Next Article in Journal
An Alkaloid from a Highly Invasive Seaweed Increases the Voracity and Reproductive Output of a Model Fish Species
Previous Article in Journal
Fluorescently Labeled α-Conotoxin TxID, a New Probe for α3β4 Neuronal Nicotinic Acetylcholine Receptors
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Marine Drugs
Volume 20
Issue 8
10.3390/md20080512
marinedrugs-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Exopolysaccharides from Marine Microbes: Source, Structure and Application

by
Mingxing Qi
1,
Caijuan Zheng
2,3,
Wenhui Wu
1,*,
Guangli Yu
4,5,* and
Peipei Wang
1,*
1
College of Food Science and Technology, Shanghai Ocean University, Shanghai 201306, China
2
Key Laboratory of Tropical Medicinal Resource Chemistry of Ministry of Education, College of Chemistry and Chemical Engineering, Hainan Normal University, Haikou 571158, China
3
Key Laboratory of Tropical Medicinal Plant Chemistry of Hainan Province, Haikou 571158, China
4
Key Laboratory of Marine Drugs, Ministry of Education, Shandong Provincial Key Laboratory of Glycoscience and Glycoengineering, School of Medicine and Pharmacy, Ocean University of China, Qingdao 266237, China
5
Laboratory for Marine Drugs and Bioproducts of Qingdao Pilot National Laboratory for Marine Science and Technology, Qingdao 266237, China
*
Authors to whom correspondence should be addressed.
Mar. Drugs 2022, 20(8), 512; https://doi.org/10.3390/md20080512
Submission received: 24 June 2022 / Revised: 10 August 2022 / Accepted: 11 August 2022 / Published: 12 August 2022
(This article belongs to the Topic Advances on the Extraction, Functionalities and Applications of Polysaccharides)
Browse Figures
Review Reports Versions Notes

Abstract

:
The unique living environment of marine microorganisms endows them with the potential to produce novel chemical compounds with various biological activities. Among them, the exopolysaccharides produced by marine microbes are an important factor for them to survive in these extreme environments. Up to now, exopolysaccharides from marine microbes, especially from extremophiles, have attracted more and more attention due to their structural complexity, biodegradability, biological activities, and biocompatibility. With the development of culture and separation methods, an increasing number of novel exopolysaccharides are being found and investigated. Here, the source, structure and biological activities of exopolysaccharides, as well as their potential applications in environmental restoration fields of the last decade are summarized, indicating the commercial potential of these versatile EPS in different areas, such as food, cosmetic, and biomedical industries, and also in environmental remediation.

Graphical Abstract

1. Introduction

Marine microorganisms, as important members of marine organisms, can produce numerous specific active substances in an extreme environment in low temperature, high salt, high pressure, and oligotrophic conditions. They have gained scientific interest due to their potential applications in the pharmaceutical, cosmetic and food industries, for environmental remediation, and astrobiology [1,2,3,4,5].
Exopolysaccharides (EPS), are high molecular weight carbohydrate polymers, which are secreted by microorganisms in the process of growth and metabolism [6,7,8,9,10,11,12]. The complex and diverse structure of EPS endows them with unique biological activities and functions [13,14,15,16]. Now, EPS, as a major active component of marine microbial resources [5,17], have become a new research hotspot, with advances in modern separation and analysis techniques [12,18,19,20,21,22,23,24]. First, because the EPS are produced by marine microorganisms, this is an important factor for them to survive in these extreme environments, such as high pressure, high temperatures, and high salinity [25]. Several pieces of evidence have indicated that the monosaccharide composition, high molecular weight, hydrophobicity and polycharged characteristics of marine EPS are involved in their cryoprotective effect, water-holding capacity, and good thermostability, which are essential for the survival of these psychrophiles, halophiles, and thermophiles [1,26,27,28,29,30]. In addition, the EPS from marine microbes have aroused more and more attention and are explored in the food industry, cosmetics, and biological medicine due to their unique properties, such as structural complexity, biodegradability, biological activities, and biocompatibility [31]. For example, HYD 657, also called deepsane, which was produced and secreted by the marine Alteromonas macleodii subsp. fijiensis biovar deepsane, has already been used in cosmetics for soothing and reducing the irritation of sensitive skin against chemical, mechanical, and UVB aggressions [32]. Levan, isolated from H. smyrnensis AAD6T, native and derivatives, showed high compatibility and anticoagulant activity, which activity was similar to heparin, a clinical anticoagulant [33]. A novel EPS, named as EPS-S3 from marine bacterium Pantoea sp., could accelerate cutaneous wound healing via the Wnt/β-catenin pathway, indicating a prospective use as a new biomaterial for skin tissue regeneration [34]. Furthermore, EPS synthesized by microorganisms have many advantages over the other polysaccharides isolated from plants, animals, and algae [22], such as high structure reproducibility, which is not possible for most plant and animal sources, due to their polysaccharide structures dependent on climate, environmental and feed conditions [21]. In addition, the high yield of EPS can be achievable by optimizing culture conditions and using the techniques of synthetic biology, which is now a promising and new research field.
At present, although the physical properties of the marine microbial EPS are promising, the studies concerning their functional and biological activities are still scarce, compared to the exploitation and application of polysaccharides from terrestrial plants and microorganisms [1]. Here, this review emphasizes the research progress in the sources, chemical structural characteristics, and application of EPS from marine microorganisms in recent years, suggesting that these marine microbial EPS can be regarded as a new and promising source, with potential applications of biological activity and environmental remediation.

2. The Source of Marine EPS

2.1. EPS Produced by General Marine Environmental Microorganisms

Among the several types of aquatic microorganisms, marine microorganisms account for half of the production of organic matter on earth [35]. Up to now, many common marine strains which can produce EPS were identified, such as Pseudoalteromonas species [15,36], Bacillus species [37], Alteromonas species [38], and the Vibrio species [39]. Several EPS with various structural features and biological activities have been isolated from those common marine strains, which are shown in Table 1 [40,41,42,43,44,45,46,47,48,49,50]. For example, an EPS, produced by a novel probiotic Pediococcus pentosaceus M41, was isolated from a marine source [40]. An exopolysaccharide EPS273 from marine bacterium P. stutzeri 273 could inhibit biofilm formation and disrupt the established biofilms of P. aeruginosa PAO1, indicating that EPS273 had a promising prospect in combating bacterial biofilm-associated infection [49]. A bacterium Bacillus thuringiensis RSK CAS4 was isolated from the ascidian Didemnum granulatum, in which the condition of producing EPS was optimized by the response surface method [42]. An EPS-producing strain FSW-25, assigned to the genus Microbacterium, was isolated from the Rasthakaadu beach, Kanyakumari, which could produce a large quantity of EPS [50]. Recently, a strain of Bacillus cereus was isolated from the Saudi Red Sea coast. EPSR3 was a major fraction of the EPS from this marine strain, which showed antioxidant, antitumor, and anti-inflammatory activities. These biological activities of EPSR3 may be attributed to its content of uronic acids [51].
Moreover, the halophilic bacteria are known to produce EPS for withstanding the osmotic pressure. However, due to their ubiquitous distribution in saline environments, the exploration for biologically active novel EPS from halophilic bacteria is in its early stages. A bacterial EPS, named as A101 from the strain Vibrio sp.QY101, had antibiofilm activity [52]. An EPS named as HMEPS was first isolated from Halolactibacillus miurensis and had good antioxidant activity [53]. A novel EPS, designated hsEPS, was successfully isolated from the high-salt fermented broth of a novel species, Halomonas saliphila LCB169T. The structural of hsEPS was well-characterized as having a major backbone composed of (1→2)-linked α-D-Manp and (1→6)-linked α-D-Manp, with branches substituted at C-2 by T-α-D-Manp and at C-6 by the fragment of T-α-D-Manp-(1→2)-α-D-Manp-(1→ [54].

2.2. EPS Produced by Polar Microorganisms

Most microorganisms in the deep-sea and polar environment are affected by low temperatures and poor nutrition [64]. For the microorganisms living in a cold environment, it has been shown that their cells are almost surrounded by EPS [5]. The ability of organisms to survive and grow in a low-temperature environment depends on a series of adaptive strategies, including membrane structure modification. To understand the role of the membrane in adaptation, it is necessary to determine the cell wall components that represent the main components of the outer membrane, such as EPS. Studies have indicated that the secreted EPS with negatively charged residues, such as sulfate and carboxylic groups, allowed them to form hydrated viscous three-dimensional networks that confer adhesive and barrier properties against freezing temperatures [1]. For example, Ornella Carrión et al. isolated Pseudomonas ID1 from the marine sediment samples of Antarctica. The EPS produced by this strain showed significant protection against the cold [65]. The Pseudomonas sp. BGI-2 isolated from the glacier ice sample could produce high amounts of EPS, which had cryoprotective activity [66]. The produce condition of EPS from a cold-adapted marinobacter, namely as W1-16, was optimized by evaluating the influences of the carbon source, temperature, pH and salinity. The monosaccharide composition of this EPS resulted in Glc:Man:Gal:GalN:GalA:GlcA, with a relative molar ratio of 1:0.9:0.2:0.1:0.1:0.01 [67]. Now, several EPS isolated from psychrophilic bacteria in the Arctic and Antarctic marine environment have been reported, which have a potential application in the cryopreservation, food, and biomedical industries [21,26,55,56,57,58,59,60]. The source, structural, and biological information of these EPS are shown in Table 1.

2.3. EPS from Marine Hot Spring Microorganisms

Over the past decade, lots of microbes from marine hot springs have been reported, most of which produce special EPS to protect themselves from extreme conditions. These thermophilic microorganisms are classified as thermophiles growing at 55 °C~80 °C and hyperthermophiles growing above 80 °C. The thermophilic microorganisms contain multiple genera, such as Aeribacillus, Anoxybacillus, Brevibacillus, and Geobacillus [31]. The EPS produced by thermophilic bacteria usually have a high molecular weight with good emulsifying properties, leading to great potential application in the food and cosmetics industries [19,28,61,62,63]. Four thermophilic aerobic Bacillus isolated from Bulgarian hot springs are reported by Radchenkova et al., which are Aeribacillus pallidus, Geobacillus toebii, Brevibacillus thermoruber, and Anoxybacillus kestanbolensis. These bacteria can all produce EPS. After optimizing the culture conditions of the Aeribacillus pallidus strain 418, the output of EPS1 and EPS2 has more than doubled [31]. A novel exopolysaccharide RH-7 with a high molecular weight of 2000 kDa was produced by this marine bacterial strain assigned to the genus Rhodobacter from the surface of the marine macroalgae (Padina sp.). This EPS showed high-temperature resistance and could act as a bio-emulsifier to create a high pH and temperature-stable emulsion of hydrocarbon/water [61].

3. The Structural Characteristics of Marine EPS

3.1. Structural Characterization Methods of Marine Microbial EPS

The marine microbial EPS have high structural diversity and complexity. To evaluate their structure, the monosaccharide composition, molecular weight, and glycosidic linkage need to be determined. Before the structural analysis, a homogeneous EPS should be obtained to remove the influence of other salt, pigment, and protein impurities. At present, the commonly used purification methods of EPS include ethanol precipitation, ultrafiltration, ion-exchange chromatography, and gel chromatography. The methods of SDS-PAGE and DOC-PAGE with Alcian blue staining are very useful to detect the presence of EPS [68]. The monosaccharide composition of EPS has been determined by a variety of methods, including acid hydrolysis followed by appropriate derivatization and gas chromatography (GC); pre-column derivatization with high-performance liquid chromatography (HPLC); and high-performance anion-exchange chromatography with pulsed amperometric detection (HPAEC-PAD) [69,70]. The molecular weight can be determined by high-performance gel-permeation chromatography (HPGPC), combined with differential detector (ID) or multi-angle laser light scattering (MALS) [71]. Furthermore, through the data of the Fourier-Transform infrared spectroscopy (FTIR), methylation analysis, and nuclear magnetic resonance (NMR), the glycosidic bond-linking types and main functional groups can be obtained [26,72,73,74].
Besides these classical chemical procedures, new and powerful tools, such as zeta potential and particle-size analyzer, attenuated total reflectance Fourier-Transform infra-red spectroscopy (ATR-FTIR), differential scanning calorimetry (DSC), scanning electron microscope (SEM), atomic force microscopy (AFM), circular dichroism spectrum (CD), small-angle neutron scattering (SANS), and X-ray diffraction (XRD) techniques have been applied to investigate the surface morphology and physical properties of EPS [28,40,41,75,76,77,78]. For example, the physicochemical properties and rheological properties of an EPS-M41, produced by a novel probiotic Pediococcus pentosaceus M41 isolated from a marine source, were evaluated in detail. The average molecular weight of this EPS was determined to be 682.07 kDa by HPGPC method. The EPS-M41 consisted of Ara, Man, Glc, and Gal with a molar ratio of 1.2:1.8:15.1:1.0 by the GC method. The structure of the EPS-M41 was proposed as →3) α-D-Glc (1→2) β-D-Man (1→2) α-D-Glc (1→6) α-D-Glc (1→4) α-D-Glc (1→4) α-D-Gal (1→), with Ara linked at the terminals by FTIR and NMR analysis. The SEM analysis showed that the EPS-M41 possessed a unique compact, stiff and layer-like structure. The particle and zeta charges analyses exhibited that the EPS-M41 had a size diameter of 446.8 nm and a zeta potential of -176.54 mV. The DSC thermogram exhibited that the EPS-M41 had a higher melting point, indicating its resistance to the thermal processes [40]. Another example, the ATR-FTIR technique, was used to observe the movement of the -SH, -PO4, and -NH functional groups in the EPS from Pseudomonas pseudoalcaligenes NP103, and confirmed their involvement in the Pb (II) binding. The results emphasized the potential importance of P. pseudoalcaligenes NP103 EPS as a biosorbent for the removal of Pb (II) from the contaminated sites [28].

3.2. Examples of Marine Microbial EPS in the Last Decade

Several reviews have summarized the culture and fermentation conditions, distribution, biosynthesis, and biotechnological production of microbial EPS from marine sources [1,12,14,19,20,21,79,80,81]. In the past decade, with the development of separation and identification technology, numbers of new marine microorganisms have been identified. By optimizing the culture conditions, novel EPS with new biological activities have been discovered. Here, a variety of EPS obtained from marine microorganisms, including bacteria, fungi, and microalgae, in the last decade are summarized in Table 1, Table 2 and Table 3. It will give us more useful information of the structure–activity relationship of the marine EPS through the analysis of their origin, monosaccharide composition, molecular weight, and bioactivities.
The examples of EPS obtained from marine bacteria in the last decade are shown in Table 1. The marine microbial EPS are complex, and large polymers, usually composed of more than one monosaccharide, including pentoses, hexoses, amino sugars, and uronic acids. More commonly, they attach to proteins, lipids, or non-carbohydrate metabolites, such as pyruvate, sulphate, acetate, phosphates, and succinate, as their additional structural components, which increased their structural diversity and complexity [13]. Some of the monosaccharides, such as fucose, ribose, uronic acid and aminosaccharides, which are not common in plant polysaccharides, are widely found in the marine bacterial EPS. These special monosaccharides present are also closely related to the biological functions of these marine bacterial EPS. For instance, the structure of a novel EPS isolated from Colwellia psychrerythraea 34H was fullly characterized to have a repeating unit, composed of a N-acetyl-quinovosamine (QuiN) unit and two galacturonic acid residues both decorated with alanine amino acids, which had a significant cryoprotective effect. By NMR and computational analysis, the pseudo-helicoidal structure of this EPS may block the local tetrahedral order of the water molecules in the first hydration shell, and could inhibit the ice recrystallization [26]. A novel anionic EPS, named as FSW-25, was produced by marine Microbacterium aurantiacum. FSW-25 was a high molecular-weight heteropolysaccharide with a high uronic acid content. It had good antioxidant potential when compared with xanthan, which might be due to the presence of sulphate and its higher uronic content [50]. In addition, the monosaccharide composition of the EPS and other residues could play an essential role in thermostability. For example, the high thermal stability of EPS1-T14 produced by Bacillus licheniformis was mainly attributed to the fucose content [28,29]. The role of the monosaccharides’ composition in the thermal stability of the marine bacteria EPS has to be further investigated.
Compared with the diversity and complexity of the marine bacteria EPS, these EPS isolated from marine fungi exhibit less significant diversity in the monosaccharide composition (Table 2). The monosaccharide compositions show that these marine fungal EPS are mainly composed of neutral monosaccharide, including Glc, Man, and Gal with a different molar ratio. Generally, these EPS have antioxidant activity. Mao et al. completed relatively systematic studies on the structure and activity screening of marine fungal EPS. Several of the EPS are isolated and fullly characterized from Aspergillus versicolor, Aspergillus Terreus, Fusarium oxysporum, and Hansfordia sinuosae (Table 2). Recently, a novel EPS (AUM-1) with immunomodulatory activity was obtained from the marine Aureobasidium melanogenum SCAU-266. The AUM-1 with a molecular weight of 8000 Da had a main monosaccharide of Glc (97.30%), whose structure possessed a potential backbone of α-D-Glcp-(1→2)-α-D-Manp-(1→4)-α-D-Glcp-(1→6)-(-(SO3−)-4-α-D-Glcp-(1→6)-1-β-D-Glcp-1→2)-α-D-Glcp-(1→6)-β-D-Glcp-1→6)-α-D-Glcp-1→4)-α-D-Glcp-6→1)-[α-D-Glcp-4]26→1)-α-D-Glcp [74]. The possible structure of these marine fungal EPS mentioned in Table 2 are shown in Figure 1.
Besides the marine bacteria and fungi, marine microalgae and cyanobacteria are other important resources to produce EPS. Information of some of the EPS obtained from marine microalgae and cyanobacteria in the last decade are shown in Table 3. These EPS usually have a complex monosaccharide composition with uronic acid and sulfate groups, with various biological activities such as antioxidant, antiviral, antifungal, antibacterial, anti-ageing, anticancer, and immunomodulatory activities [89,90]. Recently, Esqueda et al. systematically explored the diversity of 11 microalgae strains belonging to the proteorhodophytina subphylum for EPS production. Regarding the compositions, some of the common features were highlighted, such as the presence of Xyl, Gal, Glc, and GlcA in all of the compositions, but with different amounts depending on the samples. In addition, the existence of sulfate groups in EPS from those microalgae strains were much more different [91]. The EPS from Chlorella sorokiniana had anticoagulant and antioxidant activities. The sulfate content and their binding site, monosaccharide composition, and glycoside bond were involved in its bioactivity [92]. Cyanoflan, a cyanobacterial-sulfated EPS, was characterized in terms of its morphology, structural composition, and rheological and emulsifying properties. The glycosidic linkage analysis revealed that this EPS had a highly branched complex structure with a large number of sugar residues, including Man, Glc, uronic acids, Gal, Rha, Xyl, Fuc, and Ara with a molar ratio of 20:20:18:10:9:9:8:6. The high molecular weight (>1 MDa) and entangled structure was consistent with its high apparent viscosity in aqueous solutions and high emulsifying activity [75]. The EPS from the cyanobacterium Nostoc carneum was a type of polyanionic polysaccharide that contained uronic acid and sulfate groups [93]. Another EPS from Tetraselmis suecica (Kylin) with antioxidant and anticancer activities also had a high amount of uronic acid [94]. The acid groups played important roles in the antioxidant activity of the marine EPS.

4. The Biological Activities of Marine EPS

The structure of the marine microbial EPS is complex and diverse [101], and is linked to various biological activities, such as antibacterial, antioxidant, anti-cancer, antifreeze, anti-inflammatory, enhancement of immune activity and blood pressure, and lipid reduction [102,103,104,105]. In addition, due to the particularity of the marine microbial environment, the EPS produced by marine microbials also have a potential application value in the marine ecological environment. Here, we mainly introduced the antioxidant activity, anticancer activity, anti-infectious activity, and immune-enhancing biological activity of the marine microbial EPS (as shown in Table 1, Table 2 and Table 3 and Figure 2) and their potential application in bioremediation and carbon sequestration.

4.1. Antioxidant Activity

Oxygen is the key substance in the normal life-metabolism of aerobic organisms [106]. In the metabolism of organisms, the living organisms inevitably produce reactive oxygen species (ROS) [107]. High levels of ROS may disrupt the pro-oxidant/antioxidant balance in organisms, leading to oxidative stress [108]; excessive ROS will destroy the normal function of lipids, proteins, and DNA in human cells, thus inducing various diseases [109]. Several pieces of evidence have proved that antioxidants play an important role in protecting humans from cancer, diabetes, cardiovascular disease, and neurodegenerative diseases related to different types of oxidative damage [110,111,112].
The EPS from marine bacteria usually have strong antioxidant activity, which is related to the structural characteristics of EPS, including sulfate content and their binding site, monosaccharide residues, and glycoside bonds [13]. The marine bacteria EPS usually contribute to the formation of biofilms, thus adapting to extreme environments, such as high salinity, low temperatures, and high osmotic pressure [113,114,115]. For example, the AEPS from Rhodella reticulata have a stronger scavenging ability of superoxide anions than that of the standard antioxidant, α -tocopherol [116]. The EPS isolated from the Arctic marine Bacterium Polaribacter sp. SM1127 have a good antioxidant capacity. The antioxidant capacity is significantly higher than that of hyaluronic acid (HA), a common free-radical scavenging adhesive in cosmetics, which indicated that this EPS has good application prospects in the future cosmetics’ antioxidant field [59]. Further, SM1127 could remove the excess ROS produced by wound infection and inflammation, thus accelerating wound healing. Therefore, this EPS is likely to be used to accelerate the healing of frostbite, burns, and other wounds [60]. Wu et al. reported a marine bacterial EPS produced by P. stutzeri 273 named EPS27 with a good clearance rate of hydroxyl radicals, which could reach 70% when the concentration of EPS is 60 μg/mL. Therefore, EPS27 has good antioxidant activity and has potential application prospects in the food and health-care fields [49]. The skin is the largest organ of the human body and skin wound healing is an important clinical problem [117,118,119]. Since synthetic drugs have a high risk of adverse effects, such as allergies and drug resistance, natural products such as EPS are becoming increasingly important and are strongly recommended as alternative medicines for wound healing.
Another source of antioxidants is EPS produced by marine fungi. Wang et al. found a new extracellular polysaccharide (YSS) from the marine fungus Aspergillus Terreus, which was composed of Man and Gal units with a molecular weight of 18.6 kDa [85]. YSS had a strong scavenging ability on DPPH radicals, and the EC50 was 2.8 mg/mL. Chen et al. reported that the marine fungus, Fusarium oxysporum, produced a novel galactofuranose-containing EPS Fw-1, which was mainly composed of Gal, Glc, and Man with a molecular weight of 61.2 kDa [83]. The EC50 of Fw-1 on the scavenging of hydroxyl and superoxide radicals was 1.1 and 2.0 mg/mL, respectively, which was larger than that of the EPS named as AVP isolated from the marine Aspergillus Versicolor LCJ-5-4 (EC50 is 4.0 mg/mL). The antioxidant EPS extracted from marine fungi had a relatively simple monosaccharide composition and a small molecular weight, which was more suitable for studying the relationship between the structure of the marine polysaccharides and antioxidants [80,120].
The epidemiological investigations have proved a strong correlation between the antioxidant utilization and a diminished risk of commonplace chronic diseases, such as cardiovascular disease and cancer. Compared with many reports on the antioxidant activity of marine microbial EPS, there are few reports on the separation, purification, and structure analysis of marine microbial EPS. It is necessary for the in-depth study of their structure–activity relationship.

4.2. Anti-Cancer Activity

Now, new sources of non-toxic natural substances with potential anticancer effects, are being actively investigated [121]. In the past decade, there has been a great deal of interest in the development of anti-cancer polysaccharide drugs. The marine microorganisms have unique metabolic and physiological abilities, which give them the ability to produce various biological compounds [122,123,124], such as EPS. Several marine microbial EPS have been reported to have anticancer activity by the dysfunction of mitochondria, the inhibition of cell proliferation, or the modulation of the immune system [42,58,94,125,126,127,128]. Matsuda et al. studied the marine Pseudomonas polysaccharide B1, and found that it could induce U937 cells’ apoptosis [128]. Chen et al. reported that the Antarctic bacterium Pseudoaltermonas sp. S-5 produced a hetero-exopolysaccharide (named PEP) which could significantly inhibit human leukemia cell K562 growth [58]. Moreover, Ramamoorthy Sathishkumar et al. found that EPS from ascidian symbiotic bacterium Bacillus thuringiensis had good anticancer activity in vitro. This polysaccharide showed potential cytotoxicity against the cancer cell lines A549 and HEP-2 compared with normal Vero cells. The inhibition rate of EPS on both of the cancer cell lines increased in a dose-dependent manner [42]. The AS2-1 produced by Alternaria sp. could also inhibit the growth of Hela, HL-60, and K562 cells in a concentration-dependent manner [84]. The marine bacterial exopolysaccharide EPS11 could effectively inhibit the adhesion, migration, and invasion of hepatocellular carcinoma cells; this underlying target protein and molecular mechanism was first explored through the β 1-integrin signal pathway by targeting type I collagen [126]. Recently, one study showed that the newly isolated marine bacterial EPS could enhance antitumor activity in HepG2 cells by affecting the key apoptotic factors and activating the toll-like receptors (TLR) [129]. Other studies have shown that the chemical modification of EPS, such as acetylation, carboxymethylation, and sulfonation, can also enhance its biological activity [130,131], and then enhance its anticancer activity. Mazza et al. confirmed that the two polysaccharides, EPS-DR and EPS-DRS, could form complexes with scandium, and that these complexes showed a variety of biological activities, especially antiproliferative properties in cancer cells.

4.3. Anti-Infectious Diseases

EPS also play an important role in fighting infectious diseases. A quantity of research evidenced that the immune activity and anti-viral activity of marine microbial EPS have potential value in inhibiting some influenza viruses and bacteria [132]. EPS, as a potent antibacterial agent, can inhibit bacterial growth mainly by inhibiting biofilm formation. Mikhlid H et al. reported that Enterobacter sp. ACD2 EPS from the Tabuk region of Saudi Arabia had a certain inhibitory effect on E. coli and Staphylococcus aureus [48]. Durairajan Rubini et al. reported a marine polysaccharide with good antibacterial activity and strong inhibition against uropathogenic Escherichia coli (UPEC), providing an antibiotic-free method for the treatment of urinary tract infections [133]. Similarly, Wu et al. reported that an exopolysaccharide EPS273 from the culture supernatant of the marine bacterium P. stutzeri 273 inhibited Pseudomonas aeruginosa by anti-biofilm activity [49]. It can be effective not only in animal bacteria, but also in plant bacteria. Marwa Drira et al. found that EPS produced by Porphyridium sordidum had led to the control of fungal growth by the plant, and EPS could act as an inducer to enhance the resistance of A. thaliana to F. oxysporum [24]. In addition, the sulfated EPS from Porphyridium sp. has shown an antiviral effect against the herpes viruses (HSV-1 and HSV-2) [134,135].

4.4. Immunomodulatory Activity

The main function of the immune system is to identify and eliminate pathogens to maintain physiological balance and stability [136]. When the immunity is impaired, it will lead to various adverse immune reactions [137]. Several of the EPS synthesized by marine microorganisms have immunomodulatory activities [45,60,61,74,138,139,140]. For example, an EPS named as EPS2E1 was extracted from marine Halomonas sp. and displayed good immune-enhancing activity, mainly by activating the MAPK and NF-κB pathways [56]. Soumya Chatterjee et al. reported that sphingobactan, a new α-mannan EPS from Arctic Sphingobacterium sp. IITKGP-BTPF3 significantly reduced the NO production of LPS-induced macrophages. These results indicated that sphingobactan had a potential activation effect on the anti-inflammatory effects of macrophages in vitro [57]. On the one hand, evidence has shown that the expression of cytokines, such as interleukin (IL), tumor necrosis factor (IF-α), and interferon, can be induced by marine microbial EPS [141]. Moreover, Adriana et al. reported that EPS-1 could contribute to improve the immune surveillance of PBMC toward viral infection, by triggering a polarization in favor of the Th1 subset. EPS-1 produced by Bacillus Licheniformis could induce the production of cytokines to enhance immune regulation [138]. It mainly promoted the macrophages to secrete the mediators and enzymes that play a vital role in mediating inflammation and tissue repair, such as NO, COX-2, IL-1, IL-6, and TNF-α in the RAW264.7 macrophages [142,143,144,145]. YCP, a natural EPS from the mycelium of the marine filamentous fungus Phoma herbarum YS4108, could bind to TLR-2 and TLR-4 and had great antitumor potential via exhibiting a specific immunomodulatory capacity, mediated by T cells and dendritic cells (DCs) [146]. Recently, a novel EPS (AUM-1) was obtained from marine Aureobasidium melanogenum SCAU-266, with a potential effect on the ferroptosis-related immunomodulatory property in RAW264.7 cells. The mechanism studies have shown that it can adjust the expression of GPX4, regulate glutathione (oxidative), and directly cause lipid peroxidation, due to the higher ROS level by the glutamate metabolism and TCA cycle (Figure 3) [74].

5. Environmental Remediation

5.1. Biological Restoration

With the progress of industrialization, wastewater treatment is particularly important. Traditional wastewater treatment methods include mixing, precipitation, filtration, or chlorine disinfection, but these methods are expensive and prone to secondary pollution [139,140,147]. The biological treatments, by contrast, are environmentally friendly. One of the important biological systems’ methods is the use of marine microbial EPS flocculation [22]. These EPS have a significant impact on the physical and chemical properties of microbial aggregates [18], which is conducive to flocculation and the precipitation of impurities in sewage. It has also been reported that the EPS interact with cells to form a large network that protects them from dehydration and toxins [148]. In addition, the marine microbial EPS are often polyanionic with uronic acids, sulfated units, and phosphate groups. These chemical groups provide EPS with a negative charge allowing them to act as ligands toward dissolved cations, as well as trace and toxic metals [1]. For example, Zhou et al. reported that Bsi 20310, produced by Pseudoalteromonas SP in the ocean, could effectively enhance the rate of flocculation formation in the ferric chloride coagulation RX-3B simulation of fuel wastewater [149]. Similarly, Yang et al. also reported a positive correlation between LB-EPS and the sludge flocculation rate [150]. Likewise, microbial EPS are also valuable in dealing with other environmental problems. Flocculation is a common method used to remove heavy metals and other pollutants from sewage. Likewise, Paritosh Parmar et al. reported on the EPS produced by PBR1 and PBL1, collected from a fish, Indian mackerel, and an Indian squid. These two kinds of bacteria, PBR1 and PBL1, are luminescent bacteria, subordinate to vibrio genera. Although most of the vibrio strains are pathogenic, the results of a β hemolysin test for PBR1 and PBL1 showed that these two strains are not pathogenic, and that the EPS produced by them can be used to repair heavy metal pollution in the water environment, and that the luminescence characteristics of these two strains can be used to develop luminescent biosensors [151]. Given the important role of EPS in wastewater treatment, Salama et al. proposed five better ways to understand EPS: (1) Development of EPS extraction methods; (2) Establishment of EPS in situ analytical methods; (3) Identifying the sub-fractions of EPS; (4) Elucidation of the key roles of EPS; (5) Identification of the key factors influencing the production of EPS [18].

5.2. Oil pollution Remediation

There have been related applications of marine EPS in dealing with the leakage of offshore crude oil [152]. Noriyuki et al. found that the EPS produced by Monascus could be used to deal with the offshore oil spill and accelerate the degradation of crude oil [153]. For example, Ant-3b could emulsify n-hexadecane at low temperatures and had great potential in solving crude oil pollution in a low-temperature environment [154]. At the same time, the research of Ilori, Amobi, and Odocha showed that biosurfactants are superior to synthetic surfactants [155].

5.3. Carbon Sequestration

Over the past decade, the oceans have absorbed a quarter of the Earth’s greenhouse gas emissions through the carbon (C) cycle, a naturally occurring process. All of the aspects of the ocean C cycle are now being incorporated into climate change mitigation and adaptation plans [156]. According to the Global Biodiversity Assessment by the United Nations Environment Program, there are 178,000 marine species which belong to 34 phyla [157]. Thus, the ocean’s biodiversity represents 50% of the whole globe’s biodiversity [158,159]. Marine primary productivity is handled by heterotrophic microorganisms; the substrate specificity of extracellular enzymes, the rate at which they function in seawater and sediments, and the factors that control their production, distribution, and active life span, are central to the carbon cycle in marine systems [160].
The EPS produced by marine microorganisms are significant for the carbon cycle and have also been reported in the deep ocean. Joseph et al. reported that the EPS produced by the marine psychrophilic bacterium Colwellia psychrerythraea strain 34H could affect the carbon cycle and nutrient transfer in the deep sea [161]. In the Antarctic environment, the EPS promote the accumulation of soil organic matter at the landscape level in depauperate Antarctic soil [79,162]. Antarctic green algae sequester 479,000 tons of carbon each season [163]. The EPS of microorganisms in the Antarctic environment, which exist in the form of cell aggregates, biofilms, microbial mats, biocrusts, and so on, influence the global carbon cycle [164,165].

6. Conclusions and Future Perspectives

The investigation of marine environments, their microbial diversity, and unique polysaccharides are now becoming one of the focuses of scientific research. In the past decade, scientific research has focused on the isolation and culture of marine microorganisms and their unique biological activities. The EPS from marine microorganisms have considerable potential in bioremediation, wastewater treatment, heavy metal treatment, and marine oil pollution. Due to its unique and complex macromolecular structure, the marine microbial EPS show great application prospects in the pharmaceutical and biomedical fields, such as antifreeze, anti-oxidation, anti-cancer, anti-inflammation, antibacterial, and so on. Although the EPS from marine microorganisms have good applications in many fields, there are relatively few studies on the marine microbial EPS, especially in the study of EPS produced by the extreme marine environment, partly due to the difficulty of isolation and culture conditions. In brief, new and updated technical strategies are needed to constantly achieve the separation, purification, and structural analysis of novel marine microbial EPS. Furthermore, the biological activities and structure–activity relationship of these EPS need further exploration.

Author Contributions

Writing-original draft preparation, M.Q.; check and editing, C.Z.; writing-review and editing, W.W., G.Y. and P.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China 81991522,82173731), Qingdao Pilot National Laboratory for Marine Science and Technology of Shandong Province Special Found (2022QNLM030003-4), and the Taishan Scholar Climbing Project (TSPD20210304).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. López-Ortega, M.A.; Chavarría-Hernández, N.; del Rocio Lopez-Cuellar, M.; Rodríguez-Hernández, A.I. A review of extracellular polysaccharides from extreme niches: An emerging natural source for the biotechnology. From the adverse to diverse! Int. J. Biol. Macromol. 2021, 177, 559–577. [Google Scholar] [CrossRef] [PubMed]
  2. Kuzma, M.; Clack, B.; Edwards, J.; Tylingo, R.; Samaszko, J.; Madaj, J. Structure and properties of the exopolysaccharides produced by Pseudomonas mutabilis T6 and P. mutabilis ATCC 31014. Carbohydr. Res. 2012, 348, 84–90. [Google Scholar] [CrossRef]
  3. Chuan-Lu, W.; Tzu-Huang, H.; Tzu-Wen, L.; Chun-Yong, F.; San-Lang, W. Production and characterization of exopolysaccharides and antioxidant from Paenibacillus sp. TKU023. New Biotechnol. 2011, 28, 559–565. [Google Scholar]
  4. Carvalho, D.N.; Reis, R.L.; Silva, T.H. Marine origin materials on biomaterials and advanced therapies to cartilage tissue engineering and regenerative medicine. Biomater. Sci. 2021, 9, 6718–6736. [Google Scholar] [CrossRef] [PubMed]
  5. Decho, A.W.; Gutierrez, T. Microbial Extracellular Polymeric Substances (EPSs) in Ocean Systems. Front. Microbiol. 2017, 8, 922. [Google Scholar] [CrossRef]
  6. Ravella, S.R.; Quiñones, T.S.; Retter, A.; Heiermann, M.; Amon, T.; Hobbs, P.J. Extracellular polysaccharide (EPS) production by a novel strain of yeast-like fungus Aureobasidium pullulans. Carbohydr. Polym. 2010, 82, 728–732. [Google Scholar] [CrossRef]
  7. Yang, L.; Wei, Z.; Li, S.; Xiao, R.; Xu, Q.; Ran, Y.; Ding, W. Plant secondary metabolite, daphnetin reduces extracellular polysaccharides production and virulence factors of Ralstonia solanacearum. Pestic. Biochem. Phys. 2021, 179, 104948. [Google Scholar] [CrossRef] [PubMed]
  8. Kumar, A.S.; Mody, K.; Jha, B. Bacterial exopolysaccharides—A perception. J. Basic Microbiol. 2007, 47, 103–117. [Google Scholar] [CrossRef]
  9. Nichols, C.A.M.; Guezennec, J.; Bowman, J.P. Bacterial exopolysaccharides from extreme marine environments with special consideration of the Southern Ocean, sea ice, and deep-sea hydrothermal vents: A review. Mar. Biotechnol. 2005, 7, 253–271. [Google Scholar] [CrossRef]
  10. Becker, A.; Katzen, F.; Pühler, A.; Ielpi, L. Xanthan gum biosynthesis and application: A biochemical /genetic perspective. Appl. Microbiol. Biotechnol. 1998, 50, 145–152. [Google Scholar] [CrossRef] [PubMed]
  11. Liu, L.; Liu, Y.; Li, J.; Du, G.; Chen, J. Microbial production of hyaluronic acid: Current state, challenges, and perspectives. Microb. Cell Factories 2011, 10, 99. [Google Scholar] [CrossRef] [PubMed]
  12. Poli, A.; Anzelmo, G.; Nicolaus, B. Bacterial Exopolysaccharides from Extreme Marine Habitats: Production, Characterization and Biological Activities. Mar. Drugs 2010, 8, 1779–1802. [Google Scholar] [CrossRef] [PubMed]
  13. Andrew, M.; Jayaraman, G. Structural features of microbial exopolysaccharides in relation to their antioxidant activity. Carbohydr. Res. 2020, 487. [Google Scholar] [CrossRef]
  14. Barcelos, M.C.S.; Vespermann, K.A.C.; Pelissari, F.M.; Molina, G. Current status of biotechnological production and applications of microbial exopolysaccharides. Crit. Rev. Food Sci. Nutr. 2020, 60, 1475–1495. [Google Scholar] [CrossRef]
  15. Guezennec, J. Deep-sea hydrothermal vents: A new source of innovative bacterial exopolysaccharides of biotechnological interest. J. Ind. Microbiol. Biot. 2002, 29, 204–208. [Google Scholar] [CrossRef] [PubMed]
  16. Kornmann, H.; Duboc, P.; Marison, I.; von Stockar, U. Influence of nutritional factors on the nature, yield, and composition of exopolysaccharides produced by Gluconacetobacter xylinus I-2281. Appl. Environ. Microb. 2003, 69, 6091–6098. [Google Scholar] [CrossRef] [PubMed]
  17. Bar-Zeev, E.; Rahav, E. Microbial metabolism of transparent exopolymer particles during the summer months along a eutrophic estuary system. Front. Microbiol. 2015, 6, 403. [Google Scholar] [CrossRef]
  18. Salama, Y.; Chennaoui, M.; Sylla, A.; Mountadar, M.; Rihani, M.; Assobhei, O. Characterization, structure, and function of extracellular polymeric substances (EPS) of microbial biofilm in biological wastewater treatment systems: A review. Desalin. Water Treat. 2016, 57, 16220–16237. [Google Scholar] [CrossRef]
  19. Nicolaus, B.; Kambourova, M.; Oner, E.T. Exopolysaccharides from extremophiles: From fundamentals to biotechnology. Environ Technol 2010, 31, 1145–1158. [Google Scholar] [CrossRef]
  20. Manivasagan, P.; Kim, S.K. Extracellular Polysaccharides Produced by Marine Bacteria. In Marine Medicinal Foods Implications and Applications, Macro and Microalgae; Elsevier: Amsterdam, The Netherlands, 2014; Volume 72, pp. 79–94. [Google Scholar]
  21. Casillo, A.; Lanzetta, R.; Parrilli, M.; Corsaro, M.M. Exopolysaccharides from Marine and Marine Extremophilic Bacteria: Structures, Properties, Ecological Roles and Applications. Mar. Drugs. 2018, 16, 69. [Google Scholar] [CrossRef]
  22. Banerjee, A.; Sarkar, S.; Govil, T.; González-Faune, P.; Cabrera-Barjas, G.; Bandopadhyay, R.; Salem, D.R.; Sani, R.K. Extremophilic Exopolysaccharides: Biotechnologies and Wastewater Remediation. Front. Microbiol. 2021, 12, 721365. [Google Scholar] [CrossRef] [PubMed]
  23. Acuna, N.; Ortega-Morales, B.O.; Valadez-Gonzalez, A. Biofilm colonization dynamics and its influence on the corrosion resistance of austenitic UNSS31603 stainless steel exposed to Gulf of Mexico seawater. Mar. Biotechnol. 2006, 8, 62–70. [Google Scholar] [CrossRef] [PubMed]
  24. Drira, M.; Elleuch, J.; Ben Hlima, H.; Hentati, F.; Gardarin, C.; Rihouey, C.; Le Cerf, D.; Michaud, P.; Abdelkafi, S.; Fendri, I. Optimization of Exopolysaccharides Production by Porphyridium sordidum and Their Potential to In-duce Defense Responses in Arabidopsis thaliana against Fusarium oxysporum. Biomolecules 2021, 11, 282. [Google Scholar] [CrossRef]
  25. Schmid, J. Recent insights in microbial exopolysaccharide biosynthesis and engineering strategies. Curr. Opin. Biotechnol. 2018, 53, 130–136. [Google Scholar] [CrossRef] [PubMed]
  26. Casillo, A.; Parrilli, E.; Sannino, F.; Mitchell, D.E.; Gibson, M.I.; Marino, G.; Lanzetta, R.; Parrilli, M.; Cosconati, S.; Novellino, E.; et al. Structure activity relationship of the exopolysaccharide from a psychrophilic bacterium: A strategy for cryoprotection. Carbohydr. Polym. 2017, 156, 364–371. [Google Scholar] [CrossRef] [PubMed]
  27. Radchenkova, N.; Vassilev, S.; Martinov, M.; Kuncheva, M.; Panchev, I.; Vlaev, S.; Kambourova, M. Optimiza-tion of the aeration and agitation speed of Aeribacillus palidus 418 exopolysaccharide production and the emulsifying properties of the product. Process Biochem. 2014, 49, 576–582. [Google Scholar] [CrossRef]
  28. Caccamo, M.T.; Gugliandolo, C.; Zammuto, V.; Magazu, S. Thermal properties of an exopolysaccharide produced by a marine thermotolerant Bacillus licheniformis by ATR-FTIR spectroscopy. Int. J. Biol. Macromol. 2020, 145, 77–83. [Google Scholar] [CrossRef]
  29. Caccamo, M.T.; Zammuto, V.; Gugliandolo, C.; Madeleine-Perdrillat, C.; Spano, A.; Magazu, S. Thermal restraint of a bacterial exopolysaccharide of shallow vent origin. Int. J. Biol. Macromol. 2018, 114, 649–655. [Google Scholar] [CrossRef]
  30. Gan, L.; Li, X.; Wang, H.; Peng, B.; Tian, Y. Structural characterization and functional evaluation of a novel exopolysaccharide from the moderate halophile Gracilibacillus sp. SCU50. Int. J. Biol. Macromol. 2019, 154, 1140–1148. [Google Scholar] [CrossRef]
  31. Radchenkova, N.; Vassilev, S.; Panchev, I.; Anzelmo, G.; Tomova, I.; Nicolaus, B.; Kuncheva, M.; Petrov, K.; Kambourova, M. Production and Properties of Two Novel Exopolysaccharides Synthesized by a Thermophilic Bacterium Aeribacillus pallidus 418. Appl. Biochem. Biotech. 2013, 171, 31–43. [Google Scholar] [CrossRef]
  32. Le Costaouëc, T.; Cérantola, S.; Ropartz, D.; Ratiskol, J.; Sinquin, C.; Colliec-Jouault, S.; Boisset, C. Structural data on a bacterial exopolysaccharide produced by a deep-sea Alteromonas macleodii strain. Carbohydr. Polym. 2012, 90, 49–59. [Google Scholar] [CrossRef] [PubMed]
  33. Erginer, M.; Akcay, A.; Coskunkan, B.; Morova, T.; Rende, D.; Bucak, S.; Baysal, N.; Ozisik, R.; Eroglu, M.S.; Agirbasli, M.; et al. Sulfated levan from Halomonas smyrnensis as a bioactive, heparin-mimetic glycan for cardiac tissue engineering applications. Carbohydr. Polym. 2016, 149, 289–296. [Google Scholar] [CrossRef] [PubMed]
  34. Sahana, T.G.; Rekha, P.D. A novel exopolysaccharide from marine bacterium Pantoea sp. YU16-S3 accelerates cutaneous wound healing through Wnt/beta-catenin pathway. Carbohydr. Polym. 2020, 238, 116191. [Google Scholar] [CrossRef]
  35. Field, C.B.; Behrenfeld, M.J.; Randerson, J.T.; Falkowski, P. Primary Production of the Biosphere: Integrating Terrestrial and Oceanic Components. Science 1998, 281, 237–240. [Google Scholar] [CrossRef]
  36. Rougeaux, H.; Guezennec, J.; Carlson, R.W.; Kervarec, N.; Pichon, R.; Talaga, P. Structural determination of the exopolysaccharide of Pseudoalteromonas strain HYD 721 isolated from a deep-sea hydrothermal vent. Carbohydr. Res. 1999, 315, 273–285. [Google Scholar] [CrossRef]
  37. Gugliandolo, C.; Maugeri, T.L. Temporal variations in heterotrophic mesophilic bacteria from a marine shallow hydrothermal vent off the Island of Vulcano (Eolian Islands, Italy). Microb. Ecol. 1998, 36, 13–22. [Google Scholar] [CrossRef]
  38. Jouault, S.C.; Chevolot, L.; Helley, D.; Ratiskol, J.; Bros, A.; Sinquin, C.; Roger, O.; Fischer, A.M. Characterization, chemical modifications and in vitro anticoagulant properties of an exopolysaccharide produced by Alteromonas infernus. BBA-Gen Subjects 2001, 1528, 141–151. [Google Scholar] [CrossRef]
  39. Zanchetta, P.; Lagarde, N.; Guezennec, J. A new bone-healing material: A hyaluronic acid like bacterial exopolysaccharide. Calcif. Tissue Int. 2003, 72, 74–79. [Google Scholar] [CrossRef]
  40. Ayyash, M.; Abu-Jdayil, B.; Olaimat, A.; Esposito, G.; Itsaranuwat, P.; Osaili, T.; Obaid, R.; Kizhakkayil, J.; Liu, S.Q. Physicochemical, bioactive and rheological properties of an exopolysaccharide produced by a probiotic Pediococcus pentosaceus M41. Carbohydr. Polym. 2020, 229, 115462. [Google Scholar] [CrossRef]
  41. Krishnamurthy, M.; Uthaya, C.J.; Thangavel, M.; Annadurai, V.; Rajendran, R.; Gurusamy, A. Optimization, compositional analysis, and characterization of exopolysaccharides produced by multimetal resistant Bacillus cereus KMS3-1. Carbohydr. Polym. 2020, 227, 115369. [Google Scholar] [CrossRef]
  42. Ramamoorthy, S.; Gnanakan, A.; Lakshmana, S.S.; Meivelu, M.; Jeganathan, A. Structural characterization and anti-cancer activity of extracellular polysaccharides from ascidian symbiotic bacterium Bacillus thuringiensis. Carbohydr. Polym. 2018, 190, 113–120. [Google Scholar] [CrossRef] [PubMed]
  43. Kavita, K.; Singh, V.K.; Mishra, A.; Jha, B. Characterization and anti-biofilm activity of extracellular polymeric substances from Oceanobacillus iheyensis. Carbohydr. Polym. 2014, 101, 29–35. [Google Scholar] [CrossRef] [PubMed]
  44. Roca, C.; Lehmann, M.; Torres, C.A.; Baptista, S.; Gaudêncio, S.P.; Freitas, F.; Reis, M.A. Exopolysaccharide production by a marine Pseudoalteromonas sp. strain isolated from Madeira Archipelago ocean sediments. New Biotechnol. 2016, 33, 460–466. [Google Scholar] [CrossRef] [PubMed]
  45. Wei, M.; Geng, L.; Wang, Q.; Yue, Y.; Wang, J.; Wu, N.; Wang, X.; Sun, C.; Zhang, Q. Purification, characterization and immunostimulatory activity of a novel exopolysaccharide from Bacillus sp. H5. Int. J. Biol. Macromol. 2021, 189, 649–656. [Google Scholar] [CrossRef]
  46. Zhang, Z.; Cai, R.; Zhang, W.; Fu, Y.; Jiao, N. A Novel Exopolysaccharide with Metal Adsorption Capacity Produced by a Marine Bacterium Alteromonas sp. JL2810. Mar. Drugs 2017, 15, 175. [Google Scholar] [CrossRef]
  47. Dhanya, B.E.; Prabhu, A.; Rekha, P.D. Extraction and characterization of an exopolysaccharide from a marine bacterium. Int. Microbiol. 2022, 25, 285–295. [Google Scholar] [CrossRef] [PubMed]
  48. Almutairi, M.H.; Helal, M.M. Biological and microbiological activities of isolated Enterobacter sp. ACD2 exopolysaccharides from Tabuk region of Saudi Arabia. J. King Saud Univ. Sci. 2020, 33, 101328. [Google Scholar] [CrossRef]
  49. Wu, S.; Liu, G.; Jin, W.; Xiu, P.; Sun, C. Antibiofilm and Anti-Infection of a Marine Bacterial Exopolysaccharide Against Pseudomonas aeruginosa. Front. Microbiol. 2016, 7, 102. [Google Scholar] [CrossRef] [PubMed]
  50. Sran, K.S.; Bisht, B.; Mayilraj, S.; Choudhury, A.R. Structural characterization and antioxidant potential of a novel anionic exopolysaccharide produced by marine Microbacterium aurantiacum FSW-25. Int. J. Biol. Macromol. 2019, 131, 343–352. [Google Scholar] [CrossRef] [PubMed]
  51. Selim, S.; Almuhayawi, M.S.; Alharbi, M.T.; Nagshabandi, M.K.; Alanazi, A.; Warrad, M.; Hagagy, N.; Ghareeb, A.; Ali, A.S. In Vitro Assessment of Antistaphylococci, Antitumor, Immunological and Structural Characterization of Acidic Bioactive Exopolysaccharides from Marine Bacillus cereus Isolated from Saudi Arabia. Metabolites 2022, 12, 132. [Google Scholar] [CrossRef] [PubMed]
  52. Jiang, P.; Li, J.B.; Han, F.; Duan, G.F.; Lu, X.Z.; Gu, Y.C.; Yu, W.G. Antibiofilm Activity of an Exopolysaccharide from Marine Bacterium Vibrio sp QY101. PLoS ONE 2011, 6, e18514. [Google Scholar] [CrossRef]
  53. Arun, J.; Selvakumar, S.; Sathishkumar, R.; Moovendhan, M.; Ananthan, G.; Maruthiah, T.; Palavesam, A. In vitro antioxidant activities of an exopolysaccharide from a salt pan bacterium Halolactibacillus miurensis. Carbohydr. Polym. 2017, 155, 400–406. [Google Scholar] [CrossRef] [PubMed]
  54. Gan, L.; Li, X.; Zhang, H.; Zhang, R.; Wang, H.; Xu, Z.; Peng, B.; Tian, Y. Preparation, characterization and functional properties of a novel exopolysaccharide produced by the halophilic strain Halomonas saliphila LCB169T. Int. J. Biol. Macromol. 2020, 156, 372–380. [Google Scholar] [CrossRef] [PubMed]
  55. Qin, G.; Zhu, L.; Chen, X.; Wang, P.G.; Zhang, Y. Structural characterization and ecological roles of a novel exopolysaccharide from the deep-sea psychrotolerant bacterium Pseudoalteromonas sp. SM9913. Microbiology 2007, 153, 1566–1572. [Google Scholar] [CrossRef] [PubMed]
  56. Carrión, O.; Delgado, L.; Mercade, E. New emulsifying and cryoprotective exopolysaccharide from Antarctic Pseudomonas sp. ID1. Carbohydr. Polym. 2015, 117, 1028–1034. [Google Scholar] [CrossRef] [PubMed]
  57. Ali, P.; Shah, A.A.; Hasan, F.; Hertkorn, N.; Gonsior, M.; Sajjad, W.; Chen, F. A Glacier Bacterium Produces High Yield of Cryoprotective Exopolysaccharide. Front. Microbiol. 2020, 10, 3096. [Google Scholar] [CrossRef] [PubMed]
  58. Caruso, C.; Rizzo, C.; Mangano, S.; Poli, A.; Di Donato, P.; Nicolaus, B.; Finore, I.; Di Marco, G.; Michaud, L.; Giudice, A.L. Isolation, characterization and optimization of EPSs produced by a cold-adapted Marinobacter isolate from Antarctic seawater. Antarct. Sci. 2019, 31, 69–79. [Google Scholar] [CrossRef]
  59. Liu, S.-B.; Chen, X.-L.; He, H.-L.; Zhang, X.-Y.; Xie, B.-B.; Yu, Y.; Chen, B.; Zhou, B.-C.; Zhang, Y.Z. Structure and Ecological Roles of a Novel Exopolysaccharide from the Arctic Sea Ice Bacterium Pseudoalteromonas sp. Strain SM20310. Appl. Environ. Microbiol. 2013, 79, 224–230. [Google Scholar] [CrossRef]
  60. Wang, Q.; Wei, M.; Zhang, J.; Yue, Y.; Wu, N.; Geng, L.; Sun, C.; Zhang, Q.; Wang, J. Structural characteristics and immune-enhancing activity of an extracellular polysaccharide produced by marine Halomonas sp. 2E1. Int. J. Biol. Macromol. 2021, 183, 1660–1668. [Google Scholar] [CrossRef]
  61. Chatterjee, S.; Mukhopadhyay, S.K.; Gauri, S.S.; Dey, S. Sphingobactan, a new alpha-mannan exopolysaccharide from Arctic Sphingobacterium sp. IITKGP-BTPF3 capable of biological response modification. Int. Immunopharmacol. 2018, 60, 84–95. [Google Scholar] [CrossRef]
  62. Chen, G.; Qian, W.; Li, J.; Xu, Y.; Chen, K. Exopolysaccharide of Antarctic bacterium Pseudoaltermonas sp. S-5 induces apoptosis in K562 cells. Carbohydr. Polym. 2015, 121, 107–114. [Google Scholar] [CrossRef] [PubMed]
  63. Sun, M.L.; Zhao, F.; Shi, M.; Zhang, X.Y.; Zhou, B.C.; Zhang, Y.Z.; Chen, X.L. Characterization and Biotechnological Potential Analysis of a New Exopolysaccharide from the Arctic Marine Bacterium Polaribacter sp. SM1127. Sci. Rep. 2015, 5, 18435. [Google Scholar] [CrossRef]
  64. Sun, M.L.; Zhao, F.; Chen, X.L.; Zhang, X.Y.; Zhang, Y.Z.; Song, X.Y.; Sun, C.Y.; Yang, J. Promotion of Wound Healing and Prevention of Frostbite Injury in Rat Skin by Exopolysaccharide from the Arctic Marine Bacterium Polaribacter sp. SM1127. Mar. Drugs. 2020, 18, 48. [Google Scholar] [CrossRef] [PubMed]
  65. Sran, K.S.; Sundharam, S.S.; Krishnamurthi, S.; Choudhury, A.R. Production, characterization and bioemulsifying activity of a novel thermostable exopolysaccharide produced by a marine strain of Rhodobacter johrii CDR-SL 7Cii. Int. J. Biol. Macromol. 2019, 127, 240–249. [Google Scholar] [CrossRef]
  66. Zykwinska, A.; Berre, L.T.; Sinquin, C.; Ropartz, D.; Rogniaux, H.; Colliec-Jouault, S.; Delbarre-Ladrat, C. Enzymatic depolymerization of the GY785 exopolysaccharide produced by the deep-sea hydrothermal bacterium Alteromonas infernus: Structural study and enzyme activity assessment. Carbohydr. Polym. 2018, 188, 101–107. [Google Scholar] [CrossRef] [PubMed]
  67. Roger, O.; Kervarec, N.; Ratiskol, J.; Colliec-Jouault, S.; Chevolot, L. Structural studies of the main exopolysaccharide produced by the deep-sea bacterium Alteromonas infernus. Carbohydr. Res. 2004, 339, 2371–2380. [Google Scholar] [CrossRef]
  68. Renard, D. Advances in Physicochemical Properties of Biopolymers; Bentham Science Publishers: Sharjah, United Arab Emirates, 2017. [Google Scholar]
  69. Zhao, S.; Cao, F.; Zhang, H.; Zhang, L.; Zhang, F.; Liang, X. Structural Characterization and Biosorption of Exopolysaccharides from Anoxybacillus sp. R4-33 Isolated from Radioactive Radon Hot Spring. Appl. Biochem. Biotechnol. 2014, 172, 2732–2746. [Google Scholar] [CrossRef] [PubMed]
  70. Martin-Pastor, M.; Ferreira, A.S.; Moppert, X.; Nunes, C.; Coimbra, M.A.; Reis, R.L.; Guezennec, J.; Novoa Carballal, R. Structure, rheology, and copper complexation of a hyaluronan-like exopolysaccharide from Vibrio. Carbohydr. Polym. 2019, 222, 114999. [Google Scholar] [CrossRef] [PubMed]
  71. Gaborieau, M.; Castignolles, P. Size-exclusion chromatography (SEC) of branched polymers and polysaccharides. Anal. Bioanal. Chem. 2011, 399, 1413–1423. [Google Scholar] [CrossRef] [PubMed]
  72. Hu, X.; Pang, X.; Wang, P.G.; Chen, M. Isolation and characterization of an antioxidant exopolysaccharide produced by Bacillus sp. S-1 from Sichuan Pickles. Carbohydr. Polym. 2018, 204, 9–16. [Google Scholar] [CrossRef]
  73. Hong, T.; Yin, J.-Y.; Nie, S.-P.; Xie, M.-Y. Applications of infrared spectroscopy in polysaccharide structural analysis: Progress, challenge and perspective. Food Chem. X 2021, 12, 100168. [Google Scholar] [CrossRef] [PubMed]
  74. Lin, Y.; Yang, J.; Luo, L.; Zhang, X.; Deng, S.; Chen, X.; Li, Y.; Bekhit, A.E.A.; Xu, B.; Huang, R. Ferroptosis Related Immunomodulatory Effect of a Novel Extracellular Polysaccharides from Marine Fungus Aureobasidium melanogenum. Mar. Drugs. 2022, 20, 332. [Google Scholar] [CrossRef] [PubMed]
  75. Mota, R.; Vidal, R.; Pandeirada, C.; Flores, C.; Adessi, A.; De Philippis, R.; Nunes, C.; Coimbra, M.A.; Tamagnini, P. Cyanoflan: A cyanobacterial sulfated carbohydrate polymer with emulsifying properties. Carbohydr. Polym. 2019, 229, 115525. [Google Scholar] [CrossRef] [PubMed]
  76. Ba-akdah, M.A.; Satheesh, S. Characterization and antifouling activity analysis of extracellular polymeric substances produced by an epibiotic bacterial strain Kocuria flava associated with the green macroalga Ulva lactuca. Acta Oceanol. Sin. 2021, 40, 107–115. [Google Scholar] [CrossRef]
  77. Carillo, S.; Casillo, A.; Pieretti, G.; Parrilli, E.; Sannino, F.; Bayer-Giraldi, M.; Cosconati, S.; Novellino, E.; Ewert, M.; Deming, J.W.; et al. A Unique Capsular Polysaccharide Structure from the Psychrophilic Marine Bacterium Colwellia psychrerythraea 34H That Mimics Antifreeze (Glyco)proteins. J. Am. Chem. Soc. 2015, 137, 179–189. [Google Scholar] [CrossRef]
  78. Fasman, G.D. Circular dichroism and the conformational analysis of biomolecules; Springer: Berlin, Germany, 2013. [Google Scholar]
  79. Zayed, A.; Mansour, M.K.; Sedeek, M.S.; Habib, M.H.; Ulber, R.; Farag, M.A. Rediscovering bacterial exopolysaccharides of terrestrial and marine origins: Novel insights on their distribution, biosynthesis, biotechnological production, and future perspectives. Crit. Rev. Biotechnol. 2022, 42, 597–617. [Google Scholar] [CrossRef] [PubMed]
  80. Hamidi, M.; Kozani, P.S.; Kozani, P.S.; Pierre, G.; Michaud, P.; Delattre, C. Marine Bacteria versus Microalgae: Who Is the Best for Biotechnological Production of Bioactive Compounds with Antioxidant Properties and Other Biological Applications? Mar. Drugs. 2020, 18, 28. [Google Scholar] [CrossRef] [PubMed]
  81. Nagaraj, V.; Skillman, L.; Li, D.; Ho, G. Review—Bacteria and their extracellular polymeric substances causing biofouling on seawater reverse osmosis desalination membranes. J. Environ. Manag. 2018, 223, 586–599. [Google Scholar] [CrossRef] [PubMed]
  82. Chunyan, W.; Wenjun, M.; Zhengqian, C.; Weiming, Z.; Yanli, C.; Chunqi, Z.; Na, L.; Mengxia, Y.; Xue, L.; Tiantian, G. Purification, structural characterization and antioxidant property of an extracellular polysaccharide from Aspergillus terreus. Process Biochem. 2013, 48, 1395–1401. [Google Scholar]
  83. Chen, Y.-L.; Mao, W.-J.; Tao, H.-W.; Zhu, W.-M.; Yan, M.-X.; Liu, X.; Guo, T.-T.; Guo, T. Preparation and Characterization of a Novel Extracellular Polysaccharide with Antioxidant Activity, from the Mangrove-Associated Fungus Fusarium oxysporum. Mar. Biotechnol. 2015, 17, 219–228. [Google Scholar] [CrossRef] [PubMed]
  84. Chen, Y.; Mao, W.-J.; Yan, M.-X.; Liu, X.; Wang, S.-Y.; Xia, Z.; Xiao, B.; Cao, S.-J.; Yang, B.-Q.; Li, J. Purification, Chemical Characterization, and Bioactivity of an Extracellular Polysaccharide Produced by the Marine Sponge Endogenous Fungus Alternaria sp. SP-32. Mar. Biotechnol. 2016, 18, 301–313. [Google Scholar] [CrossRef] [PubMed]
  85. Chen, Y.; Mao, W.; Gao, Y.; Teng, X.; Zhu, W.; Chen, Y.; Zhao, C.; Li, N.; Wang, C.; Yan, M.; et al. Structural elucidation of an extracellular polysaccharide produced by the marine fungus Aspergillus versicolor. Carbohydr. Polym. 2013, 93, 478–483. [Google Scholar] [CrossRef] [PubMed]
  86. Chen, Y.; Mao, W.; Yang, Y.; Teng, X.; Zhu, W.; Qi, X.; Chen, Y.; Zhao, C.; Hou, Y.; Wang, C.; et al. Structure and antioxidant activity of an extracellular polysaccharide from coral-associated fungus, Aspergillus versicolor LCJ-5-4. Carbohydr. Polym. 2012, 87, 218–226. [Google Scholar] [CrossRef] [PubMed]
  87. Yan, M.; Mao, W.; Chen, C.; Kong, X.; Gu, Q.; Li, N.; Liu, X.; Wang, B.; Wang, S.; Xiao, B. Structural elucidation of the exopolysaccharide produced by the mangrove fungus Penicillium solitum. Carbohydr. Polym. 2014, 111, 485–491. [Google Scholar] [CrossRef]
  88. Li, H.; Cao, K.; Cong, P.; Liu, Y.; Cui, H.; Xue, C. Structure characterization and antitumor activity of the extracellular polysaccharide from the marine fungus Hansfordia sinuosae. Carbohydr. Polym. 2018, 190, 87–94. [Google Scholar] [CrossRef]
  89. Raposo, M.F.D.; de Morais, R.M.S.C.; de Morais, A.M.M.B. Bioactivity and Applications of Sulphated Polysaccharides from Marine Microalgae. Mar. Drugs. 2013, 11, 233–252. [Google Scholar] [CrossRef]
  90. Laroche, C. Exopolysaccharides from Microalgae and Cyanobacteria: Diversity of Strains, Production Strategies, and Applications. Mar. Drugs 2022, 20, 336. [Google Scholar] [CrossRef]
  91. Esqueda, A.B.; Gardarin, C.; Laroche, C. Exploring the Diversity of Red Microalgae for Exopolysaccharide Production. Mar. Drugs 2022, 20, 246. [Google Scholar] [CrossRef]
  92. Mousavian, Z.; Safavi, M.; Azizmohseni, F.; Hadizadeh, M.; Mirdamadi, S. Characterization, antioxidant and anticoagulant properties of exopolysaccharide from marine microalgae. AMB Express 2022, 12, 1–16. [Google Scholar] [CrossRef]
  93. Hussein, M.H.; Abou-ElWaf, G.S.; Shaaban-De, S.A.; Hassan, N.I. Characterization and Antioxidant Activity of Exopolysaccharide Secreted by Nostoc carneum. Int. J. Pharmacol. 2015, 11, 432–439. [Google Scholar] [CrossRef]
  94. Parra-Riofrío, G.; García-Márquez, J.; Casas-Arrojo, V.; Uribe-Tapia, E.; Abdala-Díaz, R. Antioxidant and Cytotoxic Effects on Tumor Cells of Exopolysaccharides from Tetraselmis suecica (Kylin) Butcher Grown Under Autotrophic and Heterotrophic Conditions. Mar. Drugs 2020, 18, 534. [Google Scholar] [CrossRef] [PubMed]
  95. Gargouch, N.; Elleuch, F.; Karkouch, I.; Tabbene, O.; Pichon, C.; Gardarin, C.; Rihouey, C.; Picton, L.; Abdelkafi, S.; Fendri, I.; et al. Potential of Exopolysaccharide from Porphyridium marinum to Contend with Bacterial Proliferation, Biofilm Formation, and Breast Cancer. Mar. Drugs. 2021, 19, 66. [Google Scholar] [CrossRef] [PubMed]
  96. Gaignard, C.; Macao, V.; Gardarin, C.; Rihouey, C.; Picton, L.; Michaud, P.; Laroche, C. The red microalga Flintiella sanguinaria as a new exopolysaccharide producer. J. Appl. Phycol. 2018, 30, 2803–2814. [Google Scholar] [CrossRef]
  97. Bafana, A. Characterization and optimization of production of exopolysaccharide from Chlamydomonas reinhardtii. Carbohydr. Polym. 2013, 95, 746–752. [Google Scholar] [CrossRef]
  98. Uhliariková, I.; Matulová, M.; Capek, P. Structural features of the bioactive cyanobacterium Nostoc sp. exopolysaccharide. Int. J. Biol. Macromol. 2020, 164, 2284–2292. [Google Scholar] [CrossRef]
  99. Uhliariková, I.; Šutovská, M.; Barboríková, J.; Molitorisová, M.; Kim, H.J.; Park, Y.I.; Matulová, M.; Lukavský, J.; Hromadková, Z.; Capek, P. Structural characteristics and biological effects of exopolysaccharide produced by cyanobacterium Nostoc sp. Int. J. Biol. Macromol. 2020, 160, 364–371. [Google Scholar] [CrossRef]
  100. Gongi, W.; Cordeiro, N.; Pinchetti, J.L.G.; Ben Ouada, H. Functional, rheological, and antioxidant properties of extracellular polymeric substances produced by a thermophilic cyanobacterium Leptolyngbya sp. J. Appl. Phycol. 2022, 34, 1423–1434. [Google Scholar] [CrossRef]
  101. Wang, Y.Z.; Li, H.; Dong, F.K.; Yan, F.; Cheng, M.; Li, W.Z.; Chang, Q.; Song, T.Z.; Liu, A.Y.; Song, B. Therapeutic Effect of Calcipotriol Pickering Nanoemulsions Prepared by Exopolysaccharides Produced by Bacillus halotolerans FYS Strain on Psoriasis. Int. J. Nanomed. 2020, 15, 10371–10384. [Google Scholar] [CrossRef]
  102. Besednova, N.N.; Smolina, T.P.; Andryukov, B.G.; Kuznetsova, T.A.; Mikhailov, V.V.; Zvyagintseva, T.N. Exopolysaccharides of Marine Bacteria: Prospects for Use in Medicine. Antibiot. Khimiote. 2018, 63, 67–78. [Google Scholar]
  103. Hassan, S.W.M.; Ibrahim, H.A.H. Production, Characterization and Valuable Applications of Exopolysaccharides from Marine Bacillus subtilis SH1. Pol. J. Microbiol. 2017, 66, 449–461. [Google Scholar] [CrossRef]
  104. Wu, M.H.; Pan, T.M.; Wu, Y.J.; Chang, S.J.; Chang, M.S.; Hu, C.Y. Exopolysaccharide activities from probi-otic bifidobacterium: Immunomodulatory effects (on J774A.1 macrophages) and antimicrobial properties. Int. J. Food Microbiol. 2010, 144, 104–110. [Google Scholar] [CrossRef] [PubMed]
  105. Yeh, M.-Y.; Ko, W.-C.; Lin, L.-Y. Hypolipidemic and Antioxidant Activity of Enoki Mushrooms (Flammulina velutipes). BioMed. Res. Int. 2014, 2014, 1–6. [Google Scholar] [CrossRef] [PubMed]
  106. Li, H.; Ding, F.; Xiao, L.; Shi, R.; Wang, H.; Han, W.; Huang, Z. Food-Derived Antioxidant Polysaccharides and Their Pharmacological Potential in Neurodegenerative Diseases. Nutrients 2017, 9, 778. [Google Scholar] [CrossRef]
  107. Wu, R.; Wu, C.; Liu, D.; Yang, X.; Huang, J.; Zhang, J.; Liao, B.; He, H.; Li, H. Overview of Antioxidant Peptides Derived from Marine Resources: The Sources, Characteristic, Purification, and Evaluation Methods. Appl. Biochem. Biotechnol. 2015, 176, 1815–1833. [Google Scholar] [CrossRef] [PubMed]
  108. Valko, M.; Rhodes, C.J.; Moncol, J.; Izakovic, M.; Mazur, M. Free radicals, metals and antioxidants in oxida-tive stress-induced cancer. Chem. Biol. Interact 2006, 160, 1–40. [Google Scholar] [CrossRef] [PubMed]
  109. Acharya, A.; Das, I.; Chandhok, D.; Saha, T. Redox regulation in cancer A double-edged sword with therapeu-tic potential. Oxid. Med. Cell Longev. 2010, 3, 23–34. [Google Scholar] [CrossRef]
  110. Lin, M.T.; Beal, M.F. The oxidative damage theory of aging. Clin. Neurosci. Res. 2003, 2, 305–315. [Google Scholar] [CrossRef]
  111. Pereira, M.D.; Ksiazek, K.; Menezes, R. Oxidative Stress in Neurodegenerative Diseases and Ageing. Oxidative Med. Cell. Longev. 2012, 2012, 376–385. [Google Scholar] [CrossRef]
  112. Pisoschi, A.M.; Pop, A. The role of antioxidants in the chemistry of oxidative stress: A review. Eur. J. Med. Chem. 2015, 97, 55–74. [Google Scholar] [CrossRef]
  113. Squillaci, G.; Finamore, R.; Diana, P.; Restaino, O.F.; Schiraldi, C.; Arbucci, S.; Ionata, E.; La Cara, F.; Morana, A. Production and properties of an exopolysaccharide synthesized by the extreme halophilic archaeon Haloterrigena turkmenica. Appl. Microbiol. Biot. 2016, 100, 613–623. [Google Scholar] [CrossRef]
  114. Xiao, R.; Yang, X.; Li, M.; Li, X.; Wei, Y.; Cao, M.; Ragauskas, A.; Thies, M.; Ding, J.; Zheng, Y. Investigation of composition, structure and bioactivity of extracellular polymeric substances from original and stress-induced strains of Thraustochytrium striatum. Carbohydr. Polym. 2018, 195, 515–524. [Google Scholar] [CrossRef]
  115. Sun, M.-L.; Liu, S.-B.; Qiao, L.-P.; Chen, X.-L.; Pang, X.; Shi, M.; Zhang, X.-Y.; Qin, Q.-L.; Zhou, B.-C.; Zhang, Y.-Z.; et al. A novel exopolysaccharide from deep-sea bacterium Zunongwangia profunda SM-A87: Low-cost fermentation, moisture retention, and antioxidant activities. Appl. Microbiol. Biotechnol. 2014, 98, 7437–7445. [Google Scholar] [CrossRef]
  116. Chen, B.; You, W.; Huang, J.; Yu, Y.; Chen, W. Isolation and antioxidant property of the extracellular polysaccharide from Rhodella reticulata. World J. Microbiol. Biotechnol. 2009, 26, 833–840. [Google Scholar] [CrossRef]
  117. Groeber, F.; Holeiter, M.; Hampel, M.; Hinderer, S.; Schenke-Layland, K. Skin tissue engineering—In vivo and in vitro applications. Adv. Drug Deliv. Rev. 2011, 63, 352–366. [Google Scholar] [CrossRef] [PubMed]
  118. Gautam, S.; Chou, C.F.; Dinda, A.K.; Potdar, P.D.; Mishra, N.C. Surface modification of nanofibrous poly-caprolactone/gelatin composite scaffold by collagen type I grafting for skin tissue engineering. Mat. Sci. Eng. C Mater. 2014, 34, 402–409. [Google Scholar] [CrossRef] [PubMed]
  119. Zhou, X.; Ning, K.; Ling, B.; Chen, X.; Cheng, H.; Lu, B.; Gao, Z.; Xu, J. Multiple Injections of Autologous Adipose-Derived Stem Cells Accelerate the Burn Wound Healing Process and Promote Blood Vessel Regeneration in a Rat Model. Stem Cells Dev. 2019, 28, 1463–1472. [Google Scholar] [CrossRef]
  120. Petruk, G.; Roxo, M.; De Lise, F.; Mensitieri, F.; Notomista, E.; Wink, M.; Izzo, V.; Monti, D.M. The marine Gram-negative bacterium Novosphingobium sp. PP1Y as a potential source of novel metabolites with antioxidant activity. Biotechnol. Lett. 2018, 41, 273–281. [Google Scholar] [CrossRef] [PubMed]
  121. Fedorov, S.N.; Ermakova, S.P.; Zvyagintseva, T.N.; Stonik, V.A. Anticancer and Cancer Preventive Properties of Marine Polysaccharides: Some Results and Prospects. Mar. Drugs. 2013, 11, 4876–4901. [Google Scholar] [CrossRef] [PubMed]
  122. Bhatnagar, I.; Kim, S.-K. Immense Essence of Excellence: Marine Microbial Bioactive Compounds. Mar. Drugs 2010, 8, 2673–2701. [Google Scholar] [CrossRef] [PubMed]
  123. De Carvalho, C.C.C.R.; Fernandes, P. Production of Metabolites as Bacterial Responses to the Marine Environment. Mar. Drugs. 2010, 8, 705–727. [Google Scholar] [CrossRef] [PubMed]
  124. Satpute, S.K.; Banat, I.M.; Dhakephalkar, P.K.; Banpurkar, A.G.; Chopade, B.A. Biosurfactants, bioemulsifiers and exopolysaccharides from marine microorganisms. Biotechnol. Adv. 2010, 28, 436–450. [Google Scholar] [CrossRef] [PubMed]
  125. Aullybux, A.A.; Puchooa, D.; Bahorun, T.; Jeewon, R.; Wen, X.S.; Matin, P. Antioxidant and Cytotoxic Activities of Exopolysaccharides from Alcaligenes faecalis Species Isolated from the Marine Environment of Mauritius. J. Polym. Environ. 2022, 30, 1462–1477. [Google Scholar] [CrossRef]
  126. Liu, G.; Liu, R.; Shan, Y.; Sun, C. Marine bacterial exopolysaccharide EPS11 inhibits migration and invasion of liver cancer cells by directly targeting collagen I. J. Biol. Chem. 2021, 297. [Google Scholar] [CrossRef]
  127. Cao, C.; Li, Y.; Wang, C.; Zhang, N.; Zhu, X.; Wu, R.; Wu, J. Purification, characterization and antitumor activity of an exopolysaccharide produced by Bacillus velezensis SN-1. Int. J. Biol. Macromol. 2020, 156, 354–361. [Google Scholar] [CrossRef]
  128. Matsuda, M.; Yamori, T.; Naitoh, M.; Okutani, K. Structural Revision of Sulfated Polysaccharide B-1 Isolated from a Marine Pseudomonas Species and Its Cytotoxic Activity Against Human Cancer Cell Lines. Mar. Biotechnol. 2003, 5, 13–19. [Google Scholar] [CrossRef] [PubMed]
  129. Yahya, S.M.M.; Abdelnasser, S.M.; Hamed, A.R.; El Sayed, O.H.; Asker, M.S. Newly isolated marine bacterial exopolysaccharides enhance antitumor activity in HepG2 cells via affecting key apoptotic factors and activating toll like receptors. Mol. Biol. Rep. 2019, 46, 6231–6241. [Google Scholar] [CrossRef] [PubMed]
  130. Koyanagi, S.; Tanigawa, N.; Nakagawa, H.; Soeda, S.; Shimeno, H. Oversulfation of fucoidan enhances its anti-angiogenic and antitumor activities. Biochem. Pharmacol. 2003, 65, 173–179. [Google Scholar] [CrossRef]
  131. Chaisuwan, W.; Jantanasakulwong, K.; Wangtueai, S.; Phimolsiripol, Y.; Chaiyaso, T.; Techapun, C.; Phongthai, S.; You, S.; Regenstein, J.M.; Seesuriyachan, P. Microbial exopolysaccharides for immune enhancement: Fermentation, modifications and bioactivities. Food Bio. Sci. 2020, 35, 100564. [Google Scholar] [CrossRef]
  132. Tang, Y.; Cui, Y.; De Agostini, A.; Zhang, L. Chapter Eighteen—Biological mechanisms of glycan and glycosaminoglycan based nutraceuticals. Prog. Mol. Biol. Transl. Sci. 2019, 163, 445–469. [Google Scholar] [PubMed]
  133. Rubini, D.; Varthan, P.V.; Jayasankari, S.; Vedahari, B.N.; Nithyanand, P. Suppressing the phenotypic virulence factors of Uropathogenic Escherichia coli using marine polysaccharide. Microb Pathog. 2020, 141, 103973. [Google Scholar] [CrossRef] [PubMed]
  134. Huleihel, M.; Ishanu, V.; Tal, J.; Arad, S. Antiviral effect of red microalgal polysaccharides on Herpes simplex and Varicella zoster viruses. J. Appl. Phycol. 2001, 13, 127–134. [Google Scholar] [CrossRef]
  135. Huheihel, M.; Ishanu, V.; Tal, J.; Arad, S. Activity of Porphyridium sp. polysaccharide against herpes simplex viruses in vitro and in vivo. J. Biochem. Biophys. Methods 2001, 50, 189–200. [Google Scholar] [CrossRef]
  136. Burston, M.; Ranasinghe, K.; Gardi, A.; Parezanović, V.; Ajaj, R.; Sabatini, R. Design principles and digital control of advanced distributed propulsion systems. Energy 2021, 241, 122788. [Google Scholar] [CrossRef]
  137. Naik, S.R.; Wala, S.M. Inflammation, Allergy and Asthma, Complex Immune Origin Diseases: Mechanisms and Therapeutic Agents. Recent Patents Inflamm. Allergy Drug Discov. 2013, 7, 62–95. [Google Scholar] [CrossRef]
  138. Arena, A.; Maugeri, T.L.; Pavone, B.; Iannello, D.; Gugliandolo, C.; Bisignano, G. Antiviral and immunoregulatory effect of a novel exopolysaccharide from a marine thermotolerant Bacillus licheniformis. Int. Immunopharma. Col. 2006, 6, 8–13. [Google Scholar] [CrossRef] [PubMed]
  139. Sarkar, S.; Banerjee, A.; Halder, U.; Biswas, R.; Bandopadhyay, R. Degradation of Synthetic Azo Dyes of Textile Industry: A Sustainable Approach Using Microbial Enzymes. Water Conserv. Sci. Eng. 2017, 2, 121–131. [Google Scholar] [CrossRef]
  140. Crini, G.; Lichtfouse, E. Advantages and disadvantages of techniques used for wastewater treatment. Environ. Chem. Lett. 2019, 17, 145–155. [Google Scholar] [CrossRef]
  141. Bai, Y.; Zhang, P.; Chen, G.; Cao, J.; Huang, T.; Chen, K. Macrophage immunomodulatory activity of extracellular polysaccharide (PEP) of Antarctic bacterium Pseudoaltermonas sp.S-5. Int Immunopharmacol 2012, 12, 611–617. [Google Scholar] [CrossRef]
  142. Aktan, F. iNOS-mediated nitric oxide production and its regulation. Life Sci. 2004, 75, 639–653. [Google Scholar] [CrossRef]
  143. Bujak, M.; Frangogiannis, N.G. The role of IL-1 in the pathogenesis of heart disease. Arch. Immunol. Et Ther. Exp. 2009, 57, 165–176. [Google Scholar] [CrossRef] [PubMed]
  144. Xing, Z.; Gauldie, J.; Cox, G.; Baumann, H.; Jordana, M.; Lei, X.F.; Achong, M.K. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J. Clin. Investig. 1998, 101, 311–320. [Google Scholar] [CrossRef]
  145. VanAntwerp, D.J.; Martin, S.J.; Kafri, T.; Green, D.R.; Verma, I.M. Suppression of TNF-alpha-induced apoptosis by NF-kappa B. Science 1996, 274, 787–789. [Google Scholar] [CrossRef]
  146. Chen, S.; Ding, R.; Zhou, Y.; Zhang, X.; Zhu, R.; Gao, X.-D. Immunomodulatory Effects of Polysaccharide from Marine Fungus Phoma herbarumYS4108 on T Cells and Dendritic Cells. Mediat. Inflamm. 2014, 2014, 1–13. [Google Scholar] [CrossRef]
  147. Syafiuddin, A.; Fulazzaky, M.A. Decolorization kinetics and mass transfer mechanisms of Remazol Brilliant Blue R dye mediated by different fungi. Biotechnol. Rep. 2020, 29, e00573. [Google Scholar] [CrossRef] [PubMed]
  148. Sutherland, I.W. Biofilm exopolysaccharides: A strong and sticky framework. Microbiology 2001, 147, 3–9. [Google Scholar] [CrossRef]
  149. Zhou, W.; Shen, B.; Meng, F.; Liu, S.; Zhang, Y. Coagulation enhancement of exopolysaccharide secreted by an Antarctic sea-ice bacterium on dye wastewater. Sep. Purif. Technol. 2010, 76, 215–221. [Google Scholar] [CrossRef]
  150. Yang, S.-F.; Li, X.-Y. Influences of extracellular polymeric substances (EPS) on the characteristics of activated sludge under non-steady-state conditions. Process Biochem. 2009, 44, 91–96. [Google Scholar] [CrossRef]
  151. Parmar, P.; Shukla, A.; Goswami, D.; Gaur, S.; Patel, B.; Saraf, M. Comprehensive depiction of novel heavy metal tolerant and EPS producing bioluminescent Vibrio alginolyticus PBR1 and V. rotiferianus PBL1 confined from marine organisms. Microbiol. Res. 2020, 238, 126526. [Google Scholar] [CrossRef]
  152. Xu, C.; Lin, P.; Zhang, S.; Sun, L.; Xing, W.; Schwehr, K.A.; Chin, W.-C.; Wade, T.L.; Knap, A.H.; Hatcher, P.G.; et al. The interplay of extracellular polymeric substances and oil/Corexit to affect the petroleum incorporation into sinking marine oil snow in four mesocosms. Sci. Total Environ. 2019, 693, 133626. [Google Scholar] [CrossRef] [PubMed]
  153. Iwabuchi, N.; Sunairi, M.; Urai, M.; Itoh, C.; Anzai, H.; Nakajima, M.; Harayama, S. Extracellular polysaccharides of Rhodococcus rhodochrous S-2 stimulate the degradation of aromatic components in crude oil by indigenous marine bacteria. Appl. Env. Microb 2002, 68, 2337–2343. [Google Scholar] [CrossRef]
  154. Pepi, M.; Ro, A.C.; Liut, G.; Baldi, F. An antarctic psychrotrophic bacterium Halomonas sp. ANT-3b, growing on n-hexadecane, produces a new emulsyfying glycolipid. FEMS Microbiol. Ecol. 2005, 53, 157–166. [Google Scholar] [CrossRef] [PubMed]
  155. Ilori, M.O.; Amobi, C.J.; Odocha, A.C. Factors affecting biosurfactant production by oil degrading Aeromonas spp. isolated from a tropical environment. Chemosphere 2005, 61, 985–992. [Google Scholar] [CrossRef] [PubMed]
  156. Martin, A.H.; Pearson, H.C.; Saba, G.K.; Olsen, E.M. Integral functions of marine vertebrates in the ocean carbon cycle and climate change mitigation. One Earth 2021, 4, 680–693. [Google Scholar] [CrossRef]
  157. Ameen, F.; AlNadhari, S.; Al-Homaidan, A.A. Marine microorganisms as an untapped source of bioactive compounds. Saudi J. Biol. Sci. 2020, 28, 224–231. [Google Scholar] [CrossRef] [PubMed]
  158. Jimeno, J.; Faircloth, G.; Sousa-Faro, J.F.; Scheuer, P.; Rinehart, K. New Marine Derived Anticancer Therapeutics—A Journey from the Sea to Clinical Trials. Mar. Drugs. 2004, 2, 14–29. [Google Scholar] [CrossRef]
  159. Mitra, T.; Sailakshmi, G.; Gnanamani, A.; Raja, S.T.K.; Thiruselvi, T.; Gowri, V.M.; Selvaraj, N.V.; Ramesh, G.; Mandal, A. Preparation and characterization of a thermostable and biodegradable biopolymers using natural cross-linker. Int. J. Biol. Macromol. 2011, 48, 276–285. [Google Scholar] [CrossRef]
  160. Arnosti, C. Microbial Extracellular Enzymes and the Marine Carbon Cycle. Annu. Rev. Mar. Sci. 2011, 3, 401–425. [Google Scholar] [CrossRef]
  161. Marx, J.G.; Carpenter, S.D.; Deming, J.W. Production of cryoprotectant extracellular polysaccharide substances (EPS) by the marine psychrophilic bacterium Colwellia psychrerythraea strain 34H under extreme conditions. This article is one of a selection of papers in the Special Issue on Polar and Alpine Microbiology. Can. J. Microbiol. 2009, 55, 63–72. [Google Scholar]
  162. Mergelov, N.; Dolgikh, A.; Shorkunov, I.; Zazovskaya, E.; Soina, V.; Yakushev, A.; Fedorov-Davydov, D.; Pryakhin, S.; Dobryansky, A. Hypolithic communities shape soils and organic matter reservoirs in the ice-free landscapes of East Antarctica. Sci. Rep. 2020, 10, 1–19. [Google Scholar] [CrossRef]
  163. Gray, A.; Krolikowski, M.; Fretwell, P.; Convey, P.; Peck, L.S.; Mendelova, M.; Smith, A.G.; Davey, M.P. Re-mote sensing reveals Antarctic green snow algae as important terrestrial carbon sink. Nat. Commun. 2020, 11, 2527. [Google Scholar] [CrossRef]
  164. Anesio, A.M.; Sattler, B.; Foreman, C.; Telling, J.; Hodson, A.; Tranter, M.; Psenner, R. Carbon fluxes through bacterial communities on glacier surfaces. Ann. Glaciol. 2010, 51, 32–40. [Google Scholar] [CrossRef]
  165. Anesio, A.M.; Hodson, A.J.; Fritz, A.; Psenner, R.; Sattler, B. High microbial activity on glaciers: Importance to the global carbon cycle. Glob. Chang. Biol. 2009, 15, 955–960. [Google Scholar] [CrossRef]
Marinedrugs 20 00512 g001 550
Figure 1. Structures of several EPS, isolated from marine fungi in the last decade [74,83,84,85,86,87,88]. (a) EPS from Penicillium solitum; (b) EPS from Aspergillus versicolor; (c) EPS from Fusarium oxysporum; (d) EPS from Alternaria sp.; (e) EPS from Hansfordia sinuosae; (f) EPS from Aureobasidium melanogenum.
Figure 1. Structures of several EPS, isolated from marine fungi in the last decade [74,83,84,85,86,87,88]. (a) EPS from Penicillium solitum; (b) EPS from Aspergillus versicolor; (c) EPS from Fusarium oxysporum; (d) EPS from Alternaria sp.; (e) EPS from Hansfordia sinuosae; (f) EPS from Aureobasidium melanogenum.
Marinedrugs 20 00512 g001
Marinedrugs 20 00512 g002 550
Figure 2. Main biological activities of EPS from marine microorganisms.
Figure 2. Main biological activities of EPS from marine microorganisms.
Marinedrugs 20 00512 g002
Marinedrugs 20 00512 g003 550
Figure 3. Potential mechanisms of ferroptosis-related immunomodulatory of AUM-1 [74].
Figure 3. Potential mechanisms of ferroptosis-related immunomodulatory of AUM-1 [74].
Marinedrugs 20 00512 g003
Table
Table 1. Information of some EPS obtained from marine bacteria in the last decade.
Table 1. Information of some EPS obtained from marine bacteria in the last decade.
SourceNamePreparation MethodMonosaccharides
Composition		Mw (Da)BioactivityReferences
Pantoea sp. YU16-S3EPS-S3Ethanol precipitation extraction and purification by
Sephacryl S500-HR column		Glc, Gal, GalNAc, GalN
(1.9:1:0.4:0.02)		1.75 × 105Promotion of Wound Healing[34]
Pediococcus pentosaceus M41EPS-M41Culture centrifugal extraction and purification by ultra-filtrationAra, Man, Glc, Gal
(1.2:1.8:15.1:1.0)		6.8 × 105Antioxidant,
Anticancer		[40]
Bacillus cereus KMS3-1EPSCulture centrifugal extraction and purification by dialysisMan, Glc, Xyl, Rha
(73.51:17.87:2.18:6.49)		 Waste-water
treatment		[41]
Oceanobacillus iheyensisEPSEthanol precipitation and
purification by dialysis		Man, Glc, Ara
(47.78:29.71:22.46)		2.14 × 106Anti-biofilm[43]
Bacillus thuringiensis RSK CAS4EPSCulture centrifugal extraction and purification by Sepharose 4-LB Fast Flow columnFuc, Gal, Xyl, Glc, Rha, Man
(43.8:20:17.8:7.2:7.1:4.1)		 Antioxidant,
Anticancer		[42]
Pseudoalteromonas, MD12-642EPSCulture centrifugal extraction and purification by ultra-filtrationGalA, GlcA, Rha, GlcN
(41–42:25–26:16–22:12–16)		>1.0 × 106 [44]
Bacillus sp. H5EPS5SHAqueous extraction and purification by GPCMan, GlcN, Glc, Gal
(1.00:0.02:0.07:0.02)		8.9 × 104Immunomodulatory activity[45]
Alteromonas sp. JL2810EPSEthanol precipitation extraction and purification by DEAE columnGalA, Man, Rha
(1:1:1)		>1.67 × 105 [46]
Pseudoalteromonas sp. YU16-DR3AEPS-DR3ACulture centrifugal extraction and purification by dialysisFuc, Erythrotetrose, Glc, Rib
(6.7:1.0:1.5:1.0)		2 × 104Antioxidant[47]
Enterobacter sp. ACD2EPSCulture centrifugal extractionGlc, Gal, Fuc, GlcA
(25:25:40:10)		 Antibacterial[48]
P. stutzeri 273EPS273Culture centrifugal extraction and purification by GPCGlcN, Rha, Glc
(35.4:28.6:27.2)		1.9 × 105Antibiofilm,
Anti-Infection		[49]
Microbacterim
FSW-25		EPS Mi25Culture centrifugal extraction and purification by dialysisGlc, Man, Fuc, GlcA7.0 × 106Antioxidant[50]
Bacillus cereusEPSR3Culture centrifugal extractionGlc, GalA, Arb
(2.0: 0.8: 1.0)		 Antioxidant,
Antitumor, Anti-inflammatory activities		[51]
Vibrio sp. QY101A101Ethanol precipitation extraction and purification by GPCGlcA, GalA, Rha, GlcN
(21.47:23.05:23.90:12.15)		5.46 × 103Antibacterial[52]
Halolactibacillus miurensisEPSCulture centrifugal extraction and purification by Sepharose 4-LB Fast Flow columnGal, Glc
(61.87:25.17)		 Antioxidant[53]
Halomonas saliphila LCB169ThsEPSEthanol precipitation, anion-exchange and gel-filtration chromatographyMan, Glc, Ara, Xyl, Gal, Fuc
(81.22:15.83:1.47:0.59:0.55:0.35)		5.133 × 104Emulsifying activity[54]
C.psychrerythraea 34HEPSCulture centrifugal extraction and purification by QFF
column		QuiN, GalA
(1:2)		 Antifreeze[26]
IssachenkoniiSM20310Ethanol precipitation
extraction and purification by DEAE column		Rha, Xyl, Man, Gal, Glc, GalNAc, GlcNAc
(2.1:0.9:71.7:9.0:10.7:1.5:4.0)		>2.0 × 106Anti-freeze[55]
Halomonas sp. 2E1EPS2E1Culture centrifugal extraction and purification by DEAE column and Sephadex G75 columnMan, Glc
(3.76:1)		4.7 × 104Immunomodulatory activity[56]
Sphingobacterium sp. IITKGP-BTPF3SphingobatanCulture centrifugal extraction and purification by DEAE columnMan>2 × 106Immunomodulatory activity[57]
Pseudoaltermonas sp.PEPCulture centrifugal extraction and purification by dialysis and GPCGlc, Gal, Man
(4.8:50.9:44.3)		3.97 × 105Anticancer[58]
Polaribacter sp.SM1127 EPSEthanol precipitation extraction and purification by Sepharose columnRha, Fuc, GlcA, Man, Gal, Glc, GlcNAc
(0.8:7.4:21.4:23.4:17.3:1.6:28.0)		2.2 × 105Promotion of Wound Healing, Prevention
of Frostbite Injury, Antioxidant		[59,60]
Aeribacillus pallidus 418EPS1,
EPS2		Culture centrifugal extraction and purification by Sepharose DEAE CL-6B columnMan, Glc, GalN, GlcN, Gal, Rib
(69.3:11.2:6.3:5.4:4.7:2.9);
Man, Gal, Glc, GalN, GlcN, Rib, Ara
(33.9:17.9:15.5:11.7:8.1:5.3:4.9)		7 × 105;
>1 × 106		 [31]
Rhodobacter johrii CDR-SL 7CiiEPS RH-7Ethanol precipitation and purification by dialysisGlc, GlcA, Rha, Gal
(3:1.5:0.25:0.25)		2 × 106Emulsifying
activity		[61]
Alteromonas ininusGY785Culture centrifugal extraction and purification by
ultra-filtration		Rha, Fuc, Man, Gal, Glc, GalA, GlcA
(0.2:0.1:0.4: 3.6:4.7:1.0:2.0)		2.0 × 106 [62,63]
Table
Table 2. Information of some EPS obtained from marine fungi in the last decade.
Table 2. Information of some EPS obtained from marine fungi in the last decade.
SourceNamePreparation MethodMonosaccharides
Composition		Mw (Da)BioactivityReferences
Aureobasidium
melanogenum
SCAU-266		AUM-1Alcohol precipitation and further purified through DEAE-columnGlc, Man, Gal
(97.30:1.9:0.08)		6.0 × 103Immunomodulatory activity[74]
Aspergillus TerreusYSSCulture centrifugal extraction and purification by QFF columnGlc, Man
(8.6:1.0)		1.86 × 104Antioxidant[82]
Fusarium oxysporumFw-1Culture centrifugal extraction and purification by QFF columnGal, Glc, Man
(1.33:1.33:1.00)		6.12 × 104Antioxidant[83]
Alternaria sp. AS2-1Culture centrifugal extraction and purification by QFF columnMan, Glc, Gal
(1.00:0.67:0.35)		2.74 × 104Anticancer,
Antioxidant		[84]
Aspergillus versicolorAWPCulture centrifugal extractionand purification by QFF columnGlc, Man
(8.6:1.0)		5 × 107 [85]
Aspergillus versicolorLCJ-5-4Culture centrifugal extractionand purification by QFF columnGlc, Man
(1.7:1.0)		7 × 103Antioxidant[86]
Penicillium solitumGW-12Ethanol precipitation,
anion-exchange and size exclusion chromatography		Man1.13 × 104 [87]
Hansfordia sinuosaeHPAEthanol precipitation,
anion-exchange and size exclusion chromatography		Man, Gal, Glc,
(96.1, 3.3, and 0.60)		2.25 × 104Anticancer[88]
Table
Table 3. Information of some EPS obtained from marine microalgae and cyanobacteria in the last decade.
Table 3. Information of some EPS obtained from marine microalgae and cyanobacteria in the last decade.
SourceNamePreparation MethodMonosaccharides CompositionMw (Da)BioactivityReferences
Porphyridium sordidumEPSCold aqueous centrifugal
extraction and purification by dialysis		Fuc, Rha, Ara, Gal, Glc, Xyl, GlcA (1.93:0.36:0.36:48.28: 19.01:28.2:0.76) Antibacterial[24]
Porphyridium marinumEPS-0C,
EPS-2C,
EPS-5C		Culture centrifugal extraction, ultra-filtration and High-Pressure HomogenizerXyl, Gal, Glc, Fuc, Ara, GlcA
(44–47:25–29:19–20:1:1–2:4–5)		1.4 × 106
5.5 × 105
5.5 × 105		Antibacterial,
Anti-biofilm, Anticancer		[95]
Flintiella
sanguinaria		EPSCulture centrifugal extraction and purification by
ultra-filtration		Xyl, Gal, GlcA, Rha, Glc, Ara
(47:21:14:10:6:2)		1.5 × 106 [96]
Cyanothece sp. CCY 0110CyanoflanCold aqueous extraction
and purification by dialysis		Man, Glc, uronic acid, Gal, Xyl, Rha, Fuc, Ara (20:20:18:10:9:9:8:6)>1 × 106 [75]
Chlamydonas
reinhardtii		EPSCulture centrifugal
extraction		GalA, Rib, Rha, Ara, Gal, Glc, Xyl2.25 × 105Antioxidant[97]
Nostoc
carneum		EPSCulture centrifugal
extraction		Xyl, Glc
(4.3:2.1)		 Antioxidant[93]
Nostoc sp.EPSCulture centrifugal extraction and purification by DEAE columnUronic acid, Rha, Fuc, Ara, Xyl, Man, Gal, Glc
(25.0:0.2:0.8:18.6:15.3:19.1:1.3:19.7)		2.37 × 105Antitussive, Immunomodulatory activity[98,99]
Tetraselmis suecicaEPSCold aqueous extractionand purification by dialysisAra, Rib, Man, GalA, Gal, Glc, GlcA (5.23:0.83:6.64:0.1:25.27:35.46:21.47) Antioxidant, Anticancer[94]
Leptolyngbya sp.EPSCulture centrifugal
extraction		Man, Ara, Glc, Rha, uronic acid (35:24:15:2:8) Antioxidant[100]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Qi, M.; Zheng, C.; Wu, W.; Yu, G.; Wang, P. Exopolysaccharides from Marine Microbes: Source, Structure and Application. Mar. Drugs 2022, 20, 512. https://doi.org/10.3390/md20080512

AMA Style

Qi M, Zheng C, Wu W, Yu G, Wang P. Exopolysaccharides from Marine Microbes: Source, Structure and Application. Marine Drugs. 2022; 20(8):512. https://doi.org/10.3390/md20080512

Chicago/Turabian Style

Qi, Mingxing, Caijuan Zheng, Wenhui Wu, Guangli Yu, and Peipei Wang. 2022. "Exopolysaccharides from Marine Microbes: Source, Structure and Application" Marine Drugs 20, no. 8: 512. https://doi.org/10.3390/md20080512

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop