Marine Microbial Polysaccharides: History
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Contributor:
Rajesh Jeewon
,
Aadil Ahmad Aullybux
,
Daneshwar Puchooa
,
Nadeem Nazurally
,
Abdulwahed Fahad Alrefaei
,
Ying Zhang

One of the most promising properties displayed by marine microbial polysaccharides is their biological activities. Indeed, it is not uncommon for studies to investigate such characteristics in view of presenting these polymers as attractive candidates for biomedical applications, with some of the most studied biological activities being anticancer, antimicrobial, anti-oxidant, and immunomodulation.

  • microorganisms
  • marine
  • polysaccharides
  • diversity
  • biotechnological applications

1. Introduction

Over the past few years, there has been increasing interest in the development of natural polymers, also referred to as biopolymers, for industrial applications [1], and in particular, polysaccharides have been gaining much attention in the biomedical, cosmetic, food, and pharmaceutical fields. Although polysaccharides can be produced by different types of organisms (e.g., bacteria, fungi, algae, crustaceans, and plants), those from bacteria and fungi have been highly popular as they replicate rapidly, are easier to manipulate, and are abundant producers of those polymers, with the latter also more easily separated than those from non-microbial counterparts [2][3]. Furthermore, in addition to their biological activities, they also display low toxicity, biocompatibility, biodegradability, and other physical and chemical characteristics [4][5][6][7].
An overview of these microbial compounds suggests that they are usually macromolecules of high molecular weight and are made up of at least 10 monosaccharide units held together by glycosidic bonds [8]. They can also be either linear or branched in structure, while in terms of content, they may be classified as homopolysaccharides or heteropolysaccharides if they, respectively, contain one type or different types of monosaccharides [7][8][9]. In the latter case, while D-glucose is often the most common constituent, other sugars (e.g., D-xylose, D-mannose, D-galactose, L-galactose, L-arabinose, and D-fructose) may also be present alongside derivatives such as simple sugar acids (glucuronic and iduronic acids) or amino sugars (D-glucosamine and D-galactosamine) [10]. Finally, in addition to the above sugars, the presence of non-organic moieties, including sulfates, phosphates, pyruvates, and acetates, is also frequently noted [4][5]. Altogether, different combinations of these variable features contribute to the extensive compositional and structural diversity displayed by microbial polysaccharides.

2. Current Research on Marine Microbial Polysaccharides

Over the years, the potential of microbial polysaccharides for biotechnological applications became increasingly recognized, as reflected by the number of studies on the subject, with Osemwegie et al. [2], as reported by Nadzir et al. [11], identifying thousands of publications focused on microbial polysaccharides between 1976 and 2018 alone. Although many of these did not specifically involve marine species, a survey of the literature suggests a similar trend as far as marine microbial polysaccharides are concerned. The following sections provide an overview of the current trends in research on marine polysaccharides from bacterial and fungal species.

2.1. Biomedical Applications

One of the most promising properties displayed by marine microbial polysaccharides is their biological activities. Indeed, it is not uncommon for studies to investigate such characteristics in view of presenting these polymers as attractive candidates for biomedical applications, with some of the most studied biological activities being anticancer, antimicrobial, anti-oxidant, and immunomodulation [12].

2.1.1. Anticancer Activity

Cancer, characterised by an uncontrolled proliferation of cells, is currently one of the major diseases affecting human health, as well as the second cause of death in the world, with an estimated 18.1 million people diagnosed with the condition in 2018 [13][14]. So far, surgery, chemotherapy, and radiotherapy remain the main forms of treatment for different types of cancers, but these approaches are not without side effects, which include a number of health complications as well as toxicity and/or injury to non-targeted organs and cells [13][15][16]. Consequently, the search for alternative forms of treatment has prompted interest in natural compounds, with results of studies often highlighting the potential of marine microbial polysaccharides for such applications.
Indeed, the anticancer activities of polysaccharides from marine bacteria and fungi are already well established, with cytotoxic effects often reported against lung [17], liver [18][19][20][21], breast [14][20][22][23][24], cervical [20], and colorectal cancers [14]. In these cases, the apoptosis of cancer cells seems to be a common mechanism, although programmed cell death can be mediated through different pathways. These different mechanisms of action are particularly obvious from studies in which different polysaccharides were tested against different cell lines. For example, Tukenmez et al. [25] noted changes in the gene and protein expression of Bax, Bcl-2, Caspase 3, Caspase 9, and Survivin when EPSs of L. delbrueckii ssp. Bulgaricus were tested against colon cancer cells at a concentration of 400 µg/mL for 24 h or 48 h. The EPS consisted of glucose, mannose, fructose, sucrose, maltose, and N-acetylglucosamine, with the observed effects attributed to the glucose and mannose content. In contrast, within a concentration range of 5–80 μg/mL, marine polysaccharides from Bacillus velezensis activated caspase-3 while increasing levels of cytochrome C to induce apoptosis in breast cancer cells [23]. Such differences in the mechanism of action could arguably be attributed to differences in the composition and/or structure of the two polysaccharides, as suggested by Tukenmez et al. [25], although the influence of other factors is not excluded. In addition, within similar cell lines, anticancer effects may also occur through different mechanisms. For instance, Cao et al. [17] reported the isolation of EPS11, a 22.3 kDa polysaccharide fraction made up of glucose, mannose, xylose, glucosamine, and galacturonic acid, from a marine Bacillus species. At varying concentrations up to 90 nM, the authors showed that this polymer could not only affect cell proliferation and adhesion of lung (A549) and liver (Huh7.5) cells, but also induce apoptosis by preventing the expression of βIII-tubulin, as well as reducing the phosphorylation of protein kinase B (PKB or AKT). However, the same polysaccharide also downregulated proteins related to the extracellular matrix–receptor interaction signaling pathway and targeted collagen I through the β1-integrin-mediated signaling pathway to prevent cell adhesion, migration, and invasion [19]. This feature of polysaccharides is, in fact, of practical significance, as the ability to induce anticancer effects through different mechanisms may reduce the likelihood that a particular cell line develops resistance to therapy, as is currently the case for a number of chemotherapeutic drugs [26].

2.1.2. Antimicrobial Activity

Another biological activity of microbial polysaccharides that is commonly investigated is their ability to inhibit the growth and/or proliferation of pathogenic microorganisms. This property is particularly relevant nowadays due to the emergence of drug-resistant pathogens that constantly threaten public health, thereby prompting the need to develop new and more potent antibiotics [27][28]. In this context, Aullybux et al. [29] isolated two sulfated EPSs from a marine Alcaligenes and Halomonas sp., which could, in addition to different pathogens, also inhibit the growth of methicillin-resistant Staphylococcus aureus (MRSA) at concentrations between 0.25 and 2 mg/mL. Although not specifically attributed to any particular features of the polymers, the authors argued that the antibacterial activities could be linked to the presence of certain functional groups that are known to act as metal chelators. Similarly, polysaccharides (1 mg/mL) from a haloalkalitolerant Alkalibacillus sp., recovered from a salt lake, displayed antibacterial effects against Candida albicans, as well as a number of Gram-positive and Gram-negative bacteria [30].
Although these studies did not determine the underlying mechanism of the antimicrobial properties, this can be inferred based on existing reports from other non-marine polysaccharides. For example, electrostatic interactions between oppositely charged polysaccharides and pathogens’ cell walls, as well as the latter’s subsequent hydrolysis to leak cell content, have been suggested as one of the mechanisms responsible for the observed antimicrobial activities [29]. Similarly, Zhou et al. [31] proposed that interactions between polysaccharides and biofilm-related signal molecules or cell-surface receptors of pathogens could disrupt cell communication and biofilm formation, while Rajoka et al. [32] suggested that metal chelation, as well as nutrient suppression through the formation of an external barrier, could represent additional ways through which antimicrobial properties are exerted.
However, while the antimicrobial properties of bacterial and fungal polysaccharides are well known, those derived from marine species are yet to be widely studied, as is the case for their terrestrial counterparts. As will be discussed in subsequent sections, this could likely be due to the different challenges encountered in the study of marine microbial polysaccharides. Nevertheless, this undoubtedly represents a research gap that, if addressed, could potentially yield new classes of antibiotics to assist the fight against resistant pathogens [33].

2.1.3. Anti-Oxidant Activity

Bacterial or fungal polysaccharides, especially those that display biological activities, have been considered not only for their cytotoxicity or antibacterial effects but also for their anti-oxidant potential [34][35]. Nowadays, it is not uncommon to come across studies that highlight the anti-oxidant potential of compounds, probably because it is intrinsically linked to human health.
Tissues in the human body require oxygen for energy production, but as the oxygen is consumed, those tissues generate free radicals as by-products [36]. Free radicals are, basically, reactive and unstable molecules containing unpaired electrons, and they can be grouped into either reactive nitrogen species (RNSs) or reactive oxygen species (ROSs) [36][37]. These compounds are normally maintained at a suitable concentration by balancing the body’s production of free radicals through a defence system involving anti-oxidant enzymes [38]. However, in addition to cellular production, external sources such as radiation, chemicals, pollutants, cigarettes, alcohol, some drugs, or heavy metals, just to name a few, can also contribute substantially to the levels of ROS/RNS [38]. These can undoubtedly cause an imbalance, especially if the body is no longer able to counteract the additional production of free radicals, hence resulting in a condition of oxidative/nitrosative stress. Under this condition, these excess radicals, especially ROS, interact with various biological macromolecules such as proteins, DNA, RNA, and lipids, causing their structural and functional alterations [38][39]. Given that these macromolecules have important physiological functions, it is, therefore, not surprising that oxidative/nitrosative stress has been established as a major cause of human diseases, which include cardiovascular, organ disorders (pancreas, lungs, eyes, kidneys, and joints), neurodegenerative diseases, and even cancer [36][38].
In light of the above, it can be understood why anti-oxidant compounds are highly regarded as being beneficial for health. Indeed, anti-oxidants are molecules that, at low concentrations, inhibit or cause a significant delay in the oxidation of compounds [40], and as such, they help to hinder the negative effects of oxidative stress. Interestingly, reports on the anti-oxidant activities of polysaccharides from marine bacteria and fungi are not lacking, with some even involving novel species (e.g., Enterobacter cloacae MBB8) or novel polymers (e.g., EPSR4 from Bacillus subtilis) [41][42][43][44]. However, while this commonly studied activity of marine microbial EPS is now fairly established, the next step would undoubtedly be developing practical applications for such polymers. In this context, it is worth noting that providing anti-oxidants as supplements has been suggested as a means of mitigating the negative effects associated with oxidative stress [45]. Hence, the successful isolation of anti-oxidant EPS from two probiotic marine bacteria (Rhodotorula sp. and Pediococcus pentosaceus), as reported by Wang et al. [46] and Ayyash et al. [47], further highlights the potential of studying marine microorganisms for this purpose.

2.1.4. Drug Delivery

Besides their biological activities, microbial polysaccharides are also suitable to enhance the activities of other compounds, and for this purpose, they are often applied in the development of drug-delivery systems. Such nano-based or targeted delivery of therapeutic agents ensures that the latter are delivered at the required site and in a controlled manner, thereby overcoming the limitations (e.g., drug bioavailability, unwanted side effects, and non-specificity of drugs) that are encountered with current methods of drug delivery [48][49]. For this purpose, the selection of a suitable carrier molecule is a key parameter that needs to be considered, as its properties eventually influence the mechanism of drug release [50]. However, more importantly, the selected carrier would need to be biodegradable, biocompatible, and safe in order to be considered for such applications, and interestingly, microbial polysaccharides display such characteristics [50][51].
Dextran, composed of a linear chain of D-glucose linked by α-(1→6) bonds and commonly synthesized by lactic acid bacteria, is a widely used EPS for developing targeted delivery systems [52]. As a result of its non-toxicity, non-immunogenicity, and biocompatibility, dextran represents a suitable polymer for encapsulating or adsorbing therapeutic agents and ensuring their delivery while effectively providing protection against the immune system, as well as digestive enzymes [53]. The efficacy of such systems was demonstrated by Wang et al. and Fang et al., who developed dextran-based nanocarriers for the delivery of doxorubicin, with the results confirming the improved anticancer effects alongside reduced toxicity to the drug [54][55]. Similarly, chitosan (a derivative of chitin) and levan (a fructose homopolymer) also display properties such as biocompatibility, biodegradability, and low toxicity [56][57]. These features were further confirmed by studies whereby cisplatin, 5-fluorouracil, and resveratrol were successfully loaded onto those polysaccharides for delivery to cancer cells while being safe for healthy ones [58][59][60].
While there are reports on the production of the above polysaccharides from marine microorganisms (e.g., Penicillum spinulosum and Halomonas sp.) [61][62], it is surprising to note that such applications are yet to be established for those obtained from marine bacteria or fungi. This was reflected in an overview of two recent reviews on the application of marine microbial EPS as drug carriers, whereby the focus was largely, if not completely, on polysaccharides from non-marine sources [50][51]. However, the absence of a significant number of studies on the subject does not suggest that the potential of marine microbial polysaccharides has been overlooked. For instance, in an attempt to develop microgels as protein carriers, Zykwinska et al. successfully assembled EPSs from Vibrio diabolicus, a deep-sea hydrothermal bacterium, for the encapsulation of bovine serum albumin [63]. As a possible extension to that study, the authors subsequently isolated EPS from Alteromonas infernus to yield microcarriers that could encapsulate Transforming Growth Factor-β1 (TGF-β1) for applications in cartilage engineering [64]. Similarly, K1T-9, a 207 kDa heteropolysaccharide isolated from the novel marine bacterium Neorhizobium urealyticum, was successfully applied as an emulsifier for the encapsulation of astaxanthin [65]. Therefore, given the diversity and possibly unique properties of marine microbial polysaccharides, addressing the current research gap could potentially lay the foundations for the development of new or improved drug-delivery systems based on these polymers.

2.2. Bioremediation

Over the past few decades, industrialization and other human activities such as the improper disposal of wastes and the excessive use of pesticides and fertilizers have been a major cause of environmental pollution [66]. In particular, water contamination via heavy metals such as chromium (Cr), cadmium (Cd), lead (Pb), arsenic (As), mercury (Hg), and silver (Ag), just to name a few, has been of concern not only due to their non-biodegradability and toxicity at certain concentrations but also due to their potential accumulation along the food chain [67]. Therefore, the removal of heavy metal contaminants has been devised as an effective strategy for treating polluted areas, and in this context, electroplating, ion exchange, precipitation, and membrane processes represent some of the most commonly used approaches for this purpose [67][68]. However, these methods are not without drawbacks, the most important of which include the high cost involved, its low efficiency, and the production of toxic by-products [67]. As a result, attention has shifted to better alternatives, with microbial-based treatments proving to be a suitable candidate for such applications.
Indeed, microorganisms, especially those from heavy-metal-polluted areas, have evolved to develop tolerance to such pollutants, and therefore, they can be ideal candidates for bioremediation processes [69][70]. Microbial polysaccharides contain a number of functional groups such as carboxyl, hydroxyl, phosphate, amine, and uronic acids, with marine-derived ones being particularly rich in the latter [5][71]. These groups confer an overall negative charge to the polymers, thereby allowing them to bind to the positively charged heavy metals through the process of adsorption and subsequently leading to their removal [5]. For instance, a Bacillus cereus strain, isolated from a contaminated estuarine sediment, showed potential for water detoxification at concentrations of 25 to 150 mg/L due to its EPSs’ affinity for Pb, Cu, and Cd [67]. In this case, higher adsorption capacity, largely attributed to the functional groups present, occurred at the lower doses. Similarly, Concórdio-Reis et al. [72] reported the isolation of the EPS FucoPol from an Enterobacter species. This polymer, which showed specificity towards Pb, had an overall metal removal efficiency of 91.6–93.9% and this was achieved at a concentration of 5 g/L through its carboxyl and hydroxyl groups, under acidic conditions and within a temperature range of 5–40 °C. A different study further highlighted the potential of marine environments as a source of novel polysaccharides for bioremediation processes. Indeed, Zhang et al. [73] reported the ability of a novel polymer from an Alteromonas species to adsorb Cu, Ni, and Cr at a concentration of 1 g/L, thus indicating its suitability for the removal of heavy metals. However, despite its novel structure, the observed effects were still attributed to the functional groups present, especially O-H, C=O, and C-O-C, as is often the case for other microbial polysaccharides.
Closely related to the above are potential applications of marine microbial polysaccharides as bioflocculants. Flocculation refers to the aggregation of small suspended particles into larger flocs to aid their removal, and while it is not limited to heavy metals, it is nevertheless also applied to water treatment [74]. In this context, Chen et al. characterized a novel bioflocculant from the marine Alteromonas species [75]. Largely composed of polysaccharides, this polymer (20–220 mg/L) could effectively remove dyes such as Methylene Blue, Direct Black, and Congo Red at efficiencies between 72.3% and 98.5%, thus proving to be effective for the treatment of dyed wastewater. In a different study, a marine Bacillus species achieved 85% bioflocculant activity, with the optimum conditions for such activities also determined [74]. Overall, based on the above studies, it would not be unlikely that the huge diversity of marine microbial polysaccharides, as well as their specificity to pollutants, could drive the search for new polymers. At the same time, the fact that the presence of a polysaccharide backbone can enhance the thermal stability of bioflocculants could spark additional interest in the isolation of such polymers.
Although the above examples are not exhaustive, a key factor that explains the wide interest in polysaccharides is the remarkable structural diversity displayed by these polymers, as this translates into a wide range of properties, as well as potential applications. Thus, any prospective uses of polysaccharides are often dependent on structural characteristics such as the monosaccharide composition, the type of functional groups present, or even the conformation, including the degree of branching and the type of linkage [76]. For instance, the presence of neutral monosaccharides (e.g., glucose, mannose, fucose, arabinose, D-galactose, and glucuronic acid) has been reported as being more likely to induce anti-oxidant activities [34], while in their study on polysaccharides from Lactobacillus reuteri, Chen et al. [77] noted that the amount of galactose was related to the anti-inflammatory activity of the polymer, with higher amounts of the monosaccharide enhancing the biological activity. Similarly, in terms of conformations, the types of glycosidic linkages may affect the solubility and flexibility of polysaccharide chains, thus making them more or less suited to certain specific applications [25][34]. In other cases, polymers with mostly β-1,3-linkages were also reported as displaying greater antitumor activities in contrast to those containing mostly β-1,6- linkages [25]. Finally, as far as functional groups are concerned, biological activities are often observed when specific groups are present. For example, phosphate groups can contribute to the immunomodulatory effects of polysaccharides by improving their affinity to immune cells. In addition, compared with neutral polysaccharides, phosphorylated ones are also more likely to inhibit the growth of certain cancer cells [78][79]. Similarly, sulfated or acetylated polysaccharides can display better biological activities than non-sulfated ones, especially antibacterial, anti-oxidant, and antitumor effects [78][80][81].

This entry is adapted from the peer-reviewed paper 10.3390/md21070420

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