin (Dunaliella tertiolecta) fucoxanthin (Phaeodactylum tricornutum) violacein (Pseudoalteromonas tunicate) prodiginines (Pseudoalteromonas rubra, Pseudoalteromonas denitrificans) chlorophyll a (Nannochloropsis gaditan)
product available on the market (producing microorganism) ω-3 oil (Schizochytrium sp.) ω-3 DHA supplement (Schizochytrium sp.) astaxanthin (Spirulina platensis) multivitamin (Spirulina platensis) β-carotene (Dunaliella salina) polytoplankton powder (marine phytoplankton) assorted algae pastes (Tetraselmis, Nannochloropsis, Isochrysis)
glaukothalin (Proteobacteria spp.) eumelanin (Marinomonas mediterranea) lycopene (Streptomyces sp.)
in the polymer may vary. Also, laminarin chains are presented in two types named M (in which the chains end with 1-Osubstituted D-mannitol) and G (in which the chains end with glucose). It has been reported that laminarins have antibacterial properties, stimulate Bifidobacteria, and increase the production of SCFAs, especially propionic and butyric acids, in gut microbiota, giving the laminarins prebiotic potential.23 Laminarin has also been shown to promote immune responses, resulting in protection of the liver against injuries by reduction of lactate dehydrogenase and increase of glutamic pyruvic transaminase in normal mice in vivo.24 Fucoidans (fucans) are branched homo- and heterosulfated polysaccharides of L-fucose units in brown algae. The homosulfated fucoidans consist of two types of fucose backbone chains. Type I is composed of (1 → 3)-linked α-Lfucopyranoside residues, and type II consists of alternating α(1 → 3)- and α-(1−4)-L-fucopyranoside residues. These polysaccharides have been shown to display numerous physiological and biological activities, such as anticoagulant, antithrombocytic, antiviral, antitumor, immunomodulatory, antioxidant, and anti-inflammatory activities.3,4 Fucoidans also have a beneficial effect on gut microbiota by increasing probiotic species and increasing the concentration of total volatile fatty acids in the proximal and distal colon.23 Prebiotic activity of a mixture of fucoidans and alginates from the brown algae Ascophyllum nodosum has also been shown that resulted in an increase in the growth rate of Lactobacillus delbruecki and Lactobacillus casei in vitro. The observed growth rate was comparable to the growth rate after supplying the standard commercial prebiotic, inulin.15 Carrageenans are linear and high-molecular-weight sulfated polysaccharides of D-galactose units (joined by alternating α-1 → 3 and β-1 → 4 glycosidic linkages) from red algae and are approved as food additives. These polysaccharides have a lot of applications in the food industry, such as clarifiers of beverages and as thickening and stabilizing agents.25,26 They are watersoluble and can form thermoreversible gels or make viscous solutions in the vicinity of salts,19 and they can be used for encapsulation of probiotics.26 A recent study showed that polysaccharides (at a concentration of 0.1%) from the red algae Grateloupia filicina (GFP) and Eucheuma spinosum (ESP)
Brown algae have high amounts of water-soluble polysaccharides named laminarins, fucoidans, and alginates. Alginates (alginic acid or algin) are high-molecular-weight carboxylated polysaccharides and are the most abundant polysaccharides in brown algae. They are linear and composed of D-mannuronic acid (M) and L-guluronic acid (G, the C5 epimer of M) connected to each other by (1 → 4) glycosidic linkages with a 1,2-cis configuration, and the arrangement of the residues is either homopolymeric [polymannuronate (−MM−) or polyguluronate (−GG−)] or heteropolymeric (−MG−). The proportion between mannuronic and guluronic acid may however vary. Alginates are anionic polysaccharides and form a viscose gum through binding with water, which has led to extensive applications in food industries and as a biomaterial.7 Alginates have potential to be used as dietary fibers,20 and use of oligosaccharides produced from these polymers have resulted in an increased ratio of beneficial gut microbiota (stimulating both Lactobacilli and Bifidobacteria). It is also reported that alginates can reduce the protein degradation, and this proteolytic inhibition can result in reduction of the glycemic load from amino acids and, consequently, reduction in the glycemic index that may have beneficial health effects on overweight people or people with impaired glucose tolerance.20,21 Alginates from edible macroalgae have also shown an inhibitory effect on porcine pancreatic α-amylase and, consequently, prevention of hyperglycaemia based on in vitro experiments.22 Moreover, alginates have shown other positive effects, such as reduction of blood cholesterol and the blood glucose level, increase in the plasma insulin level, reduction of toxic agents in the GI lumen (obtained by binding them), wound healing, and immunostimulation.20 This evidence shows that alginates can both result in prebiotic effects and other beneficial bioactivities. However, the exact structures of the molecules resulting in these effects are seldom reported (although oligomerization of the polymer may be necessary to reach the prebiotic effect), and data are often obtained from purified or commercially available polymers. Laminarins (or laminarans) are linear low-molecular-weight polysaccharides (5 kDa) composed of glucose units with a low degree of branching (β-1 → 3 linkages with 1 → 6 branches) and serve to store energy.3 The branching degree and position 11547
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Journal of Agricultural and Food Chemistry significantly promoted growth of Bifidobacteria. The main monomer of GFP and ESP polysaccharides was galactose, which was proposed to form prebiotic galacto-oligosaccharides.27 Ulvans are water-soluble sulfated heteropolysaccharides of different monosaccharides from green algae. The monosaccharide composition of the polymer is dependent upon the algae source and ecophysiological variation, but they are in principle composed of L-rhamnose, L-xylose, and D-glucuronic and L-iduronic acids.7 They are considered as dietary fibers because they cannot be digested in the upper GI tract. Ulvans contain sulfate and uronic acids, and thus, they have ionexchange capacity and can bind to bile acids and, consequently, increase the excretion of bile acids with cholesterol-lowering or antihyperlipidemic activity.28
saccharides for health-promoting purposes. Studies made to date on polysaccharides originating from these marine resources have shown interesting effects on health and, consequently, can have significant potential to be used as food or feed ingredients directly in the biomass or after refining as ingredients for different purposes. Use of both macroalgae and marine microorganisms together will enable us to produce novel prebiotics as well as bioactive compounds. Despite the increased interest and significant development, there are still gaps in our knowledge, especially on the structural details that induce the specific prebiotic or bioactivity functions (often reported for the same polysaccharide type). Therefore, despite the knowledge that we have gained on the different marine poly- and oligosaccharides to date, it is clear that a further understanding of the exact composition and distribution of substituents is needed to fully grasp their role as healthpromoting and prebiotic compounds. Thus, further studies on purified and analytically defined components are essential to decipher the exact role of the different components and the need of diversity in structure and substituents in these molecules.
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MARINE MICROBIAL EXOPOLYSACCHARIDES A lot of attention has been given to marine microbial species as potential suppliers of pigments and polyunsaturated fatty acids (Table 1). However, there are also marine bacteria with many interesting products, including potential prebiotic exopolysaccharides (EPSs) from the genera Lactobacillus, Enterococcus, Lactococcus, and Pediococcus as well as candidates from less investigated genera, such as Caranobacterium, Marinilactobacillus, Rhodothermus, and Halolactobacillus spp.8,29 (Table 1). Recently, EPSs from marine microorganisms have attracted the attention of scientists because the marine environment provides a large variety of microorganisms that produce almost half of the organic substances on the Earth.30 EPSs produced by marine microorganisms have special roles in protecting their producing microorganism, which relate to their ecological and physiological functions. Such EPSs can have widespread applications in the food industry as a result of their stabilizing, gelling, and emulsifying properties and also antitumor, antiulcer, immunomodulating, and cholesterol-lowering activities.31 The marine EPSs also have potential as prebiotics because many of them are non-digestible in the upper GI tract and some of them have also been experimentally proven to have prebiotic potential. Hongpattarakere et al. have, for example, reported the prebiotic activity of microbial EPS, produced by lactic acid bacteria isolated from shrimps, fish, and shellfish.31 These EPSs were purified by ethanol precipitation from microbial cultures, which is a common way to isolated EPSs from bacteria.29,31 More detailed characterization of the EPSs would give us further understanding on the molecular structures important for the prebiotic properties observed. Recent investigations have also shown that EPSs of some marine microbes are sulfated, such as the EPS from the marine thermophile Rhodothermus marinus.29 Sulfated EPSs have shown different biological activities, including anticoagulant, antiviral, and anti-inflammatory activities.30 Thus, the marine EPSs have been pursued for commercialization as a result of their unique properties, such as emulsifying or displaying biological activity, which give them great potential in food, pharmaceutical, medical, and biotechnological industries.
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. ORCID
Eva Nordberg Karlsson: 0000-0002-8597-7050 Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS Support from the Swedish Research Council Formas (Grant 2015-769), Era-net in Marine Biotechnology (Thermofactories) and SusFood2 (ProSeaFood), and the EU Horizon2020 BBI Project Macro Cascade (Grant 720755) is highly appreciated.
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