Marine algae – A potential source of natural antimicrobial agents and nanofiber production for food preservationDuraiarasan Surendhiran, Haiying Cui, Lin Lin*School of Food and Biological Engineering, Jiangsu University, Zhenjiang 212013, China*To whom corresponding should be addressed:Prof. Dr.
Lin Lin,School of Food and Biological Engineering, Jiangsu University, Zhenjiang 212013, ChinaE-mail: [email protected] version of title: Production of Bioactive compounds and Nanofibers from Marine AlgaeChoice of journal/section Comprehensive Reviews in Food Science and Food SafetyReviews and trendsABSTRACT: Currently, controlling food pathogens and food spoilage is practiced by addition of synthetic chemicals in many food industries worldwide. Meanwhile, artificial food preservatives cause detrimental effects on consumers because of their toxic nature. Due to awareness of the consumers and harmful effects of synthetic food preservatives, research has moved towards finding alternative and safe antimicrobial agents from natural substances.
Marine algae proved to be a rich source of many novel unique antimicrobial compounds which could ultimately replace synthetic chemicals in food applications. Moreover, marine algae are the most plentiful creatures in the marine environment that serve as the unlimited renewable source of biopolymers which could be used to fabricate nanofibers which could deliver natural antimicrobial agents in the packing material. This review highlights the diverse bioactive compounds of marine algae and their mode of action on bacterial food pathogens and their advantages. Also, an overview of different biopolymers of marine algae, their potential application in nanofibers synthesis and their current applications in food technology are also assessed in this article.Keywords: marine algae, electrospinning, nanofibers, food pathogen, biopolymers IntroductionIn the modern world, consumption of packaged foods by people has been increased day by day.
However, the most significant hurdle of the food industry is the limited shelf life of packaged food products due to contamination by food spoiling pathogens which results in a global public health issue, trade, and the economy. Given access to improper food preservation, bacteria and fungi rapidly colonize, increase in population leading to food spoilage (Hammond et al., 2015). The World Health Organization reported that unsafe food resulted in the illnesses of at least 2 billion people worldwide annually and could be deadly (Sharif, Mustapha, Mohd.Yusof, & Zaki, 2017). Addition of synthetic antimicrobial agents effectively controls the growth of food contaminants and extends the shelf life of foods (Irkin & Esmer, 2015). Recent toxicological studies indicated that specific concentrations of synthetic preservatives and their continuous use might potentially be mutagenic and genotoxic.
For example, Sales et al (2018) recently proved that artificial synthetic additives induced the formation of micronuclei in the bone marrow erythrocytes and believed as cytotoxic and genotoxic in the animal study. This apprehension led the consumers for demand of additional natural preservatives that might be nontoxic and proved to be excellent defence against microbial attack (Gyawali & Ibrahim, 2014; Brandelli &Taylor, 2015; Piran, Kafil, Ghanbarzadeh, Safdari, & Hamishehkar, 2017). Therefore, search for new alternatives to preserve foods is of great interest in the food industry.
Natural antimicrobials attracted considerable attention in the food industry because these substances would not cause any toxic or undesirable effect on the consumers (Brandelli & Taylor, 2015; Wang et al., 2018). Natural bioactive compounds from many plants, bacteria and animal sources for food application have been extensively studied by various researchers and reported the possibility of commercial use. However, each source has own disadvantages bottlenecking 100% usage for commercial purposes.
Most of the essential oils from plants show instability (Moghimipour, Aghel, Mahmoudabadi, Ramezani, & Handali, 2012) and very less effect against gram-negative bacteria (Tiwari et al., 2009; Naik, Fomda, Jaykumar, & Bhat, 2010; Nazzaro, Martino, Coppola, & Feo, 2013). Moreover, overuse of bacteriocins can lead to resistant pathogens (Cavera, Arthur, Kashtanov, & Chikindas, 2015) and loss in their activity by proteolytic enzymes (Bradshaw, 2003; Fahim, Khairalla, & El-Gendy, 2016). Some of the animal sourced antimicrobial peptides like lysozyme and pleurocidin did not show strong effects on gram-negative bacteria (Aloui & Khwaldia, 2016) and was inhibited by magnesium and calcium in foods limiting the use (Tiwari et al., 2009). There is an urgent need of using new and alternative compound against the above mentioned antimicrobial agents.
In the recent years, seaweeds have been recognized as one of the wealthiest and the most unexplored new source of antimicrobial compounds and nanofibers for therapeutics and food preservation. This review focused on various antimicrobial compounds extracted from marine algae, their biochemical compositions and antimicrobial activities against food pathogens. Also, this article pivots the potential use of marine algae for nanofiber synthesis used for incorporating antimicrobial agents for greater delivery and stability during food preservation.
Natural antimicrobial compounds from marine algaeOver the last few years marine algae has attracted many researchers worldwide to isolate high value bioactive compounds for food and pharmaceutical industries due to its broad spectrum of various biological activities such as antioxidant, antibacterial, antifungal, anticancer, anti-inflammatory and antidiabetic (Thomas & Kim, 2011; Eom, Kim, & Kim, 2012; Hamed, Ozogul, Ozogul, & Regenstein, 2015; El Shafay, Ali, & El-Sheekh, 2016; Sathya, Kanaga, Sankar, & Jeeva, 2017; Davoodbasha, Edachery, Nooruddin, Lee, & Kim, 2018). Algae are the fastest growing plants in the world and generally divided into macroalgae and microalgae based on morphology. The macroalgae or “seaweeds,” are more abundant, multicellular plants growing up to 60 meters long in ocean.
Microalgae are microscopic, mostly existing as small cells of about 2–200 µm and dwell in fresh, sea and even wastewater systems (Sirajunnisa & Surendhiran, 2016). Generally, marine algae are categorized into three main groups namely Rhodophyceae (red algae), Chlorophyceae (green algae), Phaeophyceae (brown algae) for the attribution of different pigments like phycobilins, chlorophyll and fucoxanthin respectively (Kadam, Tiwari, & O’Donnell, 2013; Barbosa, Valentão, ; Andrade, 2014). Asian countries like China, Japan, and Korea used seaweeds for medicinal and food purposes since prehistoric times (Thomas ; Kim, 2011). Many research reports revealed that marine algae could act as a potential alternative source of antimicrobial agents because of their functional groups with excellent antibacterial activity include phlorotannins, fatty acids, polysaccharides, peptides, terpenes, polyacetylenes, sterols, indole alkaloids, aromatic organic acids, shikimic acid, polyketides, hydroquinones, alcohols, aldehydes, ketones, and halogenated furanones, alkanes, and alkenes (Barbosa et al.
, 2014; Shannon ; Abu-Ghannam, 2016; Sathya et al., 2017; Pina-Pérez, Rivas, Martínez, ; Rodrigo, 2017; Zouaoui ; Ghalem, 2017). Screening for under exploited bioactive compounds from marine algae with antimicrobial properties to be employed in food applications.
Hence, the research has moved towards finding natural antimicrobial compounds against food pathogens to replace synthetic compounds. Various primary bioactive compounds from marine algae are shown in Fig.1. Antimicrobial agents from terrestrial plants such as spices and herbs and their antimicrobial activity against food pathogens have already been well documented in literature. There are more than 100,000 species of algae existing on earth (Sirajunnisa ; Surendhiran, 2016). However, information about their potential activity against food pathogens is sparse since it is a recent field of research worldwide. Recently, some research reports have been published on antimicrobial potential of bioactive compounds extracted from marine algae against food pathogens and obtained notable positive results by various researchers globally.
For instance, Rajauria et al. (2012) reported that methanol extract of polyphenolic compounds from the Irish brown seaweed Himanthalia elongates showed potent bactericidal activity against Gram-positive Listeria monocytogenes and Enterococcus faecalis and Gram-negative Pseudomonas aeruginosa and Salmonella abony at a concentration of 60 mg/mL. Dussault et al. (2016) reported that low concentrated algal extracts (?500 µg/ml) from Padina and Ulva sp. showed potential antimicrobial activity against Gram-positive foodborne pathogens such as Listeria monocytogenes, Bacillus cereus, and Staphylococcus aureus. A summary of antimicrobial agents from marine algae and their antimicrobial activities against food pathogens is shown in Table 1.Polysaccharides.
Marine algae contain many different kinds of polysaccharides as their storage compounds and show good antibacterial, antiviral and antioxidant properties. Many of them are soluble dietary fibers (Chojnacka, Saeid, Witkowska ; Tuhy, 2012) and could be converted into nontoxic bioactive oligosaccharides by simple hydrolysis (Pina-Pérez et al. 2017). For example, sulphated polysaccharides from seaweed, Chaetomorpha aerea containing alginates, fucoidans and laminaran showed potent antimicrobial activity against food pathogens, E. coli and Staphylococcus aureus, at an MIC of 50 mg/mL of extract (De Jesus Raposo, de Morais, ; de Morais, 2015). Kadam et al. (2015) recorded the remarkable effect of ultrasound assisted extraction of laminarin from two Irish brown seaweeds Ascophyllum nodosum and Laminaria hyperborean against essential food pathogens such as Staphylococcus aureus, Listeria monocytogenes, Escherichia coli, and Salmonella typhimurium.
Another report published by Pierre et al. (2011) that carrageenans and the sulphated exopolysaccharide from the red microalga Porphyridium cruentum are effectively inhibiting one of the most important foodborne pathogen, Salmonella enteritidis. Treating Helicobacter pylori, one of the most dangerous foodborne pathogen responsible for gastric ulcer, is a big challenge till now affecting 50–80% of the worldwide population (Pina-Pérez et al., 2017). Chua et al.
(2015) successfully inhibited the growth ` of H.pylori using sulphated polysaccharide fucoidan isolated from edible brown alga, Fucus vesiculosus, at the concentration of 100 µg /mL. Moreover, Araya et al. (2011) demonstrated that fucoidan showed no toxic effects on human trials with the daily intake of 6g which revealed the possibilities of applying in food industries. Phenolic compounds.
Phenolic compounds also known as Polyphenols are a group of tannin compounds that contain hydroxyl (?OH) substituents on an aromatic hydrocarbon moiety. Polyphenols in marine algae include phenolic acids, flavonoids, isoflavones, cinnamic acid, benzoic acid, quercetin, lignans, catechins, anthraquinones, phlorotannins (Chojnacka et al., 2012; Kadam et al.
, 2013; Pina-Pérez et al., 2017). Among various polyphenols, phlorotannins showed excellent, potent free radical scavenging properties than polyphenols derived from terrestrial plants due to eight interconnected phenol rings (Sathya et al., 2017). Phlorotannins found in many brown seaweeds such as Ecklonia cava, E.
kurome, E. stolonifera, Eisenia aborea, Eis. bicyclis, Ishige okamurae and Pelvetia siliquosa have medicinal and pharmaceutical benefits and have shown strong anti-oxidant, antiinflammatory, antiviral, anti-tumor, anti-diabetes and anti-cancer properties (Eom et al., 2012). Phlorotannins are polymers of phloroglucinol units (1,3,5-trihydroxybenzene) with molecular weight ranging between 126 Da and 650 kDa (Kadam et al., 2013).
In recent studies it was described that phlorotannin had excellent antimicrobial activity against food pathogens which could help devise a roadmap to replace synthetic chemicals for food preservation. A research group led by Kim et al. (2017) investigated that antimicrobial activity of phlorotannin extracted from edible brown seaweed, Eisenia bicyclis acted against Listeria monocytogenes, one of the essential food contaminants in the meat processing industry. They evidenced that phlorotannins had excellent anti-listerial activity in the range between 16 and 256 µg/ml. Choi et al. (2010) recorded the potent antimicrobial activity of eckol rich phlorotannin from E.
cava against food pathogens methicillin-resistant S. aureus (MRSA) and Salmonella sp. in the range between 125 and 250 µg/mL.
Moreover, some research results concluded that phlorotannin showed no cytotoxic effects on animal models with oral administration (Nagayama, Iwamura, Shibata, Hirayama, ; Nakamura, 2002; Eom et al., 2012) which is highly suitable for food applications. A team led by Al-Saif et al.
(2014), investigated the effects of flavonoids including rutin, quercetin, and kaempferol extracted from marine alga G.dendroides. They recorded the antibacterial activity of these compounds against some critical food contaminants such as E. coli, S. aureus and E.
faecalis at the concentration of 10.5 mg/kg (rutin), 7.5 mg/kg (quercetin) and 15.
2 mg/kg (kaempferol). Besides, marine algae can be directly added into human foods such as breads, pizza, cheese, pasta and meat products (Pina-Pérez et al., 2017) and used for edible coatings to preserve food products (Sánchez-Ortega et al., 2014; Pina-Pérez et al., 2017) which would add additional benefits of using marine algae in food industries. Proteins and peptides.
Many short chain and long chain peptide and proteins had been isolated from marine algae, and their antimicrobial activities had been exposed by many recent publications (Shannon ; Abu-Ghannam, 2016). Crude extract from marine algae that contained high amount of proteins showed higher antimicrobial potency (Al-Saif et al., 2014). When compared to larger peptides small chain peptides have more potent antimicrobial property due to their simple molecular structure (Pina-Pérez et al., 2017) aiding in effortless invasion of the bacterial cell wall. Beaulieu et al.
(2015) reported that antibacterial peptides extracted from Saccharina longicruris, a brown seaweed showed a noticeable inhibiting activity against Staphylococcus aureus with concentrations ranging between 0.31 mg/mL and 2.5 mg/mL. Recently, a carbohydrate-recognizing protein called lectin has been recognized as potential antimicrobial agents isolated from many biological sources including marine algae (Pina-Pérez et al., 2017).
The possible antimicrobial activity of lectin isolated from red alga Solieria filiformis and its antimicrobial activity had been evaluated by Holanda et al. (2005). They found that the isolated lectin acted against both Gram-positive and negative bacterial species such as Pseudomonas aeruginosa, Enterobacter aerogenes, Serratia marcescens, Salmonella typhi, Klebsiella pneumoniae and Proteus sp. at the concentration of 1000 µg/mL. Smith, Desbois, ; Dyrynda (2010) also reported the antimicrobial potential of lectins extracted from red algae, namely Eucheuma serra and Galaxaura marginata hindering the growth of Vibrio vulnificus and V.
pelagicus.Fatty acids. Apart from secondary metabolites, some of the fatty acid molecules present in marine algae also have potent antimicrobial properties which are commendably documented in literature. For example, Cakmak, Kaya, ; Asan-Ozusaglam (2014) tested that fatty acids extracted from marine microalga D. salina showed noticeable growth inhibition against Listeria monocytogenes ATCC 7644 at a concentration of 5 mg/mL and revealed that this activity was due to the presence of valuable fatty acid molecules like ?-3 and ?-6. In another study conducted by Desbois, Lebl, Yan, ; Smith (2008) observed that fatty acids from the diatom Phaeodactylum tricornutum demonstrated a very potent antibacterial activity against MRSA and had characterized three different polyunsaturated fatty acids which involved in the antibacterial activity such as eicosapentaenoic acid (EPA), monounsaturated fatty acid (MUFA) and palmitoleic acid (PA). The fatty acids profile in algae, with a predominance of myristic, palmitic, oleic and eicosapentaenoic acids (EPA), is a specific feature associated with the antimicrobial potential of algal species (Pina-Pérez et al.
2017). Furthermore, palmitic acid had been assumed to be primarily responsible for the antibacterial activity of algae (Al-Saif et al., 2014; Pina-Pérez et al. 2017). However, in our previous study, the results demonstrated that fatty acid methyl esters produced from marine microalgae Nannochloropsis oculata showed higher antimicrobial efficacy on gram-negative bacteria than the gram-positive one (Surendhiran et al., 2014). This finding was in agreement with the statement given by Mubarak Ali et al.
(2012) that the action of fatty acid methyl esters was not limited to the cell wall variations. Fatty acids are made up of carboxylic acid (an acid with a -COOH group) with long hydrocarbon side chains that creates hydrophobicity and quickly pass through a lipid bilayer of bacterial cell membrane resulted in cell lysis due to leakage of cytoplasm (Burt, 2004; Oussalah, Caillet, ; Lacroix, 2006; Dussault et al., 2016). Terpenes and lactones.
Terpenoids are dominant group of secondary metabolites found in many marine algal species and displayed potential biological activity including antibacterial and antiviral properties (Bajpai, 2016). Abad, Bedoya, ; Bermejo (2011) elucidated that sesterterpenoids, sesquiterpenoids, and meroterpenoids are the primary compounds of terpenoids which are responsible for antimicrobial properties. The highest antimicrobial potential of algae extracts against S.aureus was reported by Tüney, Çadirci, Ünal, ; Sukatar (2006), who observed a zone of inhibition ; 50 mm by diethyl ether extract (0.5 g/mL) of Enteromorpha linza (0.
5 g/mL) and 38 mm inhibition zone in the case of Ulva rigida. It is due to that the most effective antimicrobial compounds found in these algal species are terpenes, (e.g.
, usneoidone E, zosterdiol A, zosterdiol B, zosteronol, and zosteronediol) responsible for the antimicrobial and antiviral activity attributed to them (Pina-Pérez et al., 2017). Xu et al. (2003) conducted experiments on tetracyclic brominated diterpenes isolated from the organic extract of Sphaerococcus coronopifolius collected from the rocky coasts of Corfu Island that showed MIC value of 16 and 128 ?g/mL against MRSA S.aureus. According to Etahiri, Bultel-Poncé, Caux, ; Guyot (2001), two bromoditerpenes, 12 S-hydroxybromospha-erodiol, and bromosphaerone, isolated from red seaweed and Sphaerococcus coronopifolius showed antibacterial activity against S.
aureus with a minimal inhibitory concentration of 0.104 and 0.146 ?mol/L, respectively. Besides, bioactive compounds from marine algae showed excellent antimicrobial efficacy against fungal food contaminants as well.
It was evidenced by Indira et al. (2013) that seaweed Halimeda tuna extracts using various solvents like ethanol, methanol, and chloroform hindered the growth of A. niger, A. flavus, A. alternaria, C. albicans and E. floccosum at the concentration ranging between 250 and 500 mg/mL.
Bromophycolides (diterpene-benzoate macrolides) extracted from red alga Callophycus serratus showed significant growth inhibition of methicillin-resistant S.aureus and vancomycin-resistant Enterococcus faecium (Lane et al., 2009). Recently, Rodrigues et al. (2015) isolated sphaerane bromoditerpenes, an uncommon dactylomelane called sphaerodactylomelol, from the red alga Sphaerococcus coronopifolius using dichloromethane solvent and observed efficient growth inhibition against bacteria Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus and yeast Candida albicans. Furanones, cyclic esters of lactones extracted from red seaweed Delisea pulchra has been reported on inhibition of growth of Pseudomonas aeruginosa and E.coli by damaging their biofilm formation (Ren, Bedzyk, Ye, Thomas, ; Wood, 2004; Shannon ; Abu-Ghannam, 2016).
Mechanism of action of marine algal bioactive compounds on bacteriaAntimicrobial mechanism of action of marine algal compounds remains unclear still, and only limited information has been specified by some researchers. Different concepts have been proposed by some investigators. Most of the studies depicted that cell wall and cell membrane damage are primary targets of marine algal antimicrobial compounds (Wang, Xu, Bach, ; McAllister, 2009; Smith, Desbois, ; Dyrynda, 2010; Guedes, Barbosa, Amaro, Pereira, ; Malcata, 2011; Hierholtzer, Chatellard, Kierans, Akunna, ; Collier, 2012; Wei et al., 2016; Falaise et al., 2016). Mechanism of action of different natural antimicrobial compounds from marine algae on bacteria is shown in Fig.2.
Antibacterial mechanism of the marine algal polysaccharide is due to glycoprotein-receptors present on the cell-surface of polysaccharides which binds with compounds in the bacterial cell wall, cytoplasmic membrane, and DNA. This action resulted in increased permeability of the cytoplasmic membrane, protein leakage and damaging of bacterial DNA finally leading to cell death (He, Yang, Yang, ; Yu, 2010; Pierre et al., 2011; Shannon and Abu-Ghannam, 2016). An important mechanism was proposed by Shannon and Abu-Ghannam (2016) that the marine algal fatty acids target essential metabolic pathways in the bacterial cell, i.e.
, electron transport chain (ECP) and oxidative phosphorylation, which take place in cell membranes. These resulted in damages of adenosine triphosphate (ATP) energy transfer and hindered enzymes such as bacterial enoyl-acyl carrier protein reductase, essential for the production of fatty acids within the bacterial cell. Another report claimed by Guedes et al.
(2011) that the possible mechanism of action of fatty acids in cell leakage due to morphological damages of the outer cell membrane. It was corroborated by the recent research findings of El Shafay, Ali, Mostafa, ; El-Sheekh (2016). They elucidated the mechanisms of action of fatty acids extracted from seaweeds, Sargassum vulgare and S. fusiforme on gram-positive bacteria Staphylococcus aureus and gram-negative Klebsiella pneumoniae using Transmission electron microscopy (TEM).
The results showed that shrunken, ruptured and distorted shape of bacteria cells were observed due to puncture of the cell wall. Not all the marine algal bioactive compounds demonstrate potent effects on all groups of bacteria. It depends on algal species, the efficiency of the extraction method and concentration of the compositions present in the extracts. For example, diethyl ether extract of red seaweed S. fusiforme showed high activity against gram-positive bacteria S.
aureus; however, the methanol extract of same marine algae showed higher inhibition activity against gram-negative bacteria P.aeruginosa (El Shafay et al., 2016). Another example, the phycobiliproteins, and exopolysaccharides from the red microalgae Porphyridium aerugineum and Rhodella reticulata respectively were active against gram-positive bacteria S.aureus and Streptococcus pyogenes but presented no effect against the gram-negative bacteria E.
coli and Pseudomonas aeruginosa (Najdenski et al., 2013). The difference in sensitivities between bacteria may be due to their complex membrane permeability, making the penetration and the bactericidal action of the compound more difficult. Lane et al. (2009) suggested that the mechanism of antibacterial activity of terpene compounds was due to the hydrophobicity and conformational rigidity of the tetrahydropyran structure.Wang, Xu, Bach, ; McAllister (2009) accounted that mechanisms of action of phlorotannin were also similar to fatty acids documented by Shannon and Abu-Ghannam (2016). Moreover, they added that phloroglucinol units of phlorotannin contain Phenolic aromatic rings and hydroxyl group that makes the hydrogen bond with the amine group of bacterial proteins that cause cell lysis.
It was further evidenced by Wei et al. (2016) that phlorotannin extracted from S.thunbergii injured the cell membrane of V.parahaemolyticus, leads to cytoplasm outflow and disassembly of cell inclusions.
However, a higher amount of phloroglucinol is required to destroy Gram-negative bacteria than the Gram-positive due to the multifaceted structure of former than the latter (Kamei ; Isnansetyo, 2003). It was corroborated by the previous research reports of Hierholtzer et al. (2012). In their report, a mechanism of action of phlorotannin was directly evidenced by electron microscope images showing total cell membrane damages of bacterial cells. Paiva et al. (2010) explained that the antibacterial activity of lectins is due to the binding and damages of cell wall compositions of bacteria such as teichoic acids, peptidoglycans, and lipopolysaccharides and destroy them by leaking cell inclusions. However, more research findings must be required, and various advanced techniques such as molecular techniques, protein, enzyme and DNA analysis and scanning and transmission electron microscope analysis should be carried out to support the direct evidence of the mechanism of action of bioactive compounds isolated from marine algae.
Application of nanofibers in food preservationNatural bioactive compounds show ideal antimicrobial properties, too desired to be used in food preservation. Nonetheless, there is also a need for an efficient method for their delivery into foods (Balasubramanian, Rosenberg, Yam, ; Chikindas, 2009). Nowadays nanotechnology has become the call of the century. It has a thriving application in several other sectors, and its application in the food industry has been a recent event (Pradhan et al., 2015). Many nanotechniques including nanoemulsions, nanoliposomes, and nanoencapsulation using nanofibers are employed in food preservation to incorporate natural antimicrobial agents with different supportive materials.
Among various nanodelivery systems, nanofibers have more advantages than other methods due to its rapid, controlled release, high surface to volume ratios and show higher antimicrobial activity and stability than other nanomaterials. These assets create the mats composed of electrospun fibers outstanding candidates for immobilization of natural antimicrobial compounds in food applications globally. Many different methods such as phase separation, self-assembly, drawing, and electrospinning can be used to produce nanofibers (Esentürk, Erdal, ; Güngör, 2016; Akhgari, Shakib, Sanati et al., 2017) and chemical method (Saurabh et al., 2016; Berglund, Noël, Aitomäki, Öman, ; Oksman, 2016; Martelli-Tosi et al.
, 2016; Xie et al., 2016). Among the other nanofiber production, electrospinning is the most cost-effective one with simple tooling, and is applied to produce ultrafine fibers with a simple step-up production for the encapsulation of various bioactive compounds (Esentürk et al.
, 2016; Wen, Wen, Zong, Linhardt, ; Wu, 2017). Recently, the electrospun nanofibers have drawn significant interest to the food industry because of their high surface area-to-volume ratios. This property makes electrospun fibers potential materials for various applications, like edible films and additive delivery systems (Padilla, Soto, Iturriaga, ; Mendoza, 2014).
Electrospi nning The working principle of electrospinning is to use electrostatic repulsion of charged polymer jets to generate arbitrarily oriented or united nanofibers on the exterior of the collector. In general, electrospinning set up consist two electrodes; one is attached with polymer mixer and second one associated to a collector. Electrically charged polymers produce a Taylor cone at the end of the needle and are evicted at a positive charge. Nanofibers are generated after the evaporation of solvents while the mixer of polymer solution goes faster towards rotary collector or an auxiliary electrical field (Brandelli ; Taylor, 2015). Electrospinning is widely accepted and superior method for production of nanofibers, owing to its ease, less cost, good elasticity, the potential to massive scale production, the capability to produce nanofibers from most of polymers (Esentürk et al., 2016; Wen et al., 2017). Furthermore, both hydrophobic and hydrophilic compounds such as protein and amino acids could be directly encapsulated on nanofibers by electrospinning technique (Wen et al., 2017). Also, immense stability and high encapsulation efficiency of natural antimicrobial agents could be achieved by this method (Yang et al., 2017). Moreover, heat sensitive bioactive compounds could be efficiently immobilized in nanofibers during electrospinning method since it operates at ambient environment when compared to conventional techniques like spray drying which runs at high temperature (Wen et al., 2017). Basic electrospinning set up is illustrated in Fig.3.Efficient nanofiber formation and its physicochemical properties such as mechanical strength, structure, release features of drug including burst effect and biocompatibility are influenced by the selection of polymers to electrospun because that would impact the interactions of the mixer of bioactive compounds/polymer/solvent (Esentürk et al., 2016). Nowadays, considerable attention has been given to natural biopolymers due to their remarkable advantages including biocompatibility, biodegradability, renewability, and sustainability as carriers for encapsulation of bioactive compounds in the food industry (Sa?, Morshed, Ravandi, ; Ghiaci 2007; Wen et al., 2017). Many researchers have been successfully synthesized nanofibers using electrospinning from biopolymers such as cellulose acetate (Dods, Hardick, Stevens, Bracewell, 2015; Mehrabi, Shamspur, Mostafavi, Saljooqi, ; Fathirad, 2017; Liakos, Holban, Carzino, Lauciello, ; Grumezescu, 2017), chitosan (Tripathi, Mehrotra, ; Dutta, 2009; Liu, Wang, ; Lan, 2018), gelatin (Agudelo et al., 2018), dextran (Fathi, Nasrabadi, ; Varshosaz, 2017), pullulan (Liu, Li, Tomasula, Sousa, ; Liu, 2016; Wen et al., 2017), pectin (Liu et al., 2016), hyaluronic acid (Zhao et al., 2016; Wen et al., 2017), collagen and silk fibroin (Zhao et al., 2016). The basic concept of immobilization and delivery of natural antimicrobial agents through nanofibers for food preservation is represented in Fig. 4. Marine algae as potential source of nanofibersNowadays, much research have been focused on marine algae as a source of potential biopolymer for large-scale production of nanofibers as they are ubiquitous and abundant in nature and easy to harvest. Moreover, marine algal biopolymers such as sodium alginate, agar, fucoidan, and carrageenans fall under GRAS category recognized by FDA (Tavassoli-Kafrani, Shekarchizadeh, ; Masoudpour-Behabadi, 2016). Some researchers have successfully synthesized nanofibers from different kinds of marine algal biopolymers by electrospun methods such as alginate (Saquing et al., 2013; Hu, Gong, ; Zhou, 2015; Wongkanya et al., 2017), ulvan (Kikionis, Ioannou, Toskas, ; Roussis, 2015), agar and agarose (Sadrearhami, Morshed, ; Varshosaz, 2015; Cho, Singu, Na, ; Yoon, 2016), fucoidan (Jang, Hong, Jung Ro ; Yoon, 2015; Zhang et al., 2017) and carrageenan (Basilia, Robles, Ledda, ; Dagbay, 2008; Tort ; Acartürk, 2016; Goonoo et al., 2017). In aqueous solution whole biopolymers alone cannot be fabricated by electrospinning due to their poor mechanical properties and processing. Therefore, some synthetic polymers have to be added with biopolymers as blending agents to form strong intermolecular hydrogen bond which helps easy spinning of nanofibers (Safi et al., 2007; Saquing et al., 2013; Zhao et al., 2016). Many synthetic, semisynthetic and natural polymers have been applied for production of electrospun nanofibers. Synthetic polymers and copolymers such as poly (lactic acid) (PLA), poly (lactic-co-glycolic acid) (PLGA), poly(?-caprolactone) (PCL), poly(vinyl pyrrolidone) (PVP) and poly(ethyleneoxide) (PEO) have been used to produce Nanofibers (Brandelli ; Taylor, 2015; Akhgari, Shakib, ; Sanati, 2017; Wen et al., 2017). Various marine algal biopolymers blended with synthetic polymers for nanofibers synthesis is shown in Table 2. Sodium alginate. Alginates or sodium alginate (SA) or algins are biopolymer composed of two different linear copolymers such as uronic acids, ?-D-mannuronic acid (M) and ?-L-guluronic acid (G) linked in position 1?4. The salt forms (alginates), with several cations (Na+, K+, Mg2+ and Ca2+), are the significant components of brown seaweed cell walls and also of the intracellular matrix (Fathi et al., 2014; Pérez, Falqué, ; Domínguez, 2016; Abdul Khalil et al., 2017). It is hydrophilic in nature with the molecular weight of alginate ranging between 500 and 1000 kDa (Pérez et al., 2016). Due to its biocompatibility, biodegradability, nontoxicity and low cost, sodium alginate has been well recognized for nanofibers synthesis in food application. Alginate is distinct from chitosan due to its high solubility in water (Zhao et al., 2016) which is an additional advantage to be used in electrospinning to produce nanofibers mats. In general, sodium alginate is composed of three different types of regions such as G, M and MG distributed in different extent in the polymeric chain which determine the physical properties of alginate. The gelling property of alginate is mainly decided by G region which are composed of L-glucuronic acids and M regions entirely composed of D-mannuronic acid. MG regions consist of both M and G which determine the dissolving property of alginate in many solvents (Tavassoli-Kafrani et al., 2016). Sodium alginate makes strong bond with multivalent cations particularly calcium ions by producing hard gel which is the exclusive property of alginate (Tavassoli-Kafrani et al., 2016; Abdul Khalil et al., 2017). Therefore, SA is highly suitable for making nanofibers mat because most of the cross-linking of biopolymers depends on calcium ions which strengthens the nanofibers. Sodium alginate is the most studied biopolymer for electrospinning among other biopolymers from marine algae. Saquing et al. (2013) produced alginate nanofibers blend with synthetic polymer Polyethylene Oxide (PEO) by electrospinning method. Hajiali et al. (2015) fabricated sodium alginate nanofibers containing lavender oil by the electrospinning method and demonstrated potential growth inhibition using bioactive nanofibers against S.aureus. Citric acid cross-linked sodium alginate/PVA electrospun nanofibers were prepared by a team of Stone, Gosavi, Athauda, ; Ozer (2013). They used a homogeneous blend of sodium alginate-polyvinyl alcohol (1:1 weight ratio) containing cross-linking agent citric acid (5 wt%) for electrospinning and found that cross-linked nanofibers were more heat stable and water-insoluble even after two days of immersion in water than the non-cross linked electrospun nanofibers which dissolved immediately. Recently Rafiq, Hussain, Abid, Nazir, ; Masood. (2018) successfully immobilized some essential oils (EOs) such as cinnamon, clove, and lavender on electrospun nanofibers synthesized from alginate and polyvinyl alcohol (PVA) blend and evaluated antimicrobial activity against S. aureus. The results showed that all EOs displayed good antimicrobial activity and the FTIR study confirmed the successful incorporation of essential oils in nanofibers.Carrageenan. Carrageenan is a sulfated water-soluble polysaccharide present in red algae, which consists of a linear sequence of other residues forming (AB)n sequence, where A and B are units of galactose residues. They are linked by alternating ?-(1?3) (unit A) and ?-(1?4) (unit B) glycosidic bonds. Carrageenans are polyanions due to the presence of sulfated groups (Cardoso, Costa, ; Mano, 2016). Carrageenans are classified into three groups based on degree of sulfation: as kappa (?) which contain 4-sulfated galactose and a 4-linked 3,6-anhydrogalactose, iota (?) is like kappa but with addition of sulfate ester group on C-2 of the 3,6-anhydrogalactose residue and lambda (?) containing 2-sulfated, 3-linked galactose unit, and a 2,6-disulfated 4-linked galactose unit (Tavassoli-Kafrani et al., 2016). Generally, carrageenan is extracted from marine algal species including Kappaphycus alvarezii, Eucheuma denticulatum, Hypnea musciformis, Lamoroux and Solieria filiformis (Tavassoli-Kafrani et al., 2016; Cardoso et al., 2016)Carrageenan is widely used as a functional ingredient in many food industries for various purposes (Tavassoli-Kafrani et al., 2016; Abdul Khalil et al., 2017). These three different carrageenan exhibit distinct gelation properties to each other. i.e., ? -carrageenan produce rigid and brittle gels, ?-carrageenan produces softer, elastic and cohesive gels and ? -carrageenan doesn’t form gels. This is due to the presence of different sulphate groups and anhydro bridges in carrageenan (Abdul Khalil et al., 2017). Some authors pointed out that carrageenans have biological properties such as anticoagulant, antitumor, immunomodulatory, anti-hyperlipidemic and antioxidant activities. They also have protective action against bacteria, fungi and some viruses (Silva et al., 2010; Zhou et al., 2004; Panlasigui, Baello, Dimatangal, & Dumelod, 2003; De Souza et al., 2007).Basilia et al. (2008) produced polycaprolactone/carrageenan nanofibers by the electrospinning method and studied in vitro and in vivo for tissue engineering applications. Carter (2016) successfully encapsulated two essential oils such as carvacrol and eugenol in nanofibers synthesized from iota-carrageenan and tested against food pathogens L.monocytogenes and L.innocua. His results elucidated that carrageenan nanofiber encapsulated essential oils effectively inhibited the growth of tested food pathogens and potential release characteristic features. Another team led by Goonoo (2017), have reported the possibilities of producing nanofibers from mixed components of biodegradable polyhydroxybutyrate (PHB) or polyhydroxybutyrate valerate (PHBV) with the anionic sulfated polysaccharide ?-carrageenan (?-CG) by electrospinning method. Carrageenans make strong bonds with polycations compounds (Eg. chitosan), thus, applying organic solvents and toxic cross-linkers can be avoided during nanofibers synthesis (Cardoso et al., 2016). It is an added advantage to using carrageenans for nanofibers synthesis by electrospinning technique.Ulvan. Ulvan is a complex, water-soluble sulfated anionic polysaccharide obtained from cell wall matrix of the members of green algae, Ulvales (Chlorophyta) (Toskas et al., 2011). The name ulvan is derived from the original terms ulvin and ulvacin which usually are extracted by the process of hydrolysis at around 80-90°C using divalent cation chelator such as ammonium oxalate (Lahaye & Robic, 2007). Generally, ulvan are extracted from following species such as Ulva pertusa, Ulva lactuca, Ulva clathrata, Ulva compressa, Ulva conglobata, and Enteromorpha prolifera (Majee, Avlani, Ghosh, & Biswas, 2018). Ulvan is typically composed of ?- and ?-(1?4)-linked sugar residues, namely ?-1,4- and ?-1,2,4-linked L-rhamnose 3-sulphate, with branching at O-2 of rhamnose, ?-1,4- and terminally linked D-glucuronic acid and ?-1,4-linked D-xylose, partially sulphated on O-2. The primary structural units found in ulvan include ?-D-glucuronosyluronic acid- (1,4)-L-rhamnose 3-sulphate dimer (?-D-GlcpA-(1?4)-LRhap 3-sulphate) and ?-L-IdopA-(1?4)-?-L-Rhap 3-sulphate, also known as ulvanobiuronic acid A and B, respectively. The main difference between these aldobiuronic acids is the presence of glucuronic acid in A, which is replaced by iduronic acid in B (Lahaye, 1998; Quemener, Lahaye, & Bobin-Dubigeon, 1997; Alves, Sousa, & Reis, 2013). One extraordinary feature of ulvan is the occurrence of uncommon sugars within its fibers, i.e., sulphated rhamnose and iduronic acid. Rhamnose is an unusual sugar, typically found in bacteria, plants and accumulates uncommonly in animals. Branching of O-2 of 1, the associated ?-L-rhamnose residue, was found only on an exopolysaccharide produced by the bacterium Arthrobacter sp. The presence of iduronic acid in the ulvan chain is a significant feature since it is not recognized in algal polysaccharides (Quemener et al. 1997; Alves et al., 2013). The possibility of producing nanofibers from ulvan using electrospinning technique was first reported by Toskas et al. (2011). They obtained various sizes of nanofibers with different ratios of ulvan and copolymer PVA. For the rate of ulvan/PVA (50:50), they obtained nanofiber of size approximately 105±4 nm, for 70:30 as 84±4nm and for 85:15 ratio as 60±5nm. Many reports indicated that higher concentration biopolymer than the synthetic copolymer in the mixer lead to the formation of beads in nanofibers. In contrary, in their findings, a higher concentration of ulvan showed smaller size of nanofibers without any bead formation as evidenced from SEM and TEM analyses. Another research report published by Kikionis et al. (2015) demonstrated that ulvan could be converted into electrospun nanofiber by blending with two biodegradable synthetic polymers such as polyethylene oxide (PEO) and polycaprolactone (PCL). They investigated the synthesized nanofibers by SEM, FTIR which revealed the strong interaction and good compatibility between ulvan and the two copolymers. Moreover, the stability of ulvan nanofibers was examined and found that it does not lose its balance even after 18 months of storage which concluded that ulvan could represent new promising biomaterials for producing strong nanofibers for various biological applications.Agar and agarose. Agar and agarose are widely used as a gelling agent in the food industry and microbiological purposes, extracted from red seaweeds (Khalil et al., 2017). In general, agar is composed of two polysaccharides such as agarose and agaropectin with similar structural and functional properties as carrageenans. Agarose is the significant component of agar than agaropectin, and it consists of high molecular weight polysaccharides composed of repeating units of (1?3)-?-D-galactopyranosyl-(1?4)-3,6-anhydro-?-L-galactopyranose. The structure of agaropectin, with a lower molecular weight than agarose, is mainly made up of alternating (1?3)- ? -D-galactopyranose and (1?4)-3,6-anhydro- ? -L-galacto-pyranose residues (Pérez et al., 2016). Agar and agarose are associated with several biomedical applications especially as hydrogels for the release of bioactive agents, taking advantage of its ability to gel, biocompatibility and biodegradability in nature (Cardoso et al., 2016). Only sparse details are available on nanofiber synthesis from agar and agarose as limited research have been carried out on electrospinning of this marine algal polysaccharides. Sadrearhami et al. (2015) attempted to produce nanofibers from agar with polyacrylonitrile as copolymer to immobilize methotrexate for cancer therapy and succeeded by electrospinning method. To evaluate the effects of polymer ratio and drug concentration on release rate, solutions with different polyacrylonitrile/agar ratios were prepared and subsequently electrospun with varying proportions of methotrexate-polymer. The results demonstrated that increasing the drug and agar concentration led to rising in diameter due to increase in the solution blend viscosity which was confirmed by SEM analysis. Moreover, drug release rates increased with increasing agar ratio due to the increased hydrophilicity of the drug delivery systems. They concluded that novel agar nanofibers proved to be a potential candidate for controlled release of drugs or any other bioactive compounds for various biological applications. UV-irradiated agarose/polyacrylamide cross-linked double-network electrospun nanofibers were produced in the range of 187 nm (Cho et al., 2016). Moreover, they analyzed the thermal stability of double-network nanofibers using thermogravimetric analysis (TGA) and showed the excellent thermal property at 290–500 °C. From the results, they recommended that agarose/polyacrylamide nanofibers could be used as possible material in biomedical and bioengineering applications. Fucoidan. Fucoidan is a water-soluble sulfate-rich polysaccharide mainly composed of fucose (Puvaneswary et al., 2016). The molecular weight of fucoidan have been recorded in the range of 100 to 1600 kDa, and the differences are due to differing composition and chemical structure including the degree of branching, substituents, sulphation and type of linkages (Rioux, Turgeon, & Beaulieu, 2007; Pérez et al., 2016). Mostly fucoidans are extracted from seaweeds like Laminaria spp., Analipus japonicus, Cladosiphon okamuranus, Chorda filum, Ascophyllum nodosum and Fucus sp. The molecular structure of fucoidans comprises of backbone structure of (1?3)-linked ?-L-fucopyranosyl ? (1?3) and ? (1?4)-linked L-fucopyranosyls (Tutor & Meyer, 2013; Pérez et al., 2016). Names like fucans, fucosans, fucose is used for this group of polysaccharide extracted from other marine species, but fucoidan is the term held for the algal source by IUPAC naming system (Pérez et al., 2016).Lee et al. (2012) fabricated nanofiber using fucoidan and polycaprolactone (PCL) by electrospinning technique at various concentrations of fucoidan as 1, 2, 3, and 10 %w/v. The result showed that electrospun nanocomposites of fucoidan/PCL exhibited improved hydrophilicity, tensile strength than the PCL fiber mats. In another study, fucoidan nanofiber was successfully produced with Chitosan and Poly(vinyl alcohol) for vascular tissue engineering (Zhang et al., 2017). After electrospinning, they obtained well defined interconnected nanofibers composed of F/CS/PVA which was evidenced by SEM and FTIR analysis. Moreover through XRD pattern it was confirmed that electrospinning process of F/CS/PVA mixer had lowered the crystallinity of the polymers and have more excellent water uptake ability, sufficient porosity and enhanced drug release. Besides, fucoidan per se has various biological functions like anticoagulant, antiviral, immunomodulatory activity (Lee et al., 2012) and potential antibacterial activity against food pathogens (De Jesus Raposo et al., 2015; Chua et al., 2015). Hence, fucoidan is also one of the promising candidates for making nanofibers to incorporate natural antimicrobial agents to preserve foods.Advantages of marine algae for extraction of antimicrobial agents and nanofibersThe following essential features highlight that the marine algae are an ideal candidate than the other sources for isolation of antimicrobial compounds and to fabricate nanofibers to be used in food preservation. Since, marine algae exist in the complex living environment and are exposed to high salinity, they are able to synthesize many different kinds of potential bioactive compounds that cannot be found in the terrestrial environment (Hamed et al., 2015).Need for agricultural land for cultivation as like terrestrial plants and oceans occupy 70% of the earth is not required; this makes them the unlimited resource for bioactive compounds (Tittensor et al., 2010; Hamed et al., 2015; Bajpai, 2016).Non requirement of nutrients and fertilizer for their growth (Sirajunnisa and Surendhiran, 2016). Non competance with food chain since they grow in the marine environment (Sirajunnisa & Surendhiran, 2016); unlike sources like herbs and spices that are used for extraction of bioactive compounds in turn increasing the food price as some South Asian countries like India, Pakistan, Bangladesh, etc. use spices as their primary food ingredients (Zaidi, 2016). Marine algae are measured as the best potential reservoir for antimicrobial compounds by their bioavailability throughout the coastal areas of many countries (Eom et al., 2012; Kadam et al., 2013); whereas some plant sources are seasonal.Many organisms produce marine natural products that possess unique structural features when compared to terrestrial metabolites (Eom et al., 2012).Most of the marine algal bioactive compounds show both antimicrobial and antioxidant activities which are highly suitable for food application than the other sources (Senthilkumar & Sudha, 2012).Conclusion Marine algae are abundant in the marine ecosystem that offers an unlimited renewable resource of natural antimicrobial and other bioactive compounds as well as biopolymers. Since marine bioactive compounds are unexplored in the terrestrial environment, this could actively restrict the growth of resistant food pathogens. Recent studies revealed that marine algal species represent an inspirational model for the development of new alternative antimicrobial agents to be used in food preservation. Moreover, marine algal biopolymers stay as an unexploited pool of novel biomaterials for nanofiber synthesis due to their biocompatibility, biodegradability and low cost of the extraction process. Besides, marine algae contain an enormous quantity of nutritionally rich biomolecules that could be directly added into foods as functional ingredients. In conclusion, marine algae have widely been studied as the raw material for the development of novel antimicrobial agents and as carrier device for delivering them into food system without causing any harmful effects on consumers. Furthermore, the extraction and application of marine algal compounds in the food industry is in the nascent state and currently under investigation. 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