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Marine poly- and oligosaccharides as prebiotics Roya Sardari, and Eva Nordberg Karlsson J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.8b04418 • Publication Date (Web): 11 Oct 2018 Downloaded from http://pubs.acs.org on October 12, 2018

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Journal of Agricultural and Food Chemistry

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Marine poly- and oligosaccharides as prebiotics

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Roya R R Sardari and Eva Nordberg Karlsson

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Biotechnology, Department of Chemistry, Lund University, PO Box 124, 221 00 Lund, Sweden

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Abstract

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The marine environment can increase the global production of biomass. Interest in marine

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macroalgae and microorganisms has increased tremendously due to international agendas and

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market trends promoting sustainability as well as healthy food. Macroalgae and marine

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microorganisms contain unique poly- and oligosaccharides with different substitutions e.g.

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sulfation or carboxylation. There is a great potential to find prebiotic compounds from these

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marine-derived saccharides. However, the exact composition and substituent distribution needed

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for the activity is to a large extent unexplored. In depth investigations of these compounds will

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provide us with novel insights on the specific structures required for the observed functions.

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Keywords: marine, prebiotics, dietary fiber, macroalgae, polysaccharide, gut microbiota

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Introduction

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Sustainable production of agricultural resources for food and food additives is facing significant

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challenges due to increasing world population and limitations in cultivable land. Thus, there is a

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need to explore alternative production sites and food sources that have high capacity as well as low

ACS Paragon Plus Environment


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fertilization need. The seas and oceans (that make up 71% of the surface of the earth) have always

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been a resource for food and contain complex ecosystems making up valuable biodiversity 1,2.

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From this system, algae biomass can be used directly or as components in food and non-food

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applications. Macroalgae contain different kinds of poly- and oligosaccharides, which can be used

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as food products and additives and which in many cases show health promoting properties

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Macroalgae (seaweeds) are already today used as food in Asia, where most of the global production

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takes place (28.3 million tonnes in 2014 5), but is only to a limited degree utilised in Europe and in

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the US, despite a significant production potential. Macroalgae are aquatic organisms, with high

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photosynthetic ability that belong to the lower plants, and it has been reported that they have higher

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productivity-rates than terrestrial biomass, such as corn and switchgrass 6. Macroalgae are

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classified as green algae (Chlorophyta and Charophyta, the latter with mainly fresh water species)

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red algae (Rhodophyta) and brown algae (Phaeophyta), in accordance with their respective thallus

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colour, which is derived from natural pigments and chlorophylls. Many potential health promoting

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activities in macroalgae such as prebiotic, antibacterial, antioxidant, and anti-inflammatory

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properties have been linked to their poly- and oligosaccharides 4,7.

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In addition, marine microorganisms are named the lung of planet due to the production of more

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than 50% of the earth oxygen. Typical marine microorganisms are bacteria (in the phyla

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Actinobacteria,

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Basidiomycota, Chytridiomycota) including yeasts (originating from several genera in both

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Ascomycota and Basidiomycota), microalgae and diatoms [in phyla classified under Heterokonta,

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and in Dinoflagellata (classified under Alveolata)]. The marine microorganisms are living in

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different places of the oceans and produce unique molecules, of which some have broad

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applications in pharmaceutical industry 8.

Firmicutes,

Cyanobacteria,

and

Proteobacteria),


fungi

2,3,4.

(Ascomycota,

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The ageing population and the lifestyle-related diseases have created a demand for more knowledge

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about, and better access to, healthy food and food additives. Prebiotics (first identified and named

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by Gibson & Roberfroid 9) are non-digestible food ingredients that stimulate growth and/or activity

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of health promoting bacteria (probiotics) in the digestive system in humans and animals. In this

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way, prebiotic compounds modulate the gut microbiota to a more health promoting species

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distribution that e.g. results in release of bioactive, immuno-stimulating compounds.

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The marine environment can both increase the global biomass production, and supply resources

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(i.e. marine macroalgae and microorganisms) rich in prebiotic and bioactive compounds 3,10, which

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is in line with the United Nations global sustainability goals for 2030 (e.g. eliminating hunger,

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securing access to food, reducing food waste, achieving improved nutrition, promoting sustainable

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farming and water use) 11. This makes it worthwhile to highlight marine macroalgae as a source of

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prebiotic poly- and oligosaccharides, and to also pay attention to marine microorganisms, as

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producers of interesting exopolysaccharides that can further increase the product potential from

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marine environments. The importance of the exact poly- and oligosaccharide structures for the

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prebiotic function and/or bioactivity (both prebiotic properties and bioactivity are often reported

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for the same type of polymer) is however to a large extent unexplored, and more research is needed

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to highlight the importance of substituents and the exact molecular structures needed for specific

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functions.

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Prebiotics and the human gastrointestinal tract

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The microbiota of the human gastrointestinal (GI) tract is a complex system that has been the

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subject of many reviews. Recently, Thursby & Juge

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analysis via whole-genome shotgun metagenomics (e.g. MetaHit and the Human Microbiome

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highlighted that improved techniques for



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Project) led to identification of 2172 species isolated from human beings, including 386 strict

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anaerobes, the latter most likely found in the large intestine 12,13. The different species identified in

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humans were classified into 12 different phyla, of which more than 90 % belonged to

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Proteobacteria, Firmicutes, Actinobacteria and Bacteroidetes. Some of these species play very

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important roles in human health such as providing nutrients, protecting against pathogens, and

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modulating the host metabolism and immune system by secretion of metabolites. The species

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distribution, diversity and metabolic outputs of the gut microbiota thus affects the host in a way

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that can be either beneficial or harmful. Several microbial species from Firmicutes and

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Actinobacteria have for example been proposed to play beneficial (probiotic) roles (Figure 1) 14.

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The distribution of species in the gut can be influenced by intake of prebiotics. To be classified as

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prebiotics, the compounds should survive the small intestinal digestion but be substrates for gut

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microbiota in a way that is favorable for the host health. The prebiotic activity of a compound is

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evaluated based on three criteria; 1. compound resistance against digestibility in the upper

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gastrointestinal tract, 2. microbial fermentation of the compound by gut bacteria, and 3. increased

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growth of beneficial gut bacteria (probiotics), leading to stimulation of the host metabolism in a

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beneficial way

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metabolites (e.g. short chain fatty acids, SCFA) that interact with human intestinal and

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immunomodulating cells. Presence of country-specific microbial species signatures in human

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gastrointestinal tracts, show that the composition of the gut microbiota is influenced by our diet as

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well as by other, less known, host-specific factors

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favorable balance and more growth of the beneficial species are to use foods and food ingredients

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with prebiotic properties, shown to influence the microbiota (at least during the period of intake)

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3,9.

. The probiotic species utilize the prebiotics in their metabolism and secrete

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12,13.

Hence, important strategies to get a


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https://fineartamerica.com/featured/4lactococcus-lactis-scimat.html

L. lactis subsp.lactis

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http://probioticsdb.com/probiotic -strains/pediococcus-acidilacti/

P. acidilactici

http://www.bacteriainphotos.com/ streptococcus_pyogenes_3D.html

S. thermophilus

Bacillus ( convert glucose & pyruvate to lactate, acetate, ethanol, & 2,3 butanediol)

B. infantis B. animalis (subsp.lactic) B. bifidum B. longum B. breve

Streptococcus (convert fructose, glucose, lactose, mannose, and sucrose to lactic acid)

L. rhamnosus L. acidophilus L. plantarum L. casei L. delbrueckii (subsp. bulgaricus) L. brevis L. johnsonii L. fermentum L. reuteri

https://microbewiki.kenyon.edu/index.php/File :Bifidobacteriumxtina.png

Leuconostoc (convert hexoses, pentoses, & disaccharides to lactate, acetate, & ethanol)

/lactobacillus-casei/

Bifidobacterium (convert starch , starch hydrolysates,oligosaccharides to short chain fatty acids)

http://www.mysticalbiotech.com/portfolio

Pediococcus (convert glucose as major substrate to lactic acid)

Lactococcus (convert sugars mainly glocose & lactose to lactic acid)

Lactobacillus (convert hexose sugars to lactic acid)

5

http://www.nyrture.com/blog/2015/5/23 /the-subtle-beauty-of-bacillus-subtilis-part-ii

B. coagulans B. subtilis B. cereus

L. mesenteroides https://microbewiki.kenyon.edu/index.php/Fil e:Leuconostoc_Mesenteroides.jpeg

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Figure 1: Microbial genera from Firmicutes and Actinobacteria found in the gastrointestinal tract with proposed

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probiotic properties 9,14.

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The fermentation rate of the prebiotic compounds is also of importance. A slower fermentation

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rate, may for example be desirable, leading to less discomfort (e.g. less flatulence). The

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fermentation rate may be affected (often slowed down) by substituents on the prebiotic compounds.

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Most of the polysaccharides used in our diet today, originate from terrestrial plant cell walls 16 that

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are either digestible or non-digestible (dietary fibers). Various dietary fibres [host non-digestible

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polysaccharides (degree of polymerization (DP) >20) or oligosaccharides (DP 2 - 19)] are

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promising as prebiotics, and originate from many different sources 3,9,16,17 including species from

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marine environments. The glycosidic bonds joining the monosaccharides in the dietary fibres can

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be hydrolyzed by enzymes, produced by microorganisms in the GI-tract, leading to production of

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oligosaccharides or monosaccharides that can be further utilized by other species in the microbiota ACS Paragon Plus Environment


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4.

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(shorter often soluble dietary fibres) that stimulate probiotics. These probiotics are unable to

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perform the first degradation of the polysaccharides, but metabolize predigested oligosaccharides.

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Use of different combinations of compounds, substituted to different degrees and with different

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glycosidic bonds, will hence influence both which microbial species that are stimulated, and the

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fermentation rate at which the species grow.

Prehydrolysis (either enzymatic or by acids before intake) can also create oligosaccharides

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Marine macroalgal polysaccharides

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The cell wall of macroalgae differ from cell walls of terrestrial plants as it has a lower proportion

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of fibrous polysaccharides compared to the matrix polysaccharides in order to provide flexibility

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and strength against the currents and wave motions

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polysaccharide, interpreted as cellulose, has over the years been reported to be present in red, green,

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and brown algae (Figure 2). Crystalline glucans, are for example reported from marine green algae

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of the genus Valonia (classified under Ulvophyceae). Recently, non-cellulosic crystalline

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structures that consist of mixed linkage glucans (MLG) have been shown in brown algae

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(Phaeophyceae)18 that may replace cellulose in these species.

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Matrix polysaccharides are more abundant, and their composition depends on the type of algae, as

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well as on the season. Some of the matrix polysaccharides are carboxylated (e.g. alginate) or

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sulfated (e.g. fucoidan and ulvan) 7, i.e. they carry substituents that may affect their fermentability.

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The most common and known algae polysaccharides are alginates, laminarins and fucoidans (from

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brown algae), carrageenans and agar (from red algae), and ulvans (from green algae) (Figure 2),

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but even for these compounds the exact composition, substituent distribution, and distribution of

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glycosidic linkage types differ between species and varies between seasons. Frequently the main

10.

Some amounts of fibrous (crystalline)


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components in the polymer are identified (for example via monosaccharide composition), but the

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exact structures, the substituents and the linkage connecting them to the backbone, may be

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undefined. In addition, the purity of the molecules may vary.

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Purification protocols of macroalgae polysaccharides are often separated into preparation of

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biomass (a first step that includes cleaning with water, drying, and milling processes) and extraction

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of the polysaccharide fraction using solvents, which may be followed by further purification by

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e.g. chromatographic or membrane filtration techniques 19. In the extraction, dried, milled biomass

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is treated with a mixture of water and organic solvents (mainly ethanol, methanol, chloroform, and

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acetone). The solvent selection is dependent on the targeted polysaccharide), but the aim is to enrich

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the polysaccharides and remove lipids, proteins, phenols, mannitol, and chlorophyll. Solvent

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extraction may be combined with novel techniques such as microwave-assisted extraction,

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ultrasound-assisted extraction, and enzyme assisted extraction. The desired polysaccharide can

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then be further purified by ion exchange chromatography, size exclusion chromatography, affinity

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chromatography, or membrane filtration 19.



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Ciliates, Dinoflagellates

Brown algae (Phaeophyta) Class Phaeophyceae, include the large orders: Fucales (Sargassum and Fucus spp) and Laminariales (kelps e.g. Ascophyllum, Laminaria and Saccharina spp) 10-75% total polysaccharides/ biomass dry weight (DW). Polysaccharides (shown prebiotic effect): Alginate (stimulation of Bifidobacteria, immune stimulation) Fucoidans (stimulation of Lactobacilli, immune stimulation) Laminarin (mucin stimulation, Lactobacilli stimulated in mixtures with fucoidan, immune stimulation) MLGlucan (fibrous)

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Red algae (Rhodophyta) >7,000 species with the majority in the class Florideophyceae, including Eucheuma spp, (carrageenan production) Gracilaria spp (agar production) and the edible Palmaria palmata. 10-59% total polysaccharides / biomass DW.

Haptophyta

Green algae (Chlorophyta)

Fungi

Animals

Green plants

4 main classes including the class Ulvophyceae, with the multicellular edible species Ulva lactuca and Codium fragile.

Polysaccharides (shown prebiotic effect): Carrageenan (immunestimulation) Agar (immunestimulation) Porphyran MLglycans (xylans) Mannans Glucans (Floridean starch, cellulose)

29-67% total polysaccharides/biomass DW. Polysaccharides (shown prebiotic effect): Ulvans (immunestimulation) Xyloglucans Mannans Glucuronans Glucans (e.g. cellulose, starch)

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Figure 2. Schematic phylogenetic tree (not drawn to scale) of marine macro algae. The figure is giving examples of

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some well-known species and major polysaccharides occurring in brown, red and green algae. The Charophyta group

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of green algae is not shown in the chart, as the majority of these species thrive in fresh water. The total polysaccharide

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content in macroalgae range from approximately 10% to 75% of the seaweed dry weight, but both total and species-

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specific polysaccharides show seasonal variation. Generally, species of brown algae contain alginic acid, fucoidan

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(sulfated fucose), and laminaran (β-1,3 glucans). Species of red algae contain differing amounts of carrageenans, agars,

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xylans, floridean starch (amylopectin-like glucan), and water-soluble sulfated galactans. Green algae contain sulfated

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polysaccharides (galactans and xylans). Some examples of reported prebiotic effects are given next to polysaccharides

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used for trials on prebiotic effects. ML = mixed linkage.

150 151

Brown algae have high amounts of the water soluble polysaccharides named laminarins, fucoidans,

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and alginates. Alginates (alginic acid or algin), are high molecular weight carboxylated

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polysaccharides and are the most abundant polysaccharides in brown algae. They are linear and

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composed of D-mannuronic acid (M) and L-guluronic acid (G, the C5 epimer of M) connected to

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each other by (1→4) glycosidic linkages with a 1,2-cis configuration and the arrangement of the ACS Paragon Plus Environment

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residues is either homopolymetric (polymannuronate (-MM- or polyguluronate (-GG-) or

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heteropolymetric (-MG-). The proportion between mannuronic and guluronic acid may however

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vary. Alginates are anionic polysaccharides and form a viscose gum through binding with water,

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which has led to extensive applications in food industries and as a biomaterial 7. Alginates have

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potential to be used as dietary fibers 20, and use of oligosaccharides produced from these polymers

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have resulted in an increased ratio of beneficial gut microbiota (stimulating both Lactobacilli and

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Bifidobacteria). It is also reported that alginates can reduce the protein degradation and this

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proteolytic inhibition can result in reduction of glycemic load from amino acids and consequently

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reduction in glycemic index that may have beneficial health effects on overweight people or people

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with impaired glucose tolerance 20,21. Alginates from edible macroalgae, have also shown inhibitory

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effect on porcine pancreatic α-amylase and consequently prevention of hyperglycaemia based on

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in vitro experiments22. Moreover, alginates have shown other positive effects, such as reduction of

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blood cholesterol and blood glucose level and increase in plasma insulin level, reduction of toxic

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agents in the gastrointestinal lumen (obtained by binding them), wound healing, and

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immunostimulation 20. This evidence shows that alginates can both result in prebiotic effects, and

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other beneficial bioactivities. However, the exact structures of the molecules, resulting in these

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effects are seldom reported (although oligomerization of the polymer may be necessary to reach

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the prebiotic effect) and data is often obtained from purified or commercially available polymers.

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Laminarins (or laminarans) are linear low molecular weight polysaccharides (5kDa) composed of

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glucose units with low degree of branching (β 1→3 linkages with 1→6 branches) and serve to store

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energy 3. The branching degree and position in the polymer may vary. Also, laminarin chains are

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presented in two types named M (in which the chains end with 1-O-substituted D-mannitol) and G

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(in which the chains end with glucose).



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It has been reported that laminarins have antibacterial properties, stimulate Bifidobacteria, and

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increase the production of short chain fatty acids, especially propionic and butyric acids in gut

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microbiota giving the laminarins prebiotic potential 23. Laminarin has also been shown to promote

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immune responses, resulting in protection of the liver against injuries by reduction of lactate

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dehydrogenase and increase of glutamic pyruvic transaminase in normal mice in vivo 24.

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Fucoidans (fucans) are branched homo- and hetero-sulfated polysaccharides of L-fucose units in

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brown algae. The homo-sulfated fucoidans consist of two types of fucose backbone chains. Type I

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is composed of (1→3)-linked α-L-fucopyranoside residues and type II consists of alternating α-

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(1→3)- and α-(1-4)-L-fucopyranoside residues. These polysaccharides have been shown to display

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numerous physiological and biological activities such as anticoagulant, antithrombocytic, antiviral,

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antitumor, immunomodulatory, antioxidant, and anti-inflammatory activities

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have beneficial effect on gut microbiota by increasing probiotic species and by increasing the

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concentration of total volatile fatty acids in the proximal and distal colon 23. Prebiotic activity of a

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mixture of fucoidans and alginates from the brown algae Ascophyllum nodosum, has also been

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shown that resulted in an increase in the growth rate of L. delbruecki and L. casei in vitro. The

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observed growth rate was comparable with the growth rate after supplying the standard commercial

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prebiotic, inulin 15.

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Carrageenans are linear and high molecular weight sulfated polysaccharides of D-galactose units

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(joined by alternating α-1→3 and β-1→4 glycosidic linkages) from red algae and are approved as

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food additives. These polysaccharides have a lot of applications in food industry such as clarifiers

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of beverages and as thickening and stabilizing agents

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thermoreversible gels or make viscous solutions in the vicinity of salts 19, and they can be used for

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encapsulation of probiotics 26. A recent study showed that polysaccharides (at a concentration of

25,26.

3,4.

Fucoidans also

They are water soluble and can form


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0.1%) from the red algae Grateloupia filicina (GFP) and Eucheuma spinosum (ESP) significantly

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promoted growth of Bifidobacteria. The main monomer of GFP and ESP polysaccharides was

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galactose, which was proposed to form prebiotic galacto-oligosaccharides 27.

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Ulvans are water soluble sulfated heteropolysaccharides of different monosaccharides from green

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algae. The monosaccharide composition of the polymer is dependent on the algae source and

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ecophysiological variation, but they are in principle composed of L-rhamnose, L-xylose, D-

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glucuronic and L-iduronic acid 7. They are considered as dietary fibers as they cannot be digested

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in the upper gastrointestinal tract. Ulvans contain sulfate and uronic acids and thus they have ion-

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exchange capacity and can bind to bile acids and consequently increase the excretion of bile acids

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with cholesterol lowering or antihyperlipidemic activity 28.

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Marine microbial exopolysaccharides

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A lot of attention has been given to marine microbial species, as potential suppliers of pigments

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and polyunsaturated fatty acids (Table 1). However, there are also marine bacteria with many

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interesting products, including potential prebiotic exopolysaccharides (EPS) from the genera

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Lactobacillus, Enterococcus, Lactococcus, and Pediococcus as well as candidates from less

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investigated genera such as Caranobacterium, Marinilactobacillus, Rhodothermus and

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Halolactobacillus spp 8,29 (Table 1). Recently EPS from marine microorganisms have attracted the

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attention of scientists since the marine environment provide a large variety of microorganisms

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which produce almost half of the organic substances on the earth

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microorganisms have special roles in protecting their producing microorganism which relate to

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their ecological and physiological functions. Such EPS can have widespread applications in food

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industry due to their stabilizing, gelling, and emulsifying properties and also antitumor, antiulcer, ACS Paragon Plus Environment

30.

EPS produced by marine


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immuno-modulating and cholesterol-lowering activities

The marine exopolysaccharides also

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have potential as prebiotics since many of them are non-digestible in the upper gastrointestinal tract

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and some of them have also been experimentally proven to have prebiotic potential.

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Hongpattarakere et al. have for example reported the prebiotic activity of microbial EPS, produced

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by lactic acid bacteria isolated from shrimps, fish and shellfish 31. These EPS were purified by

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ethanol precipitation from microbial cultures, which is a common way to isolated EPS from

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bacteria 29,31. More detailed characterization of the EPS would give us further understanding on the

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molecular structures important for the prebiotic properties observed.

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Recent investigations have also shown that EPS of some marine microbes are sulfated, such as the

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EPS from the marine thermophile Rhodothermus marinus 29. Sulfated EPS have shown different

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biological activities, including anticoagulant, antiviral and antiinflammatory activities 30. Thus, the

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marine EPS have been pursuing for commercialization due to their unique properties such as

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emulsifying or displaying biological activity which give them great potential in food, pharmacy,

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medical, and biotechnology industries.

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Table 1: Marine microorganism-derived exopolysaccharides and pigments, also including some food products that are

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today available on the market 8,29-31


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Exopolysaccharide components Mol mass, yield (producing microorganism)

Pigment (producing microorganism)

Glucose, mannose 7 kDa, 0.2 g/l (Aspergillus versicolor)

ß-Carotene (Dunaliella salina, Synechococcus spp,. Nannochloropsis gaditan)

Omega-3 oil (Schizochytrium sp.)

Homoglucan n.d., 22.34 g/l (Cyanothece sp)

Zeaxanthin (Paracoccus sp., Zeaxanthinibacter enoshimensis)

Omega-3 DHA supplement (Schizochytrium sp.)

Heteroglycan 0.13 MDa, n.d. (Keissleriella sp. YS 4108)

Violaxanthin (Dunaliella tertiolecta)

Astaxanthin (Spirulina platensis)

Glucose. Galactose n.d., 9.23 g/l (Hahella chejuensis)

Fucoxanthin (Phaeodactylum tricornutum)

Mannose, glucose 0.4 MDa, n.d. (Geobacillus thermodenitrificans)

Violacein (Pseudoalteromonas tunicate)

Mannose, glucose, galacturonic acid 5.7 MDa, n.d. (Pseudoalteromonas sp. CAM025)

Prodiginines (Pseudoalteromonas rubra, Pseudoalteromonas denitrificans )

Polytoplankton powder (Marine phytoplankton)

n.d., 14 g/l (Weissella cibaria)

Chlorophyll a (Nannochloropsis gaditan)

Assorted algae pastes (Tetraselmis, nannochloropsis, isochrysis)

Galactose, uronic acids 18.7 MDa, 0.13 g/l (Cyrodinium impudicum)

Glaukothalin (Proteobacteria spp).

Heteroglycan (sulfated) 2.3 Mda, n.d. (Porphyridium sp.)

Eumelanin (Marinomonas mediterranea)

Heteroglycan (sulfated) 80 kDa, n.d. (Rhodothermus marinus)

Lycopene (Streptomyces sp.)

Product available on market (producing microorganism)

Multi-vitamin (Spirulina platensis) ß-Carotene (Dunaliella salina)

243 244

Need of future research

245

It is clear that marine environments, as a source of diverse organic compounds, can supply us with

246

a number of beneficial and health promoting ingredients. This has resulted in renewed research

247

interest in the use of macroalgal polysaccharides for health promoting purposes. Studies made to

248

date on polysaccharides originating from these marine resources have shown interesting effects on

249

health, and consequently can have significant potential to be used as food or feed ingredients,

250

directly in the biomass, or after refining as ingredients for different purposes. Use of both

251

macroalgae and marine microorganisms together will enable us to produce novel prebiotics as well

252

as bioactive compounds. Despite the increased interest and significant development, there are still



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gaps in our knowledge, especially on the structural details that induce the specific prebiotic or

254

bioactivity functions (often reported for the same polysaccharide type). So, despite the knowledge

255

we have gained on the different marine poly- and oligosaccharides to date, it is clear that further

256

understanding of the exact composition and distribution of substituents is needed to fully grasp

257

their role as health promoting and prebiotic compounds. Thus, further studies on purified and

258

analytically defined components are essential to decipher the exact role of the different

259

components, and the need of diversity in structure and substituents in these molecules.

260

261

Acknowledgements

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Support from the Swedish research council Formas (grant 2015-769), Era-net in Marine

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Biotechnology (Thermofactories) and SusFood2 (ProSeaFood), and the EU Horizon2020 BBI

264

project Macro cascade (grant 720755) is highly appreciated.

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References

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For Table of contents only:

MARINE ENVIRONMENT MACROALGAE

MARINE MICROORGANISMS

CELL WALL POLYSACCHARIDES

EXOPOLYSACCHARIDES

PREBIOTICS ANTI-OXIDANT ACTIVITY

ANTI-DIABETIC EFFECTS CARDIOVASCULAR BENEFITS

IMMUNE STIMULATION

342 343 344 345


Marine poly- and oligosaccharides as prebiotics - Journal of

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