Pullulan production from agro-industrial waste and its applications in food industry: A review

Carbohydrate Polymers 217 (2019) 46–57

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Pullulan production from agro-industrial waste and its applications in food industry: A review

T

⁎

Ram Sarup Singha, , Navpreet Kaura, John F. Kennedyb a b

Carbohydrate and Protein Biotechnology Laboratory, Department of Biotechnology, Punjabi University, Patiala, 147 002, Punjab, India Chembiotech Laboratories, Advanced Science and Technology Institute, 5 The Croft, Buntsford Drive, Stoke Heath, Bromsgrove, Worcs, B60 4JE, UK

A R T I C LE I N FO

A B S T R A C T

Keywords: Solid-state fermentation Submerged fermentation Agro-industrial waste Aureobasidium pullulans Pullulan

Pullulan is a microbial exopolysaccharide produced from Aureobasidium pullulans by submerged fermentation of a medium supplemented with carbon, nitrogen and other essential nutrients. These nutrients are expensive which increase the cost of pullulan production. The requirement of alternative cost-effective substrates for pullulan production is a prerequisite. Agro-based industries generate a large volume of solid/liquid waste and its accumulation generates a severe environmental impact. These wastes are composed of carbohydrates, proteins and other constituents, and can be used as substrates for the development of low-cost processes for the production of various microbial products. This could be a good environmental friendly waste management system. Pullulan production from agro-industrial wastes can be carried out by both submerged and solid-state fermentation by A. pullulans. Owing to its unique properties, pullulan has wide applications in many food-based industries. This review highlights pullulan production from agro-industrial wastes and potential applications of pullulan in various food industries.

1. Introduction Microbial polymers are promising alternatives for both natural and synthetic polymers. These can be exopolysaccharides, endopolysaccharides or polyhydroxyalkanoates and consists of uronic acid, carbohydrate and non-carbohydrate moieties (Donot, Fontana, Baccou, & Schorr-Galindo, 2012; Singh & Kaur, 2015). Pullulan is one of the commercially important microbial polymers which is produced by submerged fermentation from Aureobasidium pullulans (Singh & Saini, 2008a, 2008b; Singh, Saini, & Kennedy, 2009; Sugumaran and Ponnusami, 2017a, 2017b). The prerequisite for the fermentative production of pullulan is carbon source, nitrogen source and other essential nutrients for adequate growth of A. pullulans. The nutrients used for pullulan production are expensive which add to its cost of production. However, the waste generated by many agro-based industries is very rich in organic/inorganic constitutes required for the growth of A. pullulans. These wastes can be used as an alternative substrate for pullulan production by submerged or solid-state fermentation. Pullulan is a linear glucan and its structure consists of maltotriose as repeating units (Fig. 1a). Each maltotriose unit constitutes two α-(1→4) bonded glucopyranose rings interlinked by α-(1→6) linkage (Singh & Saini, 2012). Sometimes, partial acid hydrolysis yields rare forms of pullulan constituting panose (Fig. 1b) and isopanose (Fig. 1c) as ⁎

repeating units (Sowa, Blackwood, & Adams, 1963). Pullulan possesses unique physicochemical properties (Table 1). It is a non-ionic and nonhygroscopic polymer without any toxicity, mutagenicity, carcinogenicity and its viscosity is comparatively lower than other polymers. Owing to these distinctive properties, pullulan has potential applications in food, pharmaceutical and biomedical fields (Alhaique, Matricardi, Di Meo, Coviello, & Montanari, 2015; Singh, Saini, & Kennedy, 2008; Tabasum et al., 2018). Pullulan is an edible polymer and it has been certified harmless for usage in food products by food safety regulations in many countries. It can be used as a stabilizer, binder, intensifier, beverage filler, dietary fiber, thickener, texture improver, food packaging, etc. Pullulan and its derivatives have potential applications in drug delivery and gene delivery (Singh & Saini, 2014; Singh, Kaur, & Kennedy, 2015), corneal wound healing (Singh, Kaur, Sharma, & Rana, 2018) and tissue engineering (Singh, Kaur, Rana, & Kennedy, 2016). It is a novel molecule for biomedical applications (Singh, Kaur, Rana, & Kennedy, 2017). Plenty of agro-industrial wastes have been used as substrates for the production of pullulan from A. pullulans by solid-state and submerged fermentation. The information on numerous applications of pullulan in the food industry is scattered in the literature. In this review, pullulan production from agro-industrial wastes has been discussed. The applications of pullulan in food industries have also been described.

Corresponding author. E-mail addresses: [email protected], [email protected] (R.S. Singh).

https://doi.org/10.1016/j.carbpol.2019.04.050 Received 4 March 2019; Received in revised form 22 March 2019; Accepted 11 April 2019 Available online 13 April 2019 0144-8617/ © 2019 Elsevier Ltd. All rights reserved.

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Fig. 1. Structure of pullulan with (a) maltotriose; (b) panose and (c) isopanose as repeating units.

saprophyte fungus Tremella mesenterica producing pullulan has also been reported (Fraser & Jennings, 1971; Jennings & Smith, 1973). Some strains of obligate parasitic fungi like Cytaria harioti (Waksman, De Lederkremer, & Cerezo, 1977) and C. darwinii (Oliva, Cirelli, & De Lederkremer, 1986) also have the ability to produce pullulan. Many more fungal strains like Cryphonectria parasitica (Corsaro et al., 1998), Teloschistes flavicans (Reis, Tischer, Gorrin, & Iacomini, 2002) and Cryphonectria parasitica (Delben, Forabosco, Guerrini, Liut, & Torri, 2006; Forabosco et al., 2006) have been reported as pullulan producers. Yeast strains like Rhodotorula bacarum (Chi & Zhao, 2003) and Rhodosporidium paludigenum have also been reported as pullulan producers (Singh & Kaur, 2018).

Table 1 Physicochemical properties of pullulan. Parameter

Description

Color Nature Molecular weight Melting point Viscosity (10% (w/v) solution, 30 °C) Solubility

White or off-white Powder 45-600 kDa 250 °C 100–180 cP

Insolubility pH (1% (w/v) solution) Mineral residue-ash (sulphated) Polypeptides Moisture content (without tackiness or hygroscopy) Specific optical activity [α] D2O (1% (w/v) in water)

Easily soluble in cold water, hot water and dilute alkali Insoluble in organic solvents except formamide and dimethylsulfoxide 5–7 ≤3% ≤0.5% 10–15%

3. Pullulan production from agro-industrial wastes Agro-based industries generate a huge amount of waste and if the waste is discarded untreated, it can cause severe environmental issues. However, these agro-industrial wastes are rich source of nutrients, organic and inorganic matter. These wastes can be used as alternative carbon or nitrogen substrate for the production of various microbial products. It helps in reducing the environmental pollution generated by direct discard of untreated waste and is also economically good. Pullulan production from a number of agro-industrial wastes have been reported (Table 2). Pullulan production from agro-industrial waste can be carried out by submerged or solid-state fermentation depending on the type of waste generated (Fig. 2). A number of agro-industrial wastes mentioned below have been used as carbon/nitrogen substrates for the production of pullulan.

≥+160°

2. Microbial sources of pullulan Commercially, pullulan is produced from Aureobasidium pullulans. A. pullulans is a yeast-like polymorphic fungus which involves the formation of an elongated branched septate and large chlamydospores during its life-cycle. The morphological investigations on A. pullulans during polysaccharide elaboration established that production of pullulan is not related to its any particular morphological form (Seviour, Kristiansen, & Harvey, 1984). Later on, Yurlova and de Hoog (1997) investigated the growth cycle of A. pullulans and reported that the pullulan is produced by hyphal cells of A. pullulans. In other studies, it has also been reported that the pullulan is produced, when the blastospores are formed during the growth cycle of A. pullulans (Gibbs & Seviour, 1996; Reeslev, Storm, Jensen, & Olsen, 1997). Chlamydospores and swollen cells have also been reported to be associated with pullulan production in submerged fermentation (Campbell, Siddique, McDougall, & Seviour, 2004; Simon, Bouchet, Caye-Vaugien, & Gallant, 1995). In addition to A. pullulans, there are a number of other microbial sources which are potent pullulan producers. A mycoparasitic

3.1. Agro-industrial wastes as carbon substrate for pullulan production 3.1.1. Potato waste Potato is the most widely explored vegetable for the production of ready-to-eat products by the food industries. The potato processing plants generate a large amount of solid and liquid wastes (Arapoglou et al., 2009). The peeling of potatoes produces solid waste, while further processing of potatoes by cutting and washings generates liquid waste. The solid waste can be utilized one way in food or otherwise in animal feed preparations. The liquid potato waste has high chemical 47

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Table 2 Pullulan production from agro-industrial wastes. Agro/agro-industrial waste

Microorganism

Type of fermentation

Fermentation conditions*

Pullulan production (g/L)

References

Beet molasses

A. pullulans P 56 A. pullulans P 56

Submergeda Submergedb

24.00 49.00

(Lazaridou, Biliaderis et al., 2002) (Lazaridou, Roukas et al., 2002)

A. pullulans P 56 A. pullulans P 56

Submergeda Submergedc

28.20 27.00

(Roukas, 1998) (Roukas & Serris, 1999)

A. pullulans P 56

Submergedb

23.00

A. pullulans P 56 A. pullulans P 56

a

Submerged Submergedb

(Roukas & LiakopoulouKyriakides, 1999) (Goksungur et al., 2004) (Goksungur et al., 2004)

A. pullulans MTCC 2195 A. pullulans MTCC 1991 A. pullulans MTCC 2670

Submergeda Solid-stated Solid-statee

28 °C, 8 days, 200 rpm 28 °C, 8 days, 700 rpm, aeration 1.4 dm3 min−1 28 °C, 5 days, 200 rpm 28 °C, 5 days, shear rate 42 s−1, aeration rate 2 vvm 28 °C, 5 days, 650 rpm, aeration rate 1 vvm 28 °C, 5 days, 200 rpm 28 °C, 5 days, 400 rpm, aeration rate 2 vvm 35 °C, 150 rpm, 5 days 28 °C, 7 days 30 °C, 5 days

Coconut milk Coconut water De-oiled rice bran Grape skin pulp extract Jackfruit seeds

A. A. A. A. A. A. A.

Submergeda Submergeda Submergeda Submergeda Submergeda Submergeda Solid-stated

28 °C, 28 °C, 28 °C, 28 °C, 30 °C, 28 °C, 28 °C,

200 rpm 210 rpm 200 rpm 200 rpm 150 rpm 200 rpm

88.59 65.30 58.00 38.80 54.80 22.30 34.22

Jatropha seedcake Palm kernel

A. pullulans MTCC 2195 A. pullulans RBF 4A3 A. pullulans MTCC 2670

Submergeda Submergeda Solid-stated

30 °C, 7 days, 200 rpm 28 °C, 5 days, 200 rpm 30 °C, 7 days

18.76 83.98 18.43

A. pullulans NRRLY-6220 A. pullulans 201253 A. pullulans P 56 A. pullulans CCTCCM2012259 A. pullulans MTCC 1991

Submergeda Submergedb Submergeda Submergedb

29 °C, 7 days, 200 rpm 28 °C, 5 days, 500 rpm 28 °C, 5 days, 200 rpm 28 °C, 3 days, 400 rpm, aeration rate 3 L min−1 27 °C, 7 days, 210 rpm, aeration rate 1.25 vvm 30 °C, 4 days, 200 rpm 28 °C, 5 days, 200 rpm 28 °C, 4 days, 200 rpm 25.3 °C, 4 days, 232 rpm 35 °C, 5 days, 150 rpm 28 °C, 4 days, 200 rpm 28 °C, 5 days, 210 rpm

69.00 54.57 19.20 22.20

(Srikanth et al., 2014) (Ray & Moorthy, 2007) (Sugumaran & Ponnusami, 2017a, 2017b) (Sharma et al., 2013) (Hafez et al., 2007) (Thirumavalavan et al., 2009) (Thirumavalavan et al., 2009) (Singh & Kaur, 2019) (Israilides et al., 1998) (Sugumaran, Gowthami et al., 2013) (Sharmila et al., 2013) (Choudhury et al., 2012) (Sugumaran, Gowthami et al., 2013) (Barnett et al., 1999) (An et al., 2017) (Goksungur et al., 2011) (Wang et al., 2014)

125.7

(Sheoran et al., 2012)

7.50 11.00 15.70 25.19 45.00 29.43 12.00

(Seo et al., 2004) (1999a), (Hilares et al., 2017) (Hilares et al., 2019) (Srikanth et al., 2014) (Wu et al., 2009) (Hafez et al., 2007)

Cassava bagasse

Corn steep liquor

Potato starch water

Rice hull Soybean pomace

Spent grain liquor Sugarcane bagasse Sugarcane molasses Sweet potato hydrolysate Whey

A. A. A. A. A. A. A.

pullulans pullulans pullulans pullulans pullulans pullulans pullulans

pullulans pullulans pullulans pullulans pullulans pullulans pullulans

RBF 4A3 ATCC 42023 MTCC 2195 MTCC 2195 MTCC 6994 NRRLY 6220 NCIM 1049

HP-2001 P 56 LB83 LB83 MTCC 2195 AP329 ATCC 42023

Submergedb a

Submerged Submergeda Submergeda Submergeda Submergeda Submergeda Submergeda

5 5 7 7 7 5 7

days, days, days, days, days, days, days

16.70 6.60 45.00 32.00 19.00

* Temperature (℃); Incubation period (Days); Agitation (rpm). a Shake-flask fermentation. b Stirred tank reactor fermentation. c Airlift reactor fermentation. d Solid-state fermentation in flasks.

hydrolyzes the α-1,4 glucose linkages to produce high glucose syrup. The immobilization of glucoamylase and pullulanase in Ca-alginate beads enhances the efficiency of liquefaction of starch and the resulting hydrolysate can act as a suitable substrate for fermentative production of pullulan (Goksungur, Uzunogullari, & Dagbagli, 2011). Pullulan yield was increased 2-fold in the hydrolysate generated by the action of β-amylase as compared to glucoamylase (Barnett, Smith, Scanlon, & Israilides, 1999). Some strains of A. pullulans possess starch degrading enzyme i.e. amylase, and can partially hydrolyze potato starch. The partially hydrolyzed starch has great potential for pullulan production (Israilides, Scanlon, Smith, Harding, & Jumel, 1994, 1998; Israilides, Smith, Scanlon, & Barnett, 1999). The utilization of potato starch hydrolysate supplemented with sucrose has increased the pullulan production in 10-L bioreactor by A. pullulans (An, Ma, Chang, & Xue, 2017). The increase in pullulan production can be attributed to the stimulation of enzymes of the producer organism which has proficiently increased the pullulan yield in potato starch hydrolysate based medium (An et al., 2017). The use of Reeslev and Jensen medium with potato starch waste as a sole carbon source has also enhanced 3 folds of pullulan production in shake-flask fermentations (Hafez, Abdelhady, Sharaf, & El-Tayeb, 2007). The supplementation of Reeslev and Jensen

oxygen demand (2–3%) and very low pH (3.9–4.1). It consists of high amount of total solids (1.8–4.0%) i.e. total suspended solids (0.30−0.42%), total insoluble solids (0.48−0.64%) and volatile suspended solids (0.21−0.37%). It also contains large amount of starch (2.0–2.5%) and low content of reducing sugars (0.08−0.12%) (Huang, Jin, Lant, & Zhou, 2003). The release of potato wastewater in the environment can cause severe pollution problems. Starch can be used as a carbon substrate by different microbial flora for fermentative production of various valuable products. Starch consists of two molecules i.e. amylose and amylopectin. These molecules have a complex structure which makes their utilization in native form quite difficult for nearly all the industrially important microorganisms. However, the hydrolyzed form of starch acts as simple sugars which are good substrate for microbial growth. The enzymatic hydrolysis of starch involves two steps i.e., first is the treatment with α-amylase and second is exposure of partially hydrolyzed starch to a combination of pullulanase and glucoamylase. The α-amylase acts on amylose and break down the α-1,4 glucose linkages leading to the liquefaction of gelatinized starch. Further, pullulanase and glucoamylase are added together for efficient hydrolysis of starch (Roy & Gupta, 2004). Pullulanase hydrolyzes the α1,6 glucose linkages of amylopectin and simultaneously glucoamylase 48

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Fig. 2. Schematic representation of pullulan production by fermentation and recovery by downstream processing.

sugarcane bagasse. Though it is biodegradable and its disposal has no adverse effects on the environment, but the quantity of sugarcane bagasse produced is so high that raises serious environmental issues. Approximately 280 kg of bagasse is generated from one ton of sugar produced (Cerqueira, Filho, & Meireles, 2007), which becomes nearly 100 million tons every year (Cheng & Zhu, 2013). Although, the dried sugarcane bagasse is commonly used as the prime energy source in ethanol distilleries and sugar mills, but, a large amount of bagasse still

medium with potato starch overcomes the deficiency of nitrogen or mineral content of potato starch waste during the fermentation process (Hafez et al., 2007). 3.1.2. Sugarcane bagasse hydrolysate Sugarcane is one of the most abundantly produced crops in India and many other countries. The extraction of sugarcane juice for the production of sugar and sugar products generates solid waste i.e. 49

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Table 3 Applications of pullulan in food industries. Function

Application(s)

Reference(s)

Dried food packaging Low viscosity filler Stabilizer Prebiotic Sugar syrup Adhesive Diabetic food Intensifier Dietary fiber

(Krochta & De Mulder-Johnston, 1997; Singh & Saini, 2012; Singh & Kaur, 2015) (Tsujisaka & Mitsuhashi, 1993) (Yamaguchi & Sunamoto, 1991) (Mitsuhashi et al., 1990; Yoneyama et al., 1990) (2010b, Singh et al., 2010a,2010b) (Hijiya & Shiosaka, 1975a) (Wolf, 2005) (Yatmaz & Turhan, 2012) (Oku et al., 1979; Yoneyama et al., 1990)

Binder

Nuts, noodles, confectionaries, vegetables and meat Beverages, drinks and sauces Food pastes, emulsions and mayonnaise Promoting bifidobacteria Maltotriose syrup Nuts on cookies Dietetic snack foods Sauces, soups and beverages Artificial rice, noodles, confectionary and bakery products Seed coating, plant fertilizer and tobacco binder

Starch replacement Preservative

Pasta and baked goods Ice-cream and frozen foods

(Matsunaga, Fujimura, Namioka, Tsuji, & Watanabe, 1977; Matsunaga, Tsuji, & Watanabe, 1978; Miyaka, 1979) (Hiji, 1986; Hijiya & Shiosaka, 1975b; Kato & Shiosaka, 1975; Yuen, 1974) (Carrington, Goff, & Stanley, 1996; Goff, 1995; Goff & Sahagian, 1996)

and supernatant was separated by centrifugation (Roukas, 1998). The pretreated molasses enhanced the pullulan production by 2 folds as compared to the pullulan production from untreated molasses in shakeflask fermentation. The combination of activated carbon with sulfuric acid helps in removal of extra coloring substances and amino acids along with heavy metals which further improves the production of pullulan at shake-flask level (Goksungur, Ucan, & Guvenc, 2004; Lazaridou, Biliaderis, Roukas, & Izydorczyk, 2002). The use of pretreated molasses in production medium is cost-effective for pullulan production (Srikanth et al., 2014). In a number of studies, it has been reported that the usage of pretreated molasses enhances the pullulan production by 49.0 g/L (Lazaridou, Roukas, Biliaderis, & Vaikousi, 2002), 23.0 g/L (Roukas & Liakopoulou-Kyriakides, 1999) in stirred tank reactors and 18.5 g/L in an airlift reactor (Roukas & Serris, 1999).

remained underutilized. Sugarcane bagasse is a lignocellulosic material which consists of cellulose (38.59 ± 3.45%), hemicellulose (27.89 ± 2.68%), lignin (17.79 ± 0.62%), organic matter (1.61 ± 0.16%), extractives (1.11 ± 1.23%) and ashes (8.80 ± 0.02%) (Guilherme, Dantas, Santos, Fernandes, & Macedo, 2015). The saccharification of sugarcane bagasse converts lignocellulosic sugars to simple sugars which can be utilized by many microorganisms. The steam exploded sugarcane bagasse was hydrolyzed with sulfuric acid (0.1%) at 100 °C for 30 min (Prakash, Varma, Prabhune, Shouche, & Rao, 2011) and resultant hydrolysate was detoxified at 28 °C with activated charcoal (1%) under agitation (50 rpm) for 4 h. The hydrolysate was composed of xylose (70%), glucose (12%), arabinose (7%), other substances (11%) and it was used for pullulan production by A. pullulans (Chen et al., 2014). The supplementation of sugarcane bagasse hydrolysate based medium with DL-dithiothreitol (1.0 mM) and pH control has enhanced the pullulan production in shake-flask fermentations (Chen et al., 2014). The fermentative production of pullulan by A. pullulans is accompanied by melanin formation, which increases the cost of downstream processing. The use of blue light-emitting diode completely eliminates the melanin production in the fermentation process and the red light-emitting diode enhances the growth of A. pullulans. A low-melanin containing pullulan (20 g/L) can be produced from sugarcane bagasse hydrolysate by A. pullulans in shake-flask fermentations assisted by light-emitting diode (Hilares et al., 2017). Sugarcane bagasse hydrolysate was used for the production of pullulan by A. pullulans in shake-flask fermentations and column bubble photobioreactor (Hilares et al., 2019). Pullulan yield (25.19 g/L) in column bubble photobioreactor was similar to shake-flask fermentations.

3.1.4. Sweet potato hydrolysate Sweet potato is a sweet tuberous root vegetable rich in carbohydrates, beta-carotene, vitamins, and fibers. The sweet potato hydrolysate is composed of proteins (87%), sugar (1.56%), fat (0.6%), crude fiber (0.16%) and ash (2.19%) (Mu, Tan, & Xue, 2009). The major part of sweet potato is starch which is quite suitable for industrial fermentation, though it cannot be utilized in its native form by many industrially important microorganisms. The hydrolysis of sweet potato starch involves the same process used for potato starch. The saccharification process involves treatment of small pieces of sweet potato with three different enzymes i.e. α-amylase, pullulanase and β-amylase. Sweet potato itself consists of a substantial amount of β-amylase, so it is not required to add it from the external source (Wu, Jin, Tong, & Chen, 2009). The first step of hydrolysis involves treatment of the sweet potatoes with α-amylase and pullulanase. The hydrolysate obtained can be further saccharified by β-amylase present in sweet potato itself. The sweet potato hydrolysate can be used as an economical carbon substrate in fermentation processes. Sweet potato hydrolysate was utilized by A. pullulans in shake-flask fermentations for pullulan production (Wu et al., 2009). The molecular weight of pullulan produced from sweet potato hydrolysate (3.4 × 105 Da) was higher in comparison to sucrose (1.7 × 105 Da) and glucose (1.3 × 105 Da) media. Sweet potato starch can be effectively hydrolyzed by marine cold-adapted α-amylase (Wu et al., 2009). The sweet potato hydrolysate consists of glucose, maltose, isomaltose, maltotriose, and traces of other maltooligosaccharides. These components of hydrolysate have a good degree of polymerization (4–7). The pullulan production by A. pullulans from sweet potato hydrolysate was higher (36.17 g/L) than those obtained from glucose (22.07 g/L) and sucrose (31.42 g/L). Hence, sweet potato hydrolysate can be utilized for cost-effective pullulan production (Wu, Lu, Chen et al., 2016).

3.1.3. Molasses Molasses is dark brown viscous liquor generated as a byproduct during refining of sugarcane or sugar beet juice to sugar particles. A major amount of molasses is released to the nearest water source by the sugar industry which poses a high level of pollution in the environment. Molasses consists of fermentable sugars i.e. glucose and fructose (48–60%), total solids (70–85%), organic content (9–12%) and inorganic ash (10–15%) (Soni & Soni, 2007). Owing to these sugars, molasses can be easily assimilated as a carbon substrate for the production of pullulan by A. pullulans (Israilides et al., 1994). However, molasses also consists of heavy metals (copper, iron, manganese, zinc, calcium, magnesium, etc.) which hinder the growth of microorganisms, inactivate the advantageous enzymes and lower down the final product yield (Roukas, 1998). Hence, to attain qualitatively and quantitatively good product yield, the pretreatment of molasses is an essential step. The treatment of molasses with sulphuric acid is the best method for removal of heavy metals. In a pretreatment of molasses, sulphuric acid (1 N) was added to molasses, then liquid was allowed to stand for 24 h 50

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Table 4 Pullulan based edible films/coatings and their functional properties with potential applications in food packaging. Pullulan blended film/coating

Food product(s)

Improved functional characteristics

References

Pullulan-calcium chloride-chitosan

Chinese jujube

(Kou, Li, Wu, Chen, & Xue, 2017)

Pullulan-glycerol-chitosan

Pineapple

Pullulan-glutathione-citric acid-potassium sorbate

Razor clam Sinonovacula constricta Chinese meats

Pullulan-n-octenyl succinic anhydride

Sapota fruits of Kalipatti variety Cherry tomatoes

Delays fruit senescence; retains quality and antioxidant capacity Increases shelf-life; preserves color, odor, flavor, texture and overall acceptance; delays signs of decay; inhibits growth of Listeria monocytogenes and Salmonella typhi Inhibits bacterial growth; maintains pH of meat and total volatile basic nitrogen; enhances overall acceptability score of meat during refrigerated storage Delays ripening and senescence; extends shelf-life

Pullulan-Laminaria japonica derived oligosaccharides Pullulan

Rice starch

Pullulan-calcium chloride

Huangguan pear

Pullulan-glycerol-leather bergenia leaves extract

Apples and peppers

Pullulan

Chicken eggs

Pullulan-glycerin-locust bean-xanthan gum-nisinZlauricarginate Pullulan-sodium benzoate-potassium sorbateglycerol Pullulan-glycerol-tween 80

Raw beef

Pullulan-3-aminopropyl trimethoxysilane

–

Pullulan-glycerol-ethanol-meadowsweet flowers

Apples

Pullulan-glycerin-summer savory Satureja hortensis L.

Apples and peppers

Pullulan-glycerol-xanthan gum-oregano essential oils-rosemary essential oil-Ag nanoparticlesZnO nanoparticles Pullulan-glycerol-ethanol-meadowsweet flowers Pullulan-caraway essential oil

Raw beef, raw turkey breast and ready-to-eat turkey breast Red pepper Fresh baby carrot

Pullulan-glutathione-chitooligosaccharides

Fresh cut apples Raw turkey breast

Strawberries

Reduces respiratory intensity, vitamin C loss, weight loss and softening; increases overall likeness and shelf-life Inhibits short-term retrogradation of rice starch amylose; retards long-term retrogradation of amylopectin Inhibits brown spot disorder; delays loss of polyphenol substances; maintains structural integrity of fruit peel Inhibits growth of Staphylococcus aureus, Bacillus subtilis, Salmonella enteritidis, Aspergillus niger and Penicillium expansum; reduces weight loss; maintains hardness of apples and peppers Preserves internal quality; prolongs shelf-life; minimizes weight loss Reduces growth of Escherichia coli

Pullulan-thymol-glycerol

Apples and mandarins

Pullulan-whey protein isolate-glycerol

Chinese chestnuts

Pullulan-glycerin-locust bean-xanthan gum-sakacin A Pullulan-sorbitol-sucrose-fatty ester

Ready-to-eat turkey breast

Controls microbial growth and decay rate; preserves organoleptic properties of fruit Extends shelf-life in perforated package; delays mold formation; decreases weight loss, degradation of ascorbic acid and carotenoids; maintains firmness of fruit Inhibits growth of Staphylococcus aureus and Escherichia coli Delays disease caused by mesophilic bacteria and Rhizopus arrhizus Inhibits growth of Staphylococcus aureus, Bacillus subtilis, Salmonella enteritidis, Escherichia coli and Penicillium expansum; reduces weight loss; maintains hardness of apples and peppers Reduces growth rate of Escherichia coli, Listeria monocytogenes, Salmonella typhimurium and Staphylococcus aureus Delays disease development by Rhizopus arrhizus Maintains better visual acceptability; extends microbiological stability against Staphylococcus aureus, Saccharomyces cerevisiae and Aspergillus niger Reduces growth of psychrophilic bacteria Reduces growth of Salmonella enteritidis and Salmonella typhimurium Reduces growth of Listeria monocytogenes and Staphylococcus aureus Inhibits growth of Staphylococcus aureus, Bacillus subtilis, Escherichia coli and Salmonella enteritidis Delays color changes and moisture loss; increases shelflife Reduces growth of Listeria monocytogenes

White asparagus

Brighter appearance

Kiwi and strawberries

Reduces internal oxygen and rate of weight loss; maintains intact firmness and color of fruits Process of senescence delays; lesser weight loss

Strawberries

Deli ham

Pullulan-soy protein isolate-glycerol-stearic acid

Kiwi

(Trevino-Garza, Garcia, Heredia, Alanis-Guzman, & Arevalo-Nino, 2017) (Jiang, 2016)

(Shah, Vishwasrao, Singhal, & Ananthanarayan, 2016) (Wu, Lu, & Wang, 2016) (Chen, Ren, Zhang, Tong, & Rashed, 2015) (Kou et al., 2015) (Krasniewska et al., 2015)

(Morsy, Sharoba, Khalaf, ElTanahy, & Cutter, 2015) (Pattanayaiying, Hkittikun, & Cutter, 2015) (Trevino-Garza, Garcia, FloresGonzalez, & Arevalo-Nino, 2015) (Eroglu, Torun, Dincer, & Topuz, 2014) (Fernandes et al., 2014) (Gniewosz et al., 2014) (Krasniewska et al., 2014)

(Morsy, Khalaf, Sharoba, ElTanahi, & Cutter, 2014) (Synowiec et al., 2014) (Gniewosz, Krasniewska, Woreta, & Kosakowska, 2013) (Wu & Chen, 2013)

(Gniewosz & Synowiec, 2011) (Gounga, Xu, & Wang, 2010) (Trinetta, Cutter, & Floros, 2010) (Tzoumaki, Biliaderis, & Vasilakakis, 2008) (Diab, Biliaderis, Gerasopoulos, & Sfakiotakis, 2001) (Xu, Chen, & Sun, 2001)

required for balanced aquatic life. The high BOD of spent grain liquor is its main pollutant (Chaitanyakumar, Unnisa, Rao, & Kumar, 2011). If it is released untreated in the natural water sources, it causes a decline in dissolve oxygen, which can severely affect the aquatic ecosystem and may cause serious environmental pollution problems. Spent grain liquor was used as a substrate for pullulan production by A. pullulans (Roukas, 1999a). The supplementation of spent grain liquor based medium with K2HPO4 (0.5%, w/v), L-glutamic acid (1%, v/v), olive oil (2.5%, v/v) and Tween 80 (0.5%, v/v) has significantly improved the pullulan yield.

3.1.5. Brewery waste The brewing plants generate spent grain liquor as a byproduct along with production of brewery items like beer. Spent grain liquor is a liquid waste generated after final separation of wort from spent grains. The amount of spent grain liquor produced by the brewing industry is a noteworthy source of waste. Spent grain liquor contains organic materials and suspended solids. It consists of hemicellulose (40%, w/v), cellulose (12%, w/v), starch (2.7%, w/v), proteins (14.2%, w/v), lignin (11.5%, w/v), lipids (13%, w/v) and ash (3.3%, w/v) (Xiros, Topakas, Katapodis, & Christakopoulos, 2008). The organic content is expressed as biochemical oxygen demand (BOD) i.e. amount of dissolved oxygen 51

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Vlyssides, Mouraferi, & Karvouni, 1977). Even the growth of few microorganisms is affected by the presence of olive oil effluent. Olive oil waste consists of proteins (10.3%), total sugars (29.7%), reducing sugars (10.6%) and glucose (0.85%) (Israilides et al., 1994). It supports good growth of A. pullulans. It has been used for pullulan production in submerged fermentations (Iniotakis et al., 1991; Israilides, Smith, & Bambalov, 1993; Youssef, Biliaderis, & Rouka, 1998).

3.1.6. Grape pomace extract Grapes are important raw material in wine and juice making industries. The processing of grapes involves the removal of grape skin and the extraction of juice from its pulp. The juice of grapes is mostly used in the preparation of ready-to-drink products, but grape skin and juice-free pulp after processing become a waste known as grape pomace. Grape pomace consists of protein (7.8%), total sugars (85.2%), reducing sugars (3.4%) and glucose (1.28%) (Israilides et al., 1994). It also consists of pigments, acids and some salts which are quite valuable in food industries. Grape pomace is difficult to use in its solid form, however the grape skin and pulp extract is more easy to use. The grape pomace extract can be prepared by adding hot water in the grape pomace followed by stirring (30 min) and filtration (Israilides et al., 1998). It contains approximately all the nutrients of grape pomace. Grape pomace extract has been used for pullulan production by A. pullulans in shake-flask fermentations and pullulan yield (22.3 g/L) was obtained (Israilides et al., 1998). Pullulan produced from grape pomace extract was homogeneous in nature and has high molecular weight with augmented yield (Bambalov & Jordanov, 1993; Israilides et al., 1994, 1999).

3.1.10. Rice hull hydrolysate Rice is the most common agricultural crop in many countries. The processing of rice involves the removal of its outer brown covering known as rice hull. A large amount of rice hull is generated worldwide from rice processing mills every year. Rice hull consists of lignocellulosic materials as its main component i.e. cellulose (50%), lignin (25–30%), and silica (15–20%). These constituents of rice hull make it a desirable substrate for fermentation processes (Ummah, Suriamihardja, Selintung, & Wahab, 2015). Most of the microorganisms cannot utilize lignocellulosic sugars in their native form and therefore saccharification of rice hull is prerequisite to convert the complex sugars into fermentable sugars. The amount of sugars in hydrolysate depends on the method followed for saccharification of rice hull (Zemnukhova et al., 2004). The pretreatment of rice hull involves its drying at 70℃ for 24 h, then proper meshing in a hammer mill followed by its hydrolysis in dilute sulfuric acid (1%, v/v) at 121℃ for 1 h (Wei et al., 2010). Then acid slurry is neutralized by sodium hydroxide. After its filtration, the filtrate is decolorized by mixing it with powdered activated charcoal. The decolorized hydrolysate is used for formulation of production medium. Rice hull hydrolysate consists of xylose (25.52 ± 0.83%), glucose (5.89 ± 0.18%), arabinose (3.37 ± 0.18%), galactose (0.22 ± 0.20%) and acetic acid (0.35 ± 0.02%) (Wang, Ju, Zhou, & Wei, 2014). Rice hull hydrolysate has been used for pullulan production by A. pullulans in a stirred tank fermentor (Wang et al., 2014). The acetic acid present in hydrolysate may interfere with the growth of microbial culture and may have deleterious effect on the pullulan production. So to overcome this issue, the adaptive evolution of parental strain of A. pullulans from acetic acid can be done to improve the efficiency of pullulan production during fermentation.

3.1.7. Coconut wastewater Coconut processing plants making coconut copra, desiccated coconut and coconut meat products release coconut water as waste. Coconut waste water has high BOD (> 100 mg/L) than its permissible limit (100 mg/L) for the disposal of industrial effluents (WHO, 1995). Owing to its high biological oxygen demand (BOD), coconut wastewater acts as an active pollutant, if released untreated in the environment. The neutralization of coconut wastewater makes it within permissible limits for its disposal, but the neutralization cost is quite expensive. Coconut wastewater is rich in carbohydrates (4.41%), proteins (0.52%), ash (0.47%), total sugars (3.42%), sucrose (0.51%), glucose (1.48%) and fructose (1.43%) (Yong, Ge, Ng, & Tan, 2009). Additionally, it contains a considerable amount of vitamins, amino acids, minerals, inorganic content, etc. (Yong et al., 2009). Owing to this composition, coconut wastewater has been utilized for pullulan production in batch fermentation by A. pullulans (Thirumavalavan, Manikkadan, & Dhanasekar, 2009). The production of pullulan from coconut wastewater was double as compared to conventional carbon source sucrose. Coconut wastewater does not require any pretreatment for its utilization in the production medium which further reduces the cost of pullulan production. In another study, coconut waste water has been successfully used for the production of pullulan in shake-flask fermentations (Thirumavalavan et al., 2009).

3.1.11. Peat hydrolysate Peat is the accumulation of natural organic solid materials or partly decomposed plants grown in peatland. It is used for the production of peat briquette which acts as a slow-burning and smokeless solid fuel. These peat briquettes are produced by pretreatment of peat through wet carbonization. The pretreatment of peat with sulphuric acid at 140 °C for 2 h generates liquid waste known as peat hydrolysate (Boa & LeDuy, 1987). Peat hydrolysate consists of glucose (39–54%), xylose (14–19%), rhamnose (13–14%), galactose (13–18%), mannose (4–7%) and arabinose (2–4%) (Evdokimova, Grishina, Vasilyevskaya, Samvilova, & Bytriskaya, 1976). It can be used as a carbon substrate for pullulan production by A. pullulans (LeDuy & Boa, 1983). The use of peat hydrolysate reduces the cost of pullulan production by almost 10 folds (Boa & LeDuy, 1984).

3.1.8. Whey The processing of cheese from milk involves coagulation of milk fat and proteins along with generation of a liquid byproduct known as whey. Whey contains lactose (4.5%), salts (1.0%), proteins (0.8%), and lactic acid (0.1−0.8%) (Yang, Zhu, Li, & Hong, 1994). These constituents in whey make it a potent and cost-effective substrate for production of pullulan. Further, to enhance the utility of whey for fermentation processes, the proteins can be removed by heating it at 90℃ for 20 min. The protein precipitates are removed by filtration and the generated deproteinized whey contains approximately 80% of lactose (Roukas, 1999b). The deproteinized whey has been reported as a potential substrate for production of pullulan by A. pullulans in shakeflask fermentations (Roukas, 1999b). Co-culturing of A. pullulans and Ceratocystis ulmi improved the yield of pullulan from a lactose based medium in shake-flask fermentations (LeDuy, Yarmoff, & Chagraoui, 1983).

3.1.12. Carob pod Carob trees mostly grow on the unproductive field in the warm environments. These trees have significant use in food industries due to its edible pods. The pods of carob contain a high level of tannins which reduce its utility as food and feed. Carob pods contain sugars (40–50%) like glucose, fructose, sucrose, and maltose, along with cellulose (7%), hemicellulose (5%), proteins (3–4%), pectin (1–2%), phenolic components (20%), etc. These constituents make it a potent substrate for fermentations. Carob pod extract has been used as a substrate for pullulan production (6.5 g/L) by A. pullulans in submerged fermentation (Roukas & Biliaderis, 1995).

3.1.9. Olive oil waste The olive oil processing mills produce a phytotoxic effluent which contains phenolic compounds. The olive oil waste is a major pollutant to the environment which inhibits the growth of plants (Israilides, 52

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Jackfruit seed powder has been used for pullulan production in solidstate fermentation (Sharmila, Muthukumaran, Nayan, & Nidhi, 2013; Sugumaran, Sindhu et al., 2013).

3.1.13. De-oiled rice bran extract The rice milling industries generate a large amount of byproducts e.g. rice bran, rice husk, etc. Rice bran contains highly valuable oil and the extraction of oil from it generates de-oiled rice bran. De-oiled rice bran is a rich source of carbohydrates (58.5%, w/v) i.e. cellulose (16.0%, w/v), hemicellulose (29.8%, w/v) and lignin (12.7%, w/v), proteins (16.9%, w/v), total fiber (9.6%, w/v), and fat (1.5%, w/v) (Sunphorka, Chavasiri, Oshima, & Ngamprasertsith, 2012). Owing to these constituents, de-oiled rice bran has a great potential for pullulan production (Singh & Kaur, 2019). The de-oiled rice bran (20%, w/v) in distilled water was kept at 121℃ under pressure (15 psi) for 15 min. The resultant hydrolysate was cooled to room temperature and filtered. The filtrate was used as a sole carbon source for production of pullulan in shake-flask fermentations (Singh & Kaur, 2019). Higher pullulan production (54.80 g/L) was obtained as compared to a sucrose based medium (44.40 g/L) (Singh, Singh, & Saini, 2009).

3.2. Agro-industrial wastes as nitrogen substrate for pullulan production 3.2.1. Corn steep liquor Corn steep liquor is generated as a byproduct in the extraction of starch from corn by wet-milling process. It is a viscous concentrate containing maltotriose (4.0%), lactic acid (4.8%), dextrose (1.2%), maltobiose (0.64%), glycerol (0.35%), acetic acid (0.06%), proteins (40%) and nitrogen free extract (16%) (Amartey & Jeffries, 1994; Mirza & Mushtaq, 2006). It also contains amino acids and vitamins which make it an excellent and inexpensive nitrogen source for fermentation processes (Sharma, Prasad, & Choudhury, 2013). The cost of corn steep liquor is many times less than other nitrogen sources like yeast extract (Liggett & Koffler, 1948). So, the production of pullulan using corn steep liquor reduces its cost of production. Corn steep liquor was used for production of pullulan in shake-flask fermentations (Hafez et al., 2007; Mehta, Prasad, & Choudhury, 2014) and bioreactor (Sharma et al., 2013). The supplementation of ammonium sulphate, dipotassium hydrogen phosphate or yeast extract along with corn steep liquor enhances the production of pullulan during submerged fermentations (Wang et al., 2016).

3.1.14. Cassava bagasse Cassava is a tropical and non-tropical plant which has starchy tuberous roots rich in carbohydrates. The processing of cassava roots for starch extraction generates a huge amount of solid residues which is known as cassava starch residue or cassava bagasse (Srivas & Anatharaman, 2005). Cassava bagasse contains high organic content which needs pretreatment before its disposal in the environment. Cassava bagasse is available at low cost and it consists of starch (63%), crude fibre (10.8%), carbohydrates (2.66%), reducing sugars (1.45%), crude protein (0.88%) and lipids (0.11%) (Farias et al., 2014; Ray & Moorthy, 2007). These constituents make cassava bagasse a potent substrate for production of many microbial products in solid-state fermentation. It has been reported as a potent substrate in solid-state fermentation for pullulan production by A. pullulans (Ray & Moorthy, 2007; Sugumaran & Ponnusami, 2017a, 2017b). Further, the supplementation of mannose and sodium nitrite to cassava bagasse during solid-state fermentations improves the yield of pullulan (Sugumaran, Jothi, & Ponnusami, 2014).

3.2.2. Deoiled jatropha seedcake The seeds of jatropha plant are used for the production of biodiesel. The extraction of jatropha seed oil leaves a large amount of jatropha seed cake which consists of highly toxic constituents i.e. phorbol esters, trysin inhibitors, phytate, etc. Due to these anti-nutritional factors, it is inedible both in food and feed. On the other side, jatropha seed cake also consists of crude protein (43.48 ± 0.83%), carbohydrates (32.54 ± 0.12%), ash (8.50 ± 0.07%), crude fiber (5.73 ± 0.07%) and ether extract (1.54 ± 0.09%) (Sanchez-Arreola et al., 2015). Owing to these constituents, it can be used as a substrate for the production of many microbial products. It has been reported as a potential substrate for pullulan production by A. pullulans in submerged fermentation (Choudhury, Sharma, & Prasad, 2012). A cost-effective technology was developed using jatropha seed cake as a nutrient for production of pullulan in a laboratory scale fermenter.

3.1.15. Palm kernel Palm trees are the tropical and sub-tropical plants with leaves and fruits on the top of unbranched stems. Palm fruits have three parts i.e. the outer thin layer on the jelly-like pulp of the fruit with seed kernels in the center core. During the processing of palm fruits, the kernels of fruits are disposed as waste. Palm kernel consists of total fermentable sugars of (7.15 ± 0.25%) including mannose (6.74 ± 0.25%) and glucose (0.29 ± 0.003%) (Shukor et al., 2016). These also contains crude protein (14.5 ± 2.5%), crude fibre (13.0 ± 5%), ether extract (5.0 ± 2.5%), ash (6.5 ± 3%), etc. (Alimon, 2015). Palm kernels are quite cheap and properly chopped dried palm kernels can be used as substrate for pullulan production by A. pullulans in solid-state fermentation. Pullulan production has been reported highest in Asian palm kernel medium supplemented with yeast extract with initial pH 6.5 and moisture content 50% in solid-state fermentation (Sugumaran, Sindhu, Sukanya, Aiswarya, & Ponnusami, 2013). The statistical optimization of Asian palm kernel based medium at flask level has increased pullulan production by almost 50% (Sugumaran, Shobana, Balaji, Ponnusami, & Gowdhaman, 2014). The extract of palm kernel has also been reported for pullulan production in submerged fermentation with improved yield of pullulan (Durgalakshmi, Ponnusami, & Sugumaran, 2014).

3.2.3. Soybean pomace Soybean beans have high protein content and the processing of soybean for soy sauce, generates a byproduct known as soybean pomace. It contains high sodium chloride content and is discarded as waste, resulting in serious environmental problems. The pomace consists of proteins (33.4%), carbohydrate (17.2%), fat (8.1%), ash (29.4%), calcium (0.4%) and phosphate (0.5%) (Jin et al., 2002). Since it is a rich source of carbohydrates and proteins, its disposal is a huge loss of natural resources. Soybean pomace has been used as a nitrogen source for the production of high molecular weight (1.32–5.66 × 106 Da) pullulan (7.5 g/L) by A. pullulans (Seo et al., 2004). The direct supplementation of soybean oil in sucrose based medium also augments the pullulan yield (29.58 g/L) in submerged fermentation (Sena, Costelli, Gibson, & Coughlin, 2006). The soya flour hydrolyzed extract has also been used for production of pullulan (125.7 g/L) by A. pullulans in shake-flask fermentations (Sheoran, Kumar, Tiwari, & Singh, 2012). In brief, various agro-industrial wastes (liquid/solid) can be used as potent carbon or nitrogen substrates for pullulan production in submerged/solid-state fermentations. This is an environment friendly as well as an economical approach for cost-effective production of valueadded products. The agro-industrial wastes are rich in complex nutrients and need to be pretreated before their utilization in the fermentation process. A number of novel approaches in pretreatment of agro-industrial wastes are used depending on the composition and type of waste. A specific pretreatment method used for an agro-industrial

3.1.16. Jackfruit seed Jackfruit is an evergreen tree cultivated in tropical region. Among the fruits, jackfruits are the largest in size. The pulp of jackfruit can be used in food and the seeds left behind as waste constitute 10–15% of total fruit weight (Swords, Bobbio, & Hunter, 1978). The seeds of jackfruit consist of carbohydrate (79.34 ± 0.06%), proteins (13.50 ± 0.06%), fibre (3.19 ± 0.01%), ash (2.70 ± 0.02%), and crude fat (1.27 ± 0.01%) (Swami, Thakor, Haldankar, & Kalse, 2012). 53

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on tablets and minimizes the damage of final products during storage (Chaen, 2009). Pullulan can also be used as a thickener and texture improver. It is used in the preparation of smooth and viscous food products like dressings and seasonings. Pullulan solutions are clear and colorless, so it can be used as fillers in various beverages and sauces. The colorless solution of pullulan can be further molded into films and coatings. Pullulan solutions form clear films which are oxygenimpermeable, oil resistant and have good mechanical properties (Singh & Kaur, 2015; Yuen, 1974). Owing to these unique properties, pullulan films can be used as versatile and novel packaging materials. The oxygen impermeability of pullulan films prevents the oxidation of fat and vitamins containing food products. As pure pullulan films are considered edible and have the ability to dissolve quite quickly in water, they can be used as edible food coatings which can be cooked along with the food item and when consumed it readily dissolves in the mouth (Conca & Yang, 1993). Pullulan films have the ability to suppress the growth of microbial flora and retain the moisture content of food (Debeaufort, Quezada-Gallo, & Voilley, 1998). In addition, pullulan films can also be used as the packaging material of various food items e.g. fruits, vegetables, poultry, meat, dried fish, cashew nuts, peanuts, noodles, confectionaries, etc. (Chaen, 2009; Krochta & De MulderJohnston, 1997). The applications of pullulan blended films and coatings for packaging are tabulated in Table 4.

waste may not be appropriate to other agro-industrial wastes. The pretreatment method should be simple and cost-effective. 4. Applications of pullulan in food industries Pullulan is one of the industrially important exopolysaccharide, which possesses potential applications in food industries. It is an edible polymer without any toxicity or carcinogenicity. Pullulan is declared safe by Food and Drug Administration in the United States for use in food applications and has GRAS (Generally Regarded As Safe) status (FDA, 2002). It is also listed in the Japanese Standards for Ingredients for Drugs and extensively used in Japan as a food additive and glazing agent with oxygen-barrier properties (Ministry of Health & Welfare, 1993). Pullulan is not easily assimilated by bacteria, molds, and fungi. It can be mixed with a range of food or non-food materials to enhance the shelf-life of products which protect them from degradation (Table 3). It is a low-calorie sugar which can be easily used for the production of low-calorie foods (Yatmaz & Turhan, 2012). Owing to its low-calorie property, pullulan can be used for supplementation of dietary fibers (Oku, Yamada, & Hosoya, 1979; Yoneyama et al., 1990). It can also be used as a replacement for starch for preparation of low-calorie food products like doughnuts, cookies, and biscuits (Chaen, 2009; Hiji, 1986; Hijiya & Shiosaka, 1975a). It can even counterfeit the characteristics of starch derived foods e.g. dispersibility and consistency of the final product. Pullulan has higher moisture retaining property than starch which prevents drying of the food products (Hiji, 1986; Hijiya & Shiosaka, 1975b; Kato & Shiosaka, 1975). It can maintain the freshly cooked texture of ready to eat foods. The addition of pullulan in the making of cakes helps in retaining the shape, moisture, and appearance of the final product. The presence of pullulan in frozen foods prevents the water loss or drip and even improves the production yield in some food products (Chaen, 2009). Pullulan is known to be resistant to the mammalian amylases. It can function as prebiotic and promote the bifidobacteria growth to benefit the health of consumer (Mitsuhashi, Yoneyama, & Sakai, 1990; SugawaKatayama, Kondou, Mandai, & Yoneyama, 1994; Yoneyama et al., 1990). Pullulan is reported as an antifungal agent and it inhibits the fungal spoilage of food products (Yuen, 1974). It can be used for the preparation of maltotriose syrup (Singh, Saini, & Kennedy, 2010a; Singh, Saini, & Kennedy, 2010b; Singh, Saini, & Kennedy, 2011). Human enzymes can slowly digest pullulan and gradually convert it into glucose, so it can be incorporated in dietetic snack foods designed for diabetic patients who have impaired glucose tolerance (Wolf, 2005). Pullulan has low viscosity (Tsujisaka & Mitsuhashi, 1993) and solution making properties (Buliga & Brant, 1987; Kato, Okamoto, Tokuya, & Takahashi, 1982; Kawahara, Ohta, Miyamoto, & Nakamura, 1984; Nishinari et al., 1991). The viscosity of pullulan is not affected by the addition of sodium chloride, heating and changes in pH. Owing to these properties, pullulan can be used to impart viscosity and gloss to the food products with high salt concentration, e.g. barbecue sauce, soya sauce, pickled fruits, and vegetables. Pullulan and its derivatives exhibit good adhesive properties and can be used as a binder in food products (Hijiya & Shiosaka, 1975a; Miyaka, 1979). It can be used to bind nuts on cookies, sesame seeds on the rice cracker surface and used for the preparation of snack foods like fish sticks and beef or pork sheets (Chaen, 2009). Due to low viscosity property, pullulan solution can be sprayed on the dried powdered food products for easy granulation and to enhance the solubility of the product in water (Tsujisaka & Mitsuhashi, 1993). It can also be used as a stabilizer and protective glaze in various food products. It can be used to stabilize the fatty emulsions, quality, and texture of mayonnaise (Yamaguchi & Sunamoto, 1991). It can form a clear icing membrane or glaze on frozen food products. The coating of pullulan solution on fish and shellfish prevents any damage due to freezing, i.e. cracks during storage and discoloration. It also improves the adhesive properties of sugar coatings

5. Conclusions A huge amount of agro-industrial waste is generated everyday and its direct disposal causes severe environmental problems. The agro-industrial wastes have high nutritive values and are rich in the organic and inorganic matter. These wastes should be explored for production of pullulan at industrial scale. Pullulan has unique physicochemical properties and is declared safe for its use in food products. The potential applications of pullulan in food items are mostly identified and acknowledged, but they are not explored at industrial scale. The future challenge is to outline pullulan applications at industrial level and dictate the successful penetration of pullulan in the food market. References Alhaique, F., Matricardi, P., Di Meo, C., Coviello, T., & Montanari, E. (2015). Polysaccharide based self-assembling nanohydrogels: An overview on 25-years research on pullulan. Journal of Drug Delivery Science and Technology, 30, 300–309. Alimon, A. R. (2015). The nutritive value of palm kernel cake for animal feed. Palm Oil Developments, 40, 12–14. Amartey, S., & Jeffries, T. W. (1994). Comparison of corn steep liquor with other nutrients in the fermentation of D-xylose by Pichia stipitis CBS 6054. Biotechnology Letters, 16, 211–214. An, C., Ma, S.-j., Chang, F., & Xue, W.-j. (2017). Efficient production of pullulan by Aureobasidium pullulans grown on mixtures of potato starch hydrolysate and sucrose. Brazilian Journal of Microbiology, 48, 180–185. Arapoglou, D., Vlyssides, A., Varzakas, T., Haidemenaki, K., Malli, V., Marchant, R., et al. (2009). Alternative ways of potato industries waste utilisation. Proceedings of the 11th international conference on environmental science and technology, B54–B61. Bambalov, G., & Jordanov, P. (1993). Production of pullulan polysaccharide from wineproducing wastes. Scientific Works HIFFI-BG, 40, 229–240. Barnett, C., Smith, A., Scanlon, B., & Israilides, C. J. (1999). Pullulan production by Aureobasidium pullulans growing on hydrolysed potato starch waste. Carbohydrate Polymers, 38, 203–209. Boa, J. M., & LeDuy, A. (1984). Peat hydrolysate medium optimization for pullulan production. Applied and Environmental Microbiology, 48, 26–30. Boa, J. M., & LeDuy, A. (1987). Pullulan from peat hydrolyzate fermentation kinetics. Biotechnology and Bioengineering, 30, 463–470. Buliga, G. S., & Brant, D. A. (1987). Temperature and molecular weight dependence of the unperturbed dimensions of aqueous pullulan. International Journal of Biological Macromolecules, 9, 71–76. Campbell, B. S., Siddique, A. B. M., McDougall, B. M., & Seviour, R. J. (2004). Which morphological forms of the fungus Aureobasidium pullulans are responsible for pullulan production? FEMS Microbiology Letters, 232, 225–228. Carrington, A. K., Goff, H. D., & Stanley, D. W. (1996). Structure and stability of the glassy state in rapidly and slowly cooled carbohydrate solutions. Food Research International, 29, 207–213. Cerqueira, D. A., Filho, G. R., & Meireles, S. (2007). Optimization of sugarcane bagasse cellulose acetylation. Carbohydrate Polymers, 69, 579–582. Chaen, H. (2009). Pullulan. In A. Imeson (Ed.). Food stabilizers, thickners and gelling agents

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