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1. Introduction
Biosurfactants (BSs) could be found on the surface of microbial cell and transferred into the extracellular space by multiple filamentous fungi, and yeast (Starmerella, Candida, Ustilago, Saccharomyces, Trichosporon, and Pseudozyma) and bacteria (Nocardia, Rhodococcus, Acinetobacter, Arthrobacter, and Gordonia) [1]. They are primarily classified according to their structural characteristics, associated microorganisms, and molecular weight (MW) [2].
BSs have a hydrophobic region and a hydrophilic end consisting of hydrocarbons acids, diverse fatty acids (saturated, unsaturated, linear, or branched long-chain) and carbohydrate cyclic peptide, alcohol, carboxylic acid, amino acid, and phosphate. This amphipathic framework provides an ability to reduce the surface tension at the interfaces of phases with divergent polarities, which includes emulsion (liquid-liquid) and suspension (liquid-solid), which is collectively named “dispersion” [3, 4]. BSs have also the capacity to produce molecular aggregates, for example, micelles, like the ones patented at the critical micelle concentration (CMC). The CMC of BSs is normally 1–200 mg/L, which is 10–40 times lower than that formed with chemical surfactants [5].
BSs are produced through microbial fermentation, which includes yeast, fungi, and bacterial strains (Pseudomonas, Lactobacillus, Acinetobacter, Halomonas, Rhodococcus, Bacillus, Enterococcus, and Arthrobacter). Among all microbes, genus Bacillus is well studied for its biosurfactant production as it produces various types of cyclic lipopeptides/lipoproteins such as lichenysins, bacillomycin, fengycins, and surfactins [6].
Lipopeptides and glycolipids are highly efficient and popular group of BSs such as surfactin and rhamnolipids, with low-MW [7–9], whereas the high-MW BSs are lipoprotein, phospholipids, and emulsion [10, 11]. Lipopeptide BSs are composed of two different regions: an acyl tail (s) and a short linear oligopeptide sequence, containing an amide bond. The hydrophobic tail contains a hydrocarbon chain, whereas the hydrophilic head contains the lipopeptide BSs peptide sequence. The peptide module includes cationic and anionic residues, as well as nonproteinaceous amino acids [12].
Taking into account the unique properties of Bacillus cyclic lipopeptides, and their applications in medicine, healthcare, environment, agriculture, and food industries, their biocompatibility, bioavailability, and structural diversity attracted further attention in the last decade [13–15]. The nonribosomal peptide synthetase (NRPS) enzyme is associated with the formation of cyclic lipopeptides. Lipopeptide surfactants are classified according to their structure, with isoforms comprising a variety of D and L amino acids [16, 17]. The demand for new lipopeptides is increasing in order to broaden their application. Earlier, various studies have been conducted to establish the biotechnological production, functional qualities, and physical properties of lipopeptide surfactants. In this review article, a comprehensive study is carried out to describe the contributions of Bacillus lipopeptides in the food industry and biological activities.
2. Classes of Lipopeptides Produced by Bacillus spp
Lipopeptides are a subgroup of microbial surfactants, for example, surfactin, fengycin, iturin, lichenysin, and kurstakin [18]. The types or classifications of lipopeptides surfactants are mainly based on the amino acid sequences and various strains of Bacillus spp. producing lipopeptides such as B. subtilis, B. cereus, B. thuringiensis, B. globigii, B. amyloliquefaciens, B. megaterium, B. pumilus, and B. licheniformis. [19–22] (Table 1 and Figure 1).
Table 1
Lipopeptide-producing strains and their applications.
| Lipopeptides | LP-producing bacterial strain | Biological application | Ref. |
| Surfactin | B. methylotrophicus DCS1 | Antioxidant, antimicrobial, and antiadhesive activities | [23] |
| B. mojavensis A21 | Diesel biodegradation | [24] | |
| B. mojavensis PRC101 | Antagonism against Fusarium verticillioides (fungal species infecting maize) | [25] | |
| B. subtilis | Inhibitory activity against phytopathogenic Fusarium sp. | [26] | |
| B. atrophaeus L193 | Aphicidal activity against the aphid Rhopalosiphum padi (pest in cereal crops) | [27] | |
| B. subtilis SAS-1 B. amyloliquefaciens BR-15 | Engine oil degradation efficiently augmented (75–94%) | [28] | |
| B. subtilis SPB1 | Antioxidant activity, chelating activity, histological study proved effective treatment of complicated wound healing and skin diseases | [29] | |
| B. subtilis strain ATCC6633 | Microbial enhanced oil recovery | [30] | |
| B. subtilis 573 | Decreased viability of breast cancer cell lines, T47D and MDA-MB-231 and nontumor fibroblast cell line (MC-3 T3-E1) | [31] | |
| B. natto TK-1 | Therapeutic agent, anti-inflammation | [32] | |
| B. subtilis ANR 88 | Effective in the synthesis of silver as well as gold nanoparticles | [33] | |
| B. pumilus | Silver nanoparticles produced as antimicrobial and nematicide | [34] | |
| B. subtilis LSFM-05 | Nontoxic dispersion in biotechnology and nanotoxicology. | [35] | |
| Surfactin A | B. (SPB) NH-100 and NH-217 | Biocontrol agent against bakanae diseases in rice | [36] |
| B. stratosphericus sp. A15 | Antioxidant and antibacterial activity, wound healing activity by connective tissue regeneration, thickened epidermal layer, and keratinocyte formation | [37] | |
| Pumilacidin | B. stratosphericus FLU5 | Hydrocarbon removal from contaminated soil, negligible cytotoxic effect against the mammalian cells HEK293 | [38] |
| Lipopeptide | B. subtilis SPB1 | Anti-obesity effect through the inhibition of lipid digestive and liver dysfunction enzymes | [39] |
| Iturin A, fengycin | B. amyloliquefaciens DSM 23117 | Biocontrol agent against a common fungal phytopathogen botrytis cinerea | [40] |
| Bacillomycin D | B. amyloliquefaciens fiply 3A | Killing human cancer cell line viz. A549 (alveolar adenocarcinoma), A498 (renal carcinoma) and HCT-15 (colon adenocarcinoma) while not effecting the normal cell line L-132 (pulmonary epithelial cells) | [41] |
| Iturin A | B. subtilis | Inhibiting chronic myelogenous leukemia in vitro via paraptosis, apoptosis, and inhibition of autophagy | [42] |
| Lipopeptide | B. mojavensis ifo 15718 | Pharmaceutical applications as it possesses antibacterial activity against pathogen S. aureus and lack of toxicity to PC12 and PBMC cells | [43] |
| Iturin A | B. amyloliquefaciens PPCB004 | Activity against postharvest fungal pathogens on stored fruits | [44] |
| Fengycin | B. amyloliquefaciens FZB42 | Antifungal activity against fusarium moniliforme (rice bakanae disease), fusarium oxysporum (root rot) and trichoderma atroviride (ear rot and root rot) | [45] |
| Surfactin homologs | B. amyloliquefaciens MD4-12 | Synergistic Antimicrobial effects against various gram-positive and Gram-negative bacteria | [46] |
| B. subtilis NH 217, B. amyloliquefaciens FZB42 | Excellent biofilm formation, antifungal activity against various phytopathogen and their associated diseases | [47] | |
| Bacillomycin, Fengycin | B. methylotrophicus XT1 CECT 8661 | Effective biocontrol agent against B. cinerea infection, antioxidant triggerer in different fruits | [48] |
| Iturin A, Fengycin C | B. Subtilis EA-CBOO15 | Iturin A inhibited M. fijiensis mycelial growth, and fengycin C displayed strong inhibitory activity on ascospore germination | [49] |
| Iturin A, surfactin | B. Subtilis | Broad hypocholesterolemic activities, immune-modulators, toxins, and enzyme inhibitors | [50] |
| Surfactin, Fengycin | B. subtilis fmbj (CGMCC no. 0934) | Effective against Newcastle disease virus (NDV) and infectious bursal disease virus (IBDV) | [51] |
| Lichenysin | B. licheniformis VS16 | Biofilm inhibition, removal of heavy metals | [52] |
| B. licheniformis Ali5 | Enhanced oil recovery and motor oil removal from contaminated sand | [53] | |
| B. licheniformis W16 | Excellent emulsification and microbial enhanced oil recovery | [54] | |
| Surfactin | B. subtilis C9 | Effective biocontrol agent controlling cladoceran grazers in algal cultivation system | [55] |
| Lipopeptide biosurfactant | B. pseudomycoides OR 1 | Biocontrol agent against food-borne pathogens E. coli (MTTC 43), Klebsiella pneumoniae (MTVV 530) and staphylococcus aureus (MTCC 96) | [56] |
| Novel cyclic lipopeptide C18 | B. pseudomycoides BS6 | Bioremediation and recycling waste cooking oil | [57] |
| Pumilacidin | B. safensis CCMA-560 | Thermal stable and microbial enhanced oil recovery | [58] |
| Lipopeptide | B. sp. H20-1 | Antagonistic effect against sulfate-reducing bacteria | [59] |
| Lipopeptide | B. cereus UCP1615 | Bioremediation of petroleum derivative in soil and water with above 90% removal | [60] |
| Paenibacterin | Paenibacillus elgii HOA73 | Effective bio-pesticide against diamondback moth Plutella xylostella (destructive insect pest) | [61] |
| Paenibacterin | Paenibacillus thiaminolyticusOSY-SE | Minimized endotoxemia showed low toxicity against human kidney sell line (ATCC CRL-2190) | [62] |
| Lipopeptide | B. altitudinis MS16 | Promising emulsification and antifungal activity | [63] |
| Lipopeptide | B. brevis | Excellent emulsifier and antibacterial effects | [64] |
| Lipopeptide | B. subtilis SPB1 | Toothpaste formulation | [65] |
[figure(s) omitted; refer to PDF]
2.1. Surfactin
Surfactin belongs to the lipopeptides family, which was firstly isolated by Arima et al. in 1968 and produced by many Bacillus with surfactant activities [66]. Surfactin (1036 Da) is an amphipathic cyclic lipopeptide biosurfactant produced by many strains of the bacterial genus Bacillus. The surfactin molecule was firstly screened from the culture media of B. subtilis strains and applied as a clotting inhibitor [67, 68].
Surfactin is composed of a heptapeptide (ELLVDLL) along with chiral sequence LLDLLDL linked with β-hydroxy (fatty acid chain) of carbon chain (C12–C16) and forms a close cyclic lactone ring structure. The structure of surfactin consists of both hydrophobic (located at 2–4, 6, and 7) and hydrophilic (located at 1 and 5) part [69]. Surfactin displays a stable and conserved folding in aqueous solutions, and negatively charged amino acids, Glu and Asp, exhibit polar domain. Moreover, it is also soluble in organic solvents, for example, dichloromethane, ethanol, chloroform, butanol, and methanol [70].
The peptide part represents topology like “horse-saddle” and is called the β-sheet structure in the backbone folding, which believe that these structural traits contribute to the broad spectrum of biological properties of surfactin [71, 72].
Naturally, many isoforms of surfactin present, which only differ with their physicochemical properties such as (1) type of amino acid of peptide ring at 2nd, 4th, and 7th positions, and (2) branching of hydroxyl fatty acid moiety and chain length. What’s more, isoforms also depend upon the Bacillus strain and other factors such as media, environmental, and nutritional conditions of substrate [73, 74]. Previously, studies reported that surfactin shows potent antitumoral, antiviral, anticoagulant, inhibitors of enzymes, and antimicoplasma activities [75].
2.2. Lichenysin
Lichenysin a lipopeptide produced most of B. licheniformis strains, and it has excellent surfactant and chelating agent for Ca2+ and Mg2+ [76–79]. Lichenysin was also reported to exert antimicrobial, anti-inflammatory, antitumor, and immunosuppressive properties. Besides good biological activities, it also has hemolytic activity [79]. These traits of lichenysin are caused by the amphiphilic nature of the lipopeptide. Structurally, lichenysin consists of amino acids (7) and a β-hydroxy fatty acid along with C12–C17 carbon atoms. Many isoforms of lichenysin are present in nature, for example, lichenysin A [80–82]. The structure of lichenysin is very similar to surfactin and differs with the substitution of glutamine with glutamic acid in the first amino acid position [82]. However, this small difference markedly increases the surfactant properties of lichenysin [79].
2.3. Kurstakin
Kurstakin is a low-molecular-weight lipopeptide mainly produced and isolated from Bacillus thuringiensis kurstakin HD-1. The amino acid sequence of kurstakin was reported as follows: Thr-Gly-Ala-Ser-His-Gln-Gln. The fatty acyl chain of kurstakin is linked with N-terminal amino acid residue by amide bond, and every lipopeptide consists of lactone linkage among carboxyl terminal amino acid and hydroxyl group in the side chain of the serine residue [83, 84].
2.4. Iturin
Iturin are an important class of lipopeptides with a molecular mass of ∼1.1 kDa. Iturin A consists of two parts: (a) C14–C17 (amino fatty acids) and (b) seven amino acid residues (heptapeptides; Asn-Tyr-Asn-Gln-Pro-Asn-Ser). Iturin (D and E) varies from iturin A due to the presence of a free carboxyl group in iturin D and carboxymethyl group in iturin E. The structure of iturin shows that it has an amphiphilic character [85, 86]. Iturin molecule is of great interest because of their biological activities and physicochemical traits and used in oil, pharmaceutical, and food industries. Almost all strains of Bacillus subtilis produce iturin lipopeptide, and its operon ranges from 38 to 40 kb in size and contains four open reading frames such as ItuA, ItuB, ItuC, and ItuD [87]. Iturin lipopeptide also contains mojavensin, mycosubtilin, bacillomycin D, bacillomycin F, and bacillomycin L, which differ in amino acid sequences of the heptapeptides [88]. Iturin was reported to exert potent antifungal activity against, Botrytis cinerea, Alternaria alternate, and Penicillium expansum. Moreover, it also has strong surface activity and destabilizing effect [89].
2.5. Fengycins
Fengycins are lipopeptides mainly produced by the genera of Bacillus and Paenibacillus. Fengycins have strong antifungal activity and markedly affect filamentous fungi [90]. Fengycins are decapeptides and C14–C19 to β-hydroxy fatty acid chain, which showed potent antifungal activity [91, 92]. There are two subclasses of Fengycins, namely, Fengycin A and Fengycin B, that only differ from each by the amino acid attached at position 6. Fengycin B contains Val at position 6, whereas Fengycin A contains Ala. Fengycins (A and B) were firstly reported in B. subtilis strain by Vanittanakom et al. [93]. The closely related fengycin type was reported and named plipastatin due to the position of amino acids L- Tyr and D- Tyr [94].
3. Production, Isolation, and Characterization of Bacillus Lipopeptides
Lipopeptide surfactants are produced by many microbes including bacteria, fungi, and yeast. However, herein, we mainly focus on the production of Bacillus lipopeptides. The biosurfactants are synthesized from the extracellular or intracellular part of microbes. Notably, biosurfactants are produced during the stationary and exponential phase, whereas the biosurfactant production is predominate in the death phase. Reduction in surface tension to 8 mJm−2 is the minimum value to be considered when producing the biosurfactant. The various strains of Bacillus spp. produced novel lipopeptides such as B. licheniformis, and B. circulans. Furthermore, details of lipopeptide production from various Bacillus along with fermentation conditions are presented in Tables 1 and 2.
Table 2
Strategies and mechanisms used to enhance lipopeptide production by Bacillus sp.
| Strategy used | Factors evaluated | Strain | Results | BS nature | Ref. |
| RSM, CCD | Brewery waste and (carbon, nitrogen, agitation speed, temperature, pH) | B. subtilis N3–1P | 657 g.l−1 | Surfactin | [95] |
| RSM, BBD | (d-glucose, sucrose, xylose), hydrocarbons (hexadecane, diesel, benzene, heptane), nitrogen source (NaNO3, NH4NO3, (NH4)2SO4, NaHCO3, urea) | Bacillus sp. SS105 | 2.65 g.l−1 | Surfactin | [96] |
| CCD, PBD | Sucrose, glucose, starch, peanut oil, potato), nitrogen source (peptone, beef extract, trypsin, yeast extract), other variables (MgSO4, KCl, KH2PO4, FeSO4.6H2O, NH4Cl, MnSO4, CuSO4, sodium glutamate) | B. subtilis N7 | 0.706 g.l−1 | Surfactin | [97] |
| RSM, PBD, (TFAT) two factors at time | Nitrogen source ((NH4)2SO4, KNO3, NaNO3, NH4Cl, beef extract, yeast extract) | B. subtilis KLP2015 | 0.98 g.l−1 | Surfactin | [98] |
| RSM, OFAT one factor at a time | Carbon source (glucose, fructose, sucrose, xylose, rhamnose, soluble starch), nitrogen source (NH4Cl, C6H17N3O7, urea, peptone, soybean meal), metal ions (ZN2+, Fe3+, Mg2+, Mn2+, Ca2+, K+) | Bacillus sp. BH072 | 0.027 g.l−1 | IturinA A | [99] |
| OFAT | Single and multidose Fe2+ | B. megaterium | 4.2 g.l−1 | Surfactin | [100] |
| 22 factorial design, RSM | Glucose and yeast extract | B. subtilis EA-CB0015 | 0.78, 0.355 g.l−1 | Fengycin, Iturin A | [101] |
| PBD, CCD | Carbon source (glucose, maltose, dextrose, mannitol, sorbitol, galactose, xylose, starch), nitrogen source (KNO3, (NH4)2SO4, NaNO3, soy flour, peptone, casein hydrolysate, yeast extract urea) | B. amyloliquefaciens MD4-12 | 1.25 g.l−1 | Surfactin | [102] |
| CCD, Fed-batch strategy | Fed-batch strategy (pH-stat, DO-stat, constant rate feeding, combined feeding), Sunflower oil, NaNO3, MgSO4.7H2O, yeast extract | Aneurinibacillus thermoaerophilus HAKO1 | 11.2 g.l−1 | Surfactin | [103] |
| ANN-GA | Glucose, urea, SrCl2, and MgSo4 | B. circulans MTCC 8281 | 4.38 g.l−1 | Unidentified | [104] |
| ANN-GA | Lp concentration, Ca2+, pH | B. licheniformis, B. megaterium | 45% oil recovery | Lipopeptide | [105] |
| BBD | Glucose, glutamic acid, temperature, NaCl | B. mojavensis 14 | 4.12 g.l−1 | Lipopeptide | [106] |
| BBD | Optimization of non-nutritional factors (inoculum age and size, pH, agitation, aeration, temperature) | B. subtilis SPB1 | 3.3 g.l−1 | Lipopeptide | [107] |
| Media composition and characteristics | Nitrogen source ((NH4)2SO4, KNO3, NH4NO3, NH4Cl, peptone, beef extract, yeast extract), carbon source (glucose, sucrose, fructose, maltose, sorbitol, starch) | B. velezensis KLP2016 | 2.5 g.l−1 | Lipopeptide | [108] |
| n-paraffin, n-dodecane, n-hexadecane, sunflower oil, canola oil, sucrose, glycerol, diesel fuel, n-tetradecane, nitrogen source ((NH4)2SO4, NaNO3, KNO3, urea, peptone, yeast extract, beef extract), metal and sulfur source (FeSO4, MnSO4, MgSO4), and C/N ratio, pH | Paenibacillus sp. D9 | 4.11 g.l−1 | New lipopeptide | [109] | |
| Different culture media, shaking speed of shaker, liquid and solid fermentation, attapulgite powder | B. natto NT-6 | 1.94-fold increased | Iturin A, surfactin | [110] | |
| Different culture media, vine-trimming shoots, glucose, hemicellulosic hydrolysate, and cellulosic hydrolysate | B. tequilensis ZSB10 | 1.52 g.l−1 | Lipopeptide | [111] | |
| Taguchi method | Carbon source (sucrose, whey, crude oil)), NaCl, Na2HPO4, NaH2PO4, and (NH4)2SO4 | B. cereus | 1.8 g.l−1 | Lipopeptide | [112] |
| Use of cheap substrate/raw material | Carbon source (orange peel, citrus medica peels, banana peels, and potato peels), inoculum size, incubation time, temperature, substrate concentration | B. licheniformis KC710973 | 1.796 g.l−1 | Lichenysin | [113] |
| (Butter milk, poultry-transforming waste flour, inoculum size), submerged fermentation | B. subtilis SPB1 | 12.61 g.l−1 | Lipopeptide | [114] | |
| Corn steep liquor (CSL), iron, manganese, and magnesium | B. subtilis #573 | 4.8 g.l−1 | Surfactin | [115] | |
| Potato peels, temperature, pH, saline conditions | B. pumilus DSVP18 | 3.2 g.l−1 | Iturin A | [116] | |
| Grape seed flour | B. amyloliquefaciens C5 | 0.80 g.l−1 | Bacillomycin D | [117] | |
| Distiller grains (DGS, coculture fermentation with B. B. amyloliquefaciens X82 | B. amyloliquefaciens MT45 | 3.4 g.l−1 | Surfactin | [118] | |
| Palm oil, waste glycerol, immobilized on chitosan | Bacillus Sp. GY 19 | 9.8 g.l−1 | Lipopeptide | [119] | |
| Solid state fermentation (SSF) | Soybean flour, rice straw, starch, yeast extract, kinetic parameters (iso- and nonisothermal process, isothermal and nonisothermal process in fermenter) | B. amyloliquefaciens XZ-173 | (55.83 mg/gds) | Lipopeptide | [120] |
| Soybean flour, rice straw, glycerol, maltose, pH, water content, inoculum size, fermentation time, temperature | B. amyloliquefaciens XZ-173 | 15.03 mg/gds | Surfactin | [121] | |
| Wheat bran, rice straw, soybean flour, temperature, pH, water content, inoculum size | B. subtilis CCTCCM207209 | 70.90 mg/gds | Lipopeptide | [122] | |
| Rice bran husk, sunflower oil, coconut oil cake, cotton oil cake, corn cob, orange peel, jackfruit peel, sugarcane leaf, pineapple peel, banana leaf, cheese whey, dry yeast cells, pongamia seed cake, jatropha seed cake ground oil cake, glucose with MSM | B. amyloliquefaciens | 3-fold increased | Iturin A | [123] | |
| Olive leaf residue flour, olive cake flour | B. subtilis SPB1 | 0.3067 g.l−1 | Lipopeptide | [124] | |
| Mutagenesis induced enhanced yield | UV and gamma ray-induced mutagenesis | B. subtilis HS0121 | 2-fold increased | Surfactin | [125] |
| Random mutagenesis using gamma irradiation | B. subtilis UTB1 | 1.8-fold increased | Iturin A | [126] | |
| UV irradiation, nitrosoguanidine, and ion beam mutagenesis | B. amyloliquefaciens ES-2-4 | 10.3-fold increased | Lipopeptide | [127] | |
| Combination of UV irradiation and nitrous acid treatment | B. subtilis SPB1 | 2-fold increased | Lipopeptide | [51] | |
| Genome shuffling | Genome shuffling | B. amyloliquefaciens FMB38 | 2-fold increased | Surfactin | [128] |
| Genome shuffling and gene (fenA) expression | B. amyloliquefaciens ES-2-4 | 8.30-fold increased | Fengycin | [129] | |
| Mutagenesis (UV, nitrosoguanidine, atmospheric, and room temperature plasma) | B. amyloliquefaciens LZ-5 | 2.03-fold increased | Iturin A | [130] | |
| Protoplast fusion | B. mojavensis JF-2 | 0.382 g.l−1 | Lipopeptide | [131] | |
| Recombinant strains for higher yield | Surfactin promoter THY-15 was replaced to THY-15/pg3-srfA. Then introduced a Vitreoscilla hemoglobin (VHb) gene into engineered strain to obtain a novel THY-15/pg3-srfA (VHb) | B. subtilis THY-15 | 10.02 g.l−1 | Surfactin C15 | [132] |
| Loc gene expressed, the fosmid N13 with whole Loc gene screened from B. velezensis 916 genomic library, the cassette fused with IPTG inducible promoter Pspac induced in the fosmid N13 resulted N13+spec and N13+PSSpec transformed to obtained derivative strains FZBNPLOC and FZBPSLOC | B. velezensis FZB42 | 15-fold increased | Locillomycins | [133] | |
| Enhanced transcription of iturin A biosynthetic genes was implemented by inserting a strong promoter C2up into upstream of the itu operon, fermentation optimization using RSM and furthermore, overexpression of pleiotropic regulator DegQ | B. amyloliquefaciens LL3 | 8-fold increased | Iturin A | [134] | |
| Cloning of the biosurfactant genes sfp, sfp0, sfpA into BioS a, BioS b, BioS c, recombinant strains after cloning of biosurfactant genes in to E. coli. (E. coli DH5ά) | B. subtilis SK320 | 2-fold increased | Lipopeptide | [135] | |
| Wild type, overexpression of THY-7-Pgrac-ycxA, overexpression of THY-7-Pgrac-krsE, overexpression of THY-7-Pgrac-yerP | B. subtilis 168 | 0.55, 1.15, 0.93, 1.67 g.l−1 | Surfactin | [136] | |
| Using CRISPRi 20 genes were repressed, yrpC, racE, murC genes were inhibited individually. Furthermore, combination inhibition of bkdAA and bkdAB genes | B. subtilis | 4.69-fold increased | Surfactin | [137] | |
| Replacement of PsrfA with Pg3 | B. subtilis | 0.55–9.74 g l−1 | Surfactin | [138] | |
| Insertion of sfp gene from Paenibacillus sp. D9 into E. coli | Paenibacillus sp. D9 | 3-fold increased | Paenibacterin | [139] |
3.1. Substrates
Many substrates mainly consist of hydrophobic mixtures, vegetable oils, waste products, dairy products, etc. and are used for the production of lipopeptide-based surfactants. To minimize the production cost of lipopeptide-based surfactants, renewable and low-cost substrates were applied as presented in Tables 1 and 2. Moreover, it is also necessary to select substrates with a high nutritional value for the growth of microbes. One of the best methods used is to apply organic matter such as industrial waste, oil substrate, and agro-based materials. Interestingly, these waste materials provide distinct energy source for microbes with effective surfactants production.
3.2. Production of Biosurfactants by Using Agro-Industrial Waste
Agro-industrial waste is an ideal choice for the production of lipopeptide and helps in the industrial waste management. Agro-industrial wastes contain both carbon and lipids along with other necessary nutrients, which are the major requirement for the growth of biosurfactant-producing microbes. Previously, many researchers successfully utilized various agro-industrial wastes such as sugarcane molasses, date molasses, cassava flour, rice straw, corn, fruits and vegetable wastes, bran, and others for the production of biosurfactant [115, 140–146].
Molasses is the key waste product of sugar and date industries, and it has gained a lot of attention for the production of biosurfactant. This popularity to use as a substrate for biosurfactant production is mainly due to its low cost and rich source of dry matter (75%), protein (2.5%), nonsugar organic matter (9–12%), minerals (potassium, calcium, phosphorus, and magnesium), and other components (thiamine, biotin, inositol, and pantothenic acid). The sugar content in the molasses ranges from 48 to 56%, making it ideal for the growth of various microorganisms [147–149].
Makkar and Cameotra [150], Saimmai et al. [142], and Joshi et al. [151] reported the biosurfactant production from Bacillus subtilis strains (MTTCC 2423, MTCC1427, and SA9) and Bacillus licheniformis TR7) by using molasses as carbon source. In another study, Joshi et al. [54] documented that cane molasses and date molasses used as a carbon source enhance the production of lichenysin-A-like lipopeptide by using Bacillus licheniformis W16. Rane et al. [33] conducted a study to utilized agro-industrial wastes (molasses, banana peels, orange peels, whey, potato peels, and bagasse) as a substrate for the production of biosurfactant by Bacillus subtilis ANR 88. Their study results revealed that biosurfactant production in the molasses substrate as a carbon source was higher (0.24 g/L) compared to other agro-industrial wastes. Moreover, they also found that by optimizing the conditions (ammonium ferric citrate 0.25%, molasses 4%, and pH 7), the yield of biosurfactant significantly increases to 2-fold (0.513 g/L).
Recently, Al-Dhabi et al. [141] used date molasses as a carbon source for the production of biosurfactant from Bacillus subtilis strain Al-Dhabi-130. They found that using date molasses as a carbon source yields the biosurfactant to 74 mg/g substrate and can be used for the large-scale production of biosurfactant .
Peanut oil cake is a novel agro-waste, which can be used for the production of lipopeptide. Nalini et al. [152] reported that maximum lipopeptide production was obtained (8.18 g) from peanut oil cake as a substrate by using B. cereus strain SNAU01. Paraszkiewicz et al. [153] also observed that lipopeptide surfactants such as surfactin and iturin can be produced by Bacillus strains using carrot peel as substrate.
3.3. Production of Lipopeptides by Using Oil Waste
Wastes from oil processing industries represent one of the best and readily available renewable substrates for microbial biosurfactant production. The hydrophobic substrate containing media such as oil helps microbes to produce lipopeptide surfactant. Sunflower, olive oil, coconut oil, and canola are the main oil made from oil industries and considered the best carbon source for biosurfactant production [22, 38, 143, 154].
Ostendorf et al. [143] reported the excellent production of lipopeptide biosurfactants by Bacillus stratosphericus strain FLU5 using waste vegetable oils (olive oil, corn oil, and residual frying oil). In another study, Md Badrul Hisham et al. [155] observed the excellent yield of surfactin by Bacillus sp. HIP3 when using used cook oil as a substrate (2%).
4. Isolation, Purification, and Characterization of Lipopeptides
Lipopeptides are mostly synthesized by bacterial genus Bacillus. The bacterial cells are grown in their respective media with specific conditions (varied from strains to strains) to produce lipopeptides prior to their separation by centrifugation. Malfanova et al. [156] grew bacterial cells (60 h at 28°C) subjected to centrifugation (13,000 rpm for 10 min) to obtain crude lipopeptides. The obtained supernatant was acidified by using HCl acid, while the precipitate was extracted with methanol and further concentrated by vacuum evaporation [156, 157]. The crude extract was purified by many methods such as gel filtration in Sephadex column and high-performance liquid chromatography, and the collected eluent was further subjected to MALDI-TOF-MS/LC-MS/MS-MS/NMR/FTIR [53].
5. Pharmacological Activities
5.1. Anticancer
Bacillus lipopeptides are considered versatile bioactive compounds with potent antitumor activity. For example, surfactin has been documented to exert antitumor activity towards human colon carcinoma cell lines (HCT15 and HT29), Ehrlich’s ascites carcinoma cells, and breast cancer cell lines (T47D and MDA-MB-231) [31, 104, 158]. Surfactin inhibits the growth of transformed cells via cell cycle arrest and induction of apoptosis and suppresses ERK (extracellular-signal-regulated kinase) and PI3 K/Akt pathway [158]. In another study, Liu et al. [159] reported that surfactin-like lipopeptides purified from B. subtilis Hs0121 exert cytotoxicity towards Bcap-37 breast cancer cells (IC50: 29 ± 2.4 μM). Surfactin was also documented to inhibit the LoVo colon cancer cells (IC50: 26 μM) [158] (Figure 2). What’s more, Wang et al. [160] observed that B. subtilis natto T-2 with crude cyclic lipopeptides (CLPs) showed a cytotoxic effect against human K562 leukemia cells. Surfactin was also reported to exhibit the cytotoxic effect on hepatocellular carcinoma [159, 160]. Recently, Hong et al. [161] have reported that five Surfactin isomers produced by B. pumilus HY1 during Cheonggukjang fermentation markedly inhibited the growth of two cancer cell lines (MCF-7 and Caco-2).
[figure(s) omitted; refer to PDF]
Fengycin, a lipopeptide produced by various strains of B. subtilis, was reported to exert strong anticancer activity on colon cancer cell line HT29 and human lung cancer cell line 95D [162, 163]. Similarly, Bacillus lipopeptide (iturin) was also reported to possess a broad spectrum of anticancer activity on several cell lines (e.g., HepG2, Caco-2, BT474, MDA-MB-231, MCF-7, HUVEC, BIU-87, BRL-3A, A549, and K562 cells [42, 164–171].
5.2. Hemolytic Activity
The lipopeptide surfactants induce the hemolysis of human erythrocytes due to their detergent effect and membrane forming ability. Therefore, lipopeptide surfactants are used as potent inhibitors of fibrin clot formation. Arima et al. [172] reported for the first time that the surfactin potently inhibits the fibrin clot formation via abrogating the conversion of fibrin monomer into fibrin polymer. Bernheimer and Avigad studied the inhibition of fibrin clot formation and hemolysis of erythrocyte by subtilysin derived from B. subtilis since 1970 [173] (Figure 2).
The hemolytic activity of lipopeptide iturin A was studied by Aranda et al. They documented that iturin dependently exerts hemolytic activity on human erythrocytes. The underlying mechanism of action was that iturin A induced hemolysis via colloid-osmotic mechanism and K+ leakage followed by hemoglobin release [85]. In another study, Dehghan-Noudeh et al. [174] documented that B. subtilis ATCC 6633-derived lipopeptide surfactant attenuated potent hemolytic effect in comparison with chemical surfactants such as hexadecyl trimethyl ammonium bromide, sodium dodecyl sulfate, tetradecyl trimethyl ammonium bromide, and benzalkonium chloride.
5.3. Anti-Inflammatory
Previously, it was reported that lipopeptides exert anti-inflammatory activities via several pathways such as modulation of the TLR4 (Toll-like receptor 4), inhibition of lipoteichoic acid (LTA)-induced NF-κB, activator of transcription-1 (STAT-1), interaction with cytosolic phospholipase A2 (PLA2), and increase in the phosphorylation of STAT-3 [88] (Figure 3).
[figure(s) omitted; refer to PDF]
Moreover, it also impairs the antigen-presenting function of macrophages, suppresses the LPS-induced expression of cluster of differentiations (CD40, CD54, CD80), and inhibits the activation of CD4+ T-cells [32, 88].
It was also documented that surfactin markedly inhibits the overproduction pro-inflammatory mediators (IL-6, tumor necrosis factor alpha or TNF-alpha, and interleukin beta or IL-1β), prostaglandin E2, monocyte chemoattractant protein-1, NO, and reactive oxygen species (ROS), and suppresses the expression of MMP-9 (matrix metallopeptidase 9), COX-2 (cyclooxygenase-2), and iNOS (inducible nitric oxide synthase) [175].
5.4. Antibacterial Activity
The demand for new antimicrobial agents significantly increases due to the resistance of pathogenic microorganisms towards already present antimicrobial drugs. Surfactin, a lipopeptide, was reported to exert antibacterial activity against various pathogenic bacteria. Beside surfactin, other Bacillus-related lipopeptides were also reported to possess well-known inhibitory activity towards the growth of pathogenic bacteria [176–179].
Huang et al. [178] reported that surfactin and fengycin produced by the strain B. subtilis fmbj effectively inactivate endospores of B. cereus. The lipopeptide mainly damages the surface structure of the spores. B. velezensis strain H3-isolated surfactin isoforms were reported to active against P. aeruginosa, St. aureus, Klebsiella pneumoniae, and Mycobacterium [179].
In another study, fengycin isoforms isolated from marine Bacillus strain markedly inhibited the growth of various bacteria such as K. aerogenes, Citrobacter fruendii, Micrococcus flavus, Proteus vulgaris, Alcaligenes faecalis, E. coli, and Serratia marcescens [180].
Lipopeptide antibiotic subtulene A isolated from the culture filtrate of B. subtilis SSE4 was reported to inhibit the growth of Gram-positive and Gram-negative bacterial strains such as Stenotrophomonas maltophilia, Enterobacter cloacae, and Xanthomonas campestris [181]. Fengycin and surfactin lipopeptides containing culture filtrate of the endophytic B. amyloliquefaciens was reported to potently inhibited the growth of all tested Gram-negative ones except Ochrobactrum anthropi and all Gram-positive bacteria tested except B. [157].
Recently, a study conducted by Lv et al. [177] has also reported that B. amyloliquefaciens C-1 fermentation supernatant contains a mixture containing surfactin and fengycin, which inactivate the growth of Clostridium difficile (bacteria that can infect the bowel and cause diarrhoea). Iturin analog isolated from Bacillus strain was reported to inactivate the growth of Xanthomonas arboricola and Pseudomonas syringae [176].
5.5. Antifungal and Biocontrol
It has been documented that Bacillus lipopeptides exert a wide array of antifungal activities. Briefly, iturin markedly inhibits the growth of nematophagous fungi, wood-staining fungi, Aspergillus flavus, Penicillium roqueforti, and Colletotrichum demiatium [19, 182–186], whereas fengycin was reported to inhibit the Fusarium graminearum, Botrytis cinerea, and Podosphaera fusca [187, 188].
More detailed investigations conducted by various researchers reported that lipopeptides exert morphological changes such as hyphal swellings, changed organization of mitochondria, decreased intracellular pH, esterases, and mitochondria activities, and decreased hydrophobicity of the hyphae [48, 189].
Desmyttere et al. [190] conducted a study to explore the antifungal activities of lipopeptides isolated from B. subtilis against apple scab disease causing Venturia inaequalis strains. Their study results revealed that Bacillus subtilis lipopeptide mixtures containing (fengycin, surfactin, and mycosubtilin) markedly inhibited the growth of V. inaequalis S755 and V. inaequalis rs552.
Han et al. [191] documented that B. amyloliquefaciens L-H15-derived peptides (iturin A with C15β-amino fatty acid and cyclic peptide with a molecular weight of 852.4 Da) exhibited strong antagonism against Fusarium oxysporum, Rhizoctonia solani, and Phytophthora capsici.
Dimkić et al. [176] studied five different lipopeptide-producing strains of Bacillus (SS-10.7, SS-12.6, SS-13.1, SS-27.2, and SS-38.4), and their extracts were further tested against Pseudomonas syringae pv. aptata (P16) and Xanthomonas arboricola pv. juglandis (301, 311, and 320). The results revealed that Bacillus strains mostly produced kurstakins, iturins, surfactins, and fengycins lipopeptides. Moreover, they reported that ethyl acetate extracts exert more favorable effect on phytopathogens.
Botrytis cinerea is a necrotrophic fungi, which infects more than 200 plant species including fruits and vegetables. Toral et al. [48] conducted a study to determine anti-B. cinerea activity of lipopeptides isolated from Bacillus XT1 CECT 8661. They observed that lipopeptide-rich extract mainly containing surfactin, bacillomycin, and fengycin potently inhibits the growth of B. cinerea. What’s more, SEM (scanning electron microscope) and TEM (transmission electron microscope) analysis revealed that lipopeptides alter the morphology of the phytopathogen.
5.6. Antiviral Activity
It has been well documented that lipopeptides such as surfactin possess a broad spectrum of antiviral activity against SARS-CoV-2, herpes simplex virus (HSV-1 and HSV-2), Newcastle disease virus, Semliki Forest virus, murine encephalomyocarditis virus, Simian immunodeficiency virus, vesicular stomatitis virus, transmissible gastroenteritis virus, porcine parvovirus feline calicivirus, pseudorabies virus, and bursal disease virus, porcine epidemic diarrhoea virus, and viral hemorrhagic septicemia virus. The chemical structure of surfactin lipopeptide, for example, length of the carbon chain, makes it fit for the inactivation of various viruses [51, 192–194]. Moreover, it was also observed that surfactin more significantly inactivates the enveloped viruses such as herpes viruses and retroviruses compared with nonenveloped viruses [195]. This may be due to the physicochemical interaction among membrane active property of surfactin and the virus lipid membrane [196]. Surfactin permeates into the lipid bilayer and results in the complete disintegration of the envelope containing the viral proteins involved in virus adsorption and penetration to the target cells [195].
5.7. Antiadhesion and Antibiofilm
Surface adhesion and biofilm formation are the mechanisms by which most of bacteria are used for their survival. Lipopeptides have the potential to decrease the interfacial tension and surface of biofilms. In numerous ways, lipopeptides disrupt the membrane structure. For example, surfactin gets inserted into the lipid bilayers, chelates monovalent and divalent cations, solubilizes the fluid phospholipid phase, and modifies the membrane permeability [197]. Surfactin may form voltage-independent channels in biofilms, and these channels disturb the membrane integrity and permeability, leading to membrane disruption [13, 198]. Iturin isoform (mycosubtilin) produced by B. subtilis interacts with membranes via its sterol alcohol group and exhibits resistance to fungi [199]. B. circulans strain showed antiadhesive property towards many bacteria species [200]. Similarly, various Bacillus strains inhibit biofilm formation [6, 78–80].
5.8. Others
Bacillus lipopeptides were also reported in wound healing and oral care products [65]. Zouari et al. [29] documented how the B. subtilis SPB1 biosurfactant supplementation improves the liver function, hyperlipidemia, and hypertriglyceridemia in high-fat-high-fructose (HFHF) diet-fed rats. In another study, the same research group also observed that B. subtilis SPB1 biosurfactant treatment improves the renal functions and inhibits angiotensin I-converting enzyme (ACE) in HFHF diet-fed rats [39]. Moreover, B. subtilis strain containing surfactin was shown to effectively kill the larval and pupal stages of mosquito species, for example, Aedes aegypti, Culex quinquefasciatus, and Anopheles stephensi [195].
6. Lipopeptide Applications in Food
Lipopeptides have well-defined antiadhesive, antibacterial, antiviral, and anticancer properties, ensuring their role in the cosmetics, pharmaceutical, and even food industries. Lipopeptides are mainly employed as surfactants in the food industry. Moreover, rhamnolipids and surfactins are positively exploited in the baking industry, providing good texture, volume, and product stability. They are also used to promote the emulsification process in the fat tissue to regulate fat globule agglomeration. Certain lipopeptides derived from Enterobacter cloacae have recently been presented into the food market with their high emulsifying characteristics owing to the potential to improve viscosity even at extreme acidic conditions. In terms of economic growth, the most significant increases in food additives have been seen in emulsifiers and hydrocolloids that were up to 10.5% and 6.0%, respectively.
The vulnerability of biologically active peptides as an antimicrobial agent in the food preservation is rare due to their limits to proteases. The usage of ring-structured peptides like lipopeptides, on the other hand, can prevent this susceptibility. There are two types of lipopeptides: a cyclic heptapeptide acylated with β-amino fatty acids that have a chain length of C14–C16, and the fengycin group containing a β-hydroxy fatty acid with uncommon amino acids including allo-threonine and ornithine. They also consisted of cyclic heptapeptide that makes a lactone linkage with β-hydroxy fatty acids. They are enzyme-insensitive (particular protease), suppressing the development of a broad variety of pathogenic fungi (Fusarium graminearum, Rhizoctonia solani, and Aspergillus flavus) as well as postharvest pathogens such as Botrytis cinerea and Penicillium expansum.
Gandhi and his coworkers revealed that the rhamnolipid emulsifier with a concentration of 0.10% significantly improved the texture, moisture content, and appearance of muffins for longer periods. Surfactin inclusion in many fermented food products, like natto, a Japanese soybean meal, is extremely favorable for acceptance as an ingredient or addition. Juola et al. [201] determined the surfactin content of various natto types. Notably, the greatest concentrations discovered were close to 2.2 mg/g, which corresponds to 80–100 mg surfactin per 50 g natto. Additional research is required to establish the surfactant’s recommended daily intake (RDI) to pronounce it harmless and is usually considered to be a generally recognized as safe (GRAS) organism. Therefore, surfactin has strong potential to be used in the food sector.
Zouari et al. [202] prepared the cookies using sesame peel flour partially replaced with white wheat flour. When additional sesame peel flour was employed, the characteristics such as toughness, water content, and spread factor had been degraded. Interestingly, adding 0.1% B. subtilis SPB1 biosurfactant significantly enhanced the textural profile, even when compared to the standard surfactant glycerol monostearate [202]. In another research, the possible lipopeptides from Bacillus spp. reduced the Ochratoxin and A. carbonarius that were found in the processing of wine-making [203]. In the wine-making process, the concentration of Ochratoxin should not surpass 2.0 μg/L as it is a carcinogenic mycotoxin. Additionally, this compound has a detrimental effect on yeast fermentation behaviour. Lipopeptides also had higher antifungal capabilities than SO2 and stimulated yeast growth as well as the generation of esters and acids that are involved in the olfactory profile [203].
7. Conclusion
Lipopeptides are very useful molecules due to their multiple applications. Most Bacillus lipopeptides have been applied in food, cosmetic, biotechnology, pharmaceutical industries, where emulsifying, antimicrobial, and surfactant properties are used. The application and production of lipopeptides are very promising trend; however, the high cost of production makes them unfit for large-scale synthesis. Furthermore, even though there are many reports displaying the thrombolytic, antitumor, and anti-inflammatory activity of lipopeptides, the few numbers of clinical trials warrant more significant efforts. In future, extensive studies should be carried out to verify previously published author findings, which further help with the utilization of these miracle compounds. In summary, Bacillus lipopeptides have strong potential application in various fields and a lot of work will be needed to formulate strategies for improved large-scale biosynthesis of lipopeptides.
Acknowledgments
The authors are highly grateful to the “National Key R & D Program of China (2017YFB03089)” and “Open Research Program of Beijing Advanced Innovation Center for Soft Matter Science and Engineering” for the support and research grants.
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Abstract
Biosurfactants are a functionally and structurally heterogeneous group of biomolecules produced by multiple filamentous fungi, yeast, and bacteria, and characterized by their distinct surface and emulsifying ability. The genus Bacillus is well studied for biosurfactant production as it produces various types of lipopeptides, for example, lichenysins, bacillomycin, fengycins, and surfactins. Bacillus lipopeptides possess a broad spectrum of biological activities such as antimicrobial, antitumor, immunosuppressant, and antidiabetic, in addition to their use in skincare. Moreover, Bacillus lipopeptides are also involved in various food products to increase the antimicrobial, surfactant, and emulsification impact. From the previously published articles, it can be concluded that biosurfactants have strong potential to be used in food, healthcare, and agriculture. In this review article, we discuss the versatile functions of lipopeptide Bacillus species with particular emphasis on the biological activities and their applications in food.
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Details
; Pang, Zhengjun 2 ; Wang, Fenghuan 1
; Xu, Baocai 1
; El-Seedi, Hesham R 3 1 Beijing Advanced Innovation Center for Food Nutrition and Human Health, Beijing Technology & Business University (BTBU), Beijing 100048, China; School of Light Industry, Beijing Technology & Business University (BTBU), Beijing 100048, China
2 School of Light Industry, Beijing Technology & Business University (BTBU), Beijing 100048, China
3 Pharmacognosy Group, Department of Pharmaceutical Biosciences, Uppsala University, Biomedical Centre, Box 591, SE-751 24, Uppsala, Sweden; International Research Center for Food Nutrition and Safety, Jiangsu University, Zhenjiang 212013, China