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Biosurfactants from Fungi: A Review

Garima Bhardwaj1, Swaranjit Singh Cameotra2 and Harish Kumar Chopra1*
1Department of Chemistry, Sant Longowal Institute of Engineering and Technology, Longowal - 148106, Sangrur, Pubjab, India
2Institute of Microbial Technology, Sector-39-A, Chandigarh-160036, India
Corresponding Author : Harish Kumar Chopra
Professor, Department of Chemistry
Sant Longowal Institute of Engineering and Technology
Longowal - 148106, Sangrur, Pubjab, India
Tel: 91-1672-305204
Fax: 91-1672-280072
E-mail: [email protected]; [email protected]
Received September 17, 2013; Accepted November 08, 2013; Published November 16, 2013
Citation: Bhardwaj G, Cameotra SS, Chopra HK (2013) Biosurfactants from Fungi: A Review. J Phylogenetics Evol Biol 4:160. doi:10.4172/2157-7463.1000160
Copyright: © 2013 Bhardwaj G, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Biosurfactants are the surfactants of microbial origin. They offer so many advantages over their synthetic counterparts due to their biodegradable and environmental friendly nature, that’s why gaining much more attention in creating the era of green technology. Their applications range from cosmetic, pharmaceutical and food processes as emulsifiers, humectants, preservatives, detergents etc. The present review deals with the production, purification, characterization and applications of various fungal biosurfactants.

Biosurfactants; Sophorolipids; Fungi; Purification; Characterization
Biosurfactants are structurally and functionally diverse amphiphilic, surface active compounds which lower the surface and interfacial tension between individual molecules at respective surfaces and interfaces. Thus, these are very important in the living systems and can be regarded as the backbone of the biological membranes which promise the transport and exchange of the various important materials [1,2]. Biosurfactants are ecologically safe and can be applied in bioremediation processes. The microorganisms which produce biosurfactants can also be used in the various bioremediation technologies like solubilisation and removal of oil from contaminated soil, sludge in oil storage tank etc. [3]. The most important example of this is in Microbial Enhanced Oil Recovery (MEOR) which is an ecofriendly petroleum recovery process [4].
Variety of bacteria and few fungi are reported to produce biosurfactants using renewable sources [5,6]. Higher yields of 120 and 40 g/L of fungal surfactants has been reported using carbon sources like tallow fatty acid residues, animal fat, glycerol and oleic acid [7-9]. Furthermore fungi yield a good amount of biosurfactant when compared to bacteria. The reason may be presence of rigid cell wall in them [10]. The higher yield seems to make their use possible at industrial level and replacement of surfactants by biosurfactants.
Fungi Producing Biosurfactants
Where the field of production of biosurfactants by bacterial species is well explored, relatively fewer fungi are known to produce biosurfactants. Among fungi, Candida bombicola [11-14,7,8], Candida lipolytica [15,16], Candida ishiwadae [17], Candida batistae [18], Aspergillus ustus [19], Ustilago maydis [20] and Trichosporon ashii [21] are the explored ones. Many of these are known to produce biosurfactant on low cost raw materials. The major type of biosurfactants produced by these strains is sophorolipids (glycolipids). The structure of sophorolipids produced by Candida batistae [18], Candida bombicola [22] and Candida sp. SY16 [10] are given in Figure 1.
Patents on fungal biosurfactants
Due to wide industrial applications many authors have claimed for patents on biosurfactants. Some of the important patents in the last few years are listed in Table 1.
Physicochemical Parameters Affecting the Biosurfactant Production
The production of biosurfactants by the use of various culture conditions is an important aspect because a small alteration in the composition of important nutrients leads to the modification of the resulting biosurfactant. The various physicochemical factors are discussed as follows:
Carbon sources
Carbon source plays an important role in the growth as well as production of biosurfactants by the various microorganisms and it varies from species to species. When only one from glucose and vegetable oil was used for the production of biosurfactant by Torulopsis bombicola, a very low yield of biosurfactant was obtained but when both carbon sources were supplemented together yield increased to 70 g/L [23]. While at the concentration of 80 and 40 g/L of glucose and soybean oil, the maximum yield of sophorose lipids was obtained by Torulopsis bombicola [24], even higher yields of 120 g/L sophorolipids was produced with Candida bombicola in 8 days, when sugar and oil were used as carbon sources [13]. When canola oil and glucose were used as the carbon sources by Candida lipolytica, in the concentrations of 10% each, maximum yield of sophorolipids (8 g/L) was obtained [15]. Also, when the industrial residue were used for the production of biosurfactant by Candida lipolytica, yielded 4.5 g/L of protein-lipidcarbohydrate complex with the reduction in surface tension of distilled water from 71 to 32 mN/m [16]. Although with Candida lipolytica higher production of bioemulsifier was obtained, when supplemented with 1.5% glucose (w/v) [25]. Candida antarctica and Candida apicola yielded 13.4 and 7.3 g/L of sophorolipids respectively, when soap stock was supplemented in 5% v/v concentration [26]. The resting cells of Pseudozyma (Candida antarctica) was able to covert C12 to C18 n-alkanes into Mannosylerythritol Lipids (MEL), the yield of MEL was 140 g/L after 4 weeks and the produced biosurfactant was able to emulsify soybean oil [27]. The modification in the fatty acid constitution of final biosurfactant was observed when the fatty acid composition was changed in the fermentation media of Candida ingens [28].
Nitrogen sources
This is the second most important supplement for the production of biosurfactants by microorganisms. Various organic and inorganic nitrogen sources were used in the production of biosurfactants. The higher yields of sophorose lipids, biosurfactant by the fungi Torulopsis bombicola and Candida bombicola were observed using yeast extract and urea as the nitrogen source [13,8,24]. Although, the higher yields of mannosylerythritol lipid by Candida sp. SY16, Candida lipolytica and Candida glabrata UCP 1002 were observed with ammonium nitrate and yeast extract [10,29,15,16].
pH plays an important role in the production of biosurfactants. Candida species produced maximum yields of biosurfactants in a wide pH range, as seen in Candida glabrata UCP 1002 which produced maximum biosurfactant at pH 5.7, Candida sp. SY16 at pH 7.8, Candida lipolytica at pH 5.0, Candida batistae at pH 6.0 [29,10,30,18]. While Aspergillus ustus and Pichia anamola produced maximum yield of biosurfactant at the pH 7.0 and 5.5 respectively [19,31].
Various microbial processes are temperature dependent and get affected by a little change. The most favorable temperature for the production of biosurfactants by various fungi is 30°C as observed in various Candida species viz. Candida sp. SY16, Candida bombicola, Candida batistae and Torulopsis bombicola [10,8,18,23]. While, in case of Candida lipolytica, 27 °C was found to be the best temperature.
Incubation time
Incubation time also have a significant effect on the production of biosurfactant. Different microorganisms are able to produce biosurfactants at different time intervals. The maximum biosurfactant production by Aspergillus ustus MSF3 was observed after 5 days of incubation while in case of Candida bombicola, the incubation periods were 7, 8 and 11 days [7,13,12]. Also, the maximum biosurfactant production by Candida bombicola using animal fat was observed after the 68 h of incubation [8].
Purification and Analytical Methods for the Characterization of Biosurfactants
After the production of biosurfactants the most important step is their purification from the fermentation media so as to make them available for various industrial applications. This section deals with the purification and characterization methods employed for the extraction of biosurfactants from various fungal species. The purification and analytical methods for the characterization of fungal biosurfactants are given in Table 2.
Characterization of Biosurfactants by Various Chromatographic and Spectroscopic Techniques
For the complete structure elucidation of biosurfactants, various chromatographic and spectroscopic techniques were used. A combination of these techniques is very helpful in the characterization of the compound. These techniques are discussed as follows:
Thin layer chromatography (TLC)
This is the most important and preliminary technique for the characterization of various types of biosurfactants. The various solvent systems and developer employed in thin layer chromatography are given in Table 3.
Gas chromatography- mass spectroscopy (GC-MS)
In the structure elucidation of sophorolipids by Candida batistae, for the confirmation of fatty acids, the sample was investigated for GC-MS analysis. The major peak at Retention Time (RT) 51.5 min. was supposed due to be 18-hydroxyoctadecenic acid and this was confirmed by comparing the sample with the authenticated sample produced by Starmerella bombicola. The Fragmentation pattern of the sample were observed at m/z 312 [M] + (relative intensity, 1.3); m/z 294 [M-H2O] + (relative intensity, 2.4), m/z 31 [CH2CH=CH2] + (relative intensity, 52). In addition to the major peaks additional peaks were also observed (e.g. m/z 31, m/z 55, m/z 67, m/z 81, m/z 95, m/z 110, m/z 123, m/z 137, m/z 151, m/z 165, m/z 213, m/z 237, m/z 262 and m/z 280). The major peak for the standard sophorolipids was observed at 36.9 min. and this reveals the presence of 17-hydroxyoctadecenic acid. The Fragmentation pattern of the standard peak were observed at m/z 312 [M] + (relative intensity 0.6), m/z 294 [M-H2O] + (relative intensity, 18), m/z 45 [CH3-CH=OH] + (relative intensity, 57). Here, also the additional peaks were observed (e.g. m/z 29, m/z 55, m/z 67, m/z 81, m/z 95, m/z 109, m/z 123, m/z 137, m/z 151, m/z 165, m/z 213, m/z 265 and m/z 279) [18]. For the structure elucidation of monoacylglycerols produced by Candida ishiwadae, the fatty acid moieties methyl oleate and linoleyl of the compounds (a & b) having Retention Factor (Rf) values 0.23 and 0.17 was determined by the methanolysis. From the combined data of 1H-NMR and mass spectral data, the compounds (a & b) were determined to be 1-oleylglycerol and 1-linoleylglycerol. Further confirmation was done from their molecular weights, 356 and 354 [17]. In the structure elucidation of sophorolipids produced by the Candida bombicola, hydroxyl-acid methyl esters were liberated by the methanolysis and were confirmed by GC-MS. The 16-hydroxydecanoic acid was confirmed by comparing the fragmentation pattern with the standard 16-hydroxyhexadecanoic acid purchased from Sigma Aldrich. Also, an isomer 15-hydroxyhexadecanoic acid was confirmed because of the availability of the same fragmentation pattern in the library [12].
High performance liquid chromatography (HPLC) and Liquid chromatography-mass spectroscopy (LC-MS)
In the structure elucidation of mannosylerythritol lipid from Candida sp. SY16, the acid hydrolysate of glycoside gave two spots on TLC at Rf values 0.38 and 0.46 respectively and corresponded to D-mannose and meso-erythritol. Also, in the HPLC chromatogram the peaks at RT 10.5 and 7.8 min. corresponded to D-mannose and meso-erythritol respectively. The molar ratio of D-mannose and mesoerythritol was calculated by integration of HPLC peak areas against the known concentrations of the authenticated standards and hence calculated to be 1:1 [10]. The comparative studies of sophorolipids from two carbon sources soybean and glucose by Pichia anamola were done. The HPLC of the biosurfactant from glucose and soybean medium showed the peaks at retention time of 9.269 (m/z 675.687, 691.880 and 708.062) and 9.779 min. (m/z 659.499, 675.627 and 691.830). These were compared with the standard sophorolipids sample having a peak at RT of 9.646 (m/z 648.760 and 650.816). The comparative study is given in Table 4 [31] .
Proton nuclear magnetic resonance spectroscopy (1H-NMR)
In the 1H-NMR spectrum of sophorolipids produced by Starmellela bombicola, the duplet at 1.20 ppm was assigned as –CH3 at ω-end of fatty acid (C-18) and the sextet at 3.74 ppm was assigned as hydroxylated methine group (-CHOH-) at ω-1 position (C-17). While, the sophorolipids produced by Candida batistae showed two multiplets at 3.58 and 3.80 ppm and were assigned as the hydroxylated methylene group (-OCH2-) at ω-end of fatty acid (C-18) [18]. For the structure elucidation of monoacylglycerols produced by Candida ishiwadae, the compounds with Rf values 0.23 and 0.17 were subjected for 1H-NMR. For Rf 0.17, the five protons at δ 3.5-4.2 corresponded to the carbinol protons which indicated the presence of glycerol moiety. The glycerol moiety contains a substituent at –OH group attached to Cl-atom as indicated by high values at δ 4.10 and 4.18. Also, the additional protons at δ 0.9-2.5 and two olefinic protons at δ 5.38 suggested the presence of monounsaturated fatty acid moiety. Also, for the Rf value 0.23 the compound elucidated was monoacylglycerol with an additional double bond [17]. For the structure elucidation of mannosylerythritol lipid by Canida sp. SY16, the protons resonating at 5.45, 4.93, 4.26 and 4.44 ppm confirms the acylation positions of sugar moiety. They had lower chemical shifts in comparison to the lipid-free sugar moiety protons which resonate at 4.00, 3.62, 3.72 and 3.88 ppm. The triplet at 0.90 ppm and singlet at 2.08 was assigned due to methyl (-CH3), broad peak at 1.28-1.40 ppm was assigned due to –CH2- groups in fatty acids, multiplet at 5.30-5.38 ppm was assigned =CH2- in unsaturated fatty acids [10].
Carbon nuclear magnetic resonance spectroscopy (13C-NMR)
In 13C-NMR spectrum of sophorolipids produced by Starmellela bombicola, peak at 20.7 were assigned as the ω-end carbon (C-18) and the one at 77.4 ppm were assigned as ω-1 carbon (C-17) of fatty acid respectively. While the peak at 69.7 ppm in the 13C-NMR spectrum of sophorolipids produced by Candida batistae was assigned as the ω-end carbon (C-18) [18]. In the structure elucidation of mannosylerythritol lipid from Candida sp. SY16, peaks at 23.7-33.1 ppm were assigned as –CH2- groups in fatty acids and peaks at 128.8, 129.7, 130.2 and 131.1 ppm were assigned as four =CH- groups in unsaturated fatty acids [10].
Biosurfactants have numerous applications in the bioremediation processes, food industries, cosmetic industries and biomedical fields. The various reported applications of the fungal biosurfactants are as follows:
Microbial enhanced oil recovery and cleaning of oil tanks
The Sophorolipids from Candida lipolytica and Candida bombicola are very promising in the cleaning of oil tanks, decontamination of polluted areas, microbial enhanced oil recovery, industrial cleaning, low-end consumer products and house-hold applications [16,7]. The biosurfactants from Torulopsis bombicola and Aspergillus ustus MSF3 were used for the release of bitumen from the contaminated soil and for the degradation of hydrocarbons [23,19]. Mannosylerythritol lipids from Candida antarctica have potential applications in the removal and biodegradation of hydrocarbons in oil-contaminated soil and were also used to rinse oil and grease from the contaminated soil [27,55].
Food and oil industry
Biosurfactants are able to stabilise various types of emulsions, so are valuable for the food industry. The biosurfactants from the Candida lipolytica and Saccharomyces cerevisiae are good choices for the food and oil industries [15] further, the biosurfactant from Saccharomyces cerevisiae used as a single cell protein [56]. The bioemulsifier, liposan from Candida lipolytica was able to stabilize the emulsions of vegetative oils and water. It was also able to stabilize the cottonseed oil, corn oil, soybean oil and peanut oil emulsions [57-60].
Biomedical field
The biosurfactants are extensively useful in the biomedical fields. They possess significant anti-biological activities. The biosurfactant from the Aspergillus ustus MSF3 have significant antimicrobial activity against the Candida albicans and gram-negative bacterium [19].
Cosmetic industry
The biosurfactants are capable of their usage in the cosmetic industry due to their skin friendly properties. Sophorolipids from the mutant strain Candida bomobicola ATCC 22214 have great uses in the cosmetic industries due to their anti-radical properties, stimulation of fibroblast metabolism and hygroscopic properties to support healthy skin physiology [14].

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