Abstract
The increasing influence of human activity and industrialization has adversely impacted the environment via pollution with organic contaminants, which are minimally soluble in water. These hydrophobic organopollutants may be present in sediment, water or biota and have created concern due to their toxic effects in mammals. The ability of microorganisms to degrade pollutants makes their use the most effective, inexpensive and ecofriendly method for environmental remediation. Microorganisms have the ability to produce natural surfactants (biosurfactants) that increase the bioavailability of hydrophobic organopollutants, which enables their use as carbon and energy sources. Due to microbial diversity in production, and the biodegradability, nontoxicity, stability and specific activity of the surfactants, the use of microbial surfactants has the potential to overcome problems associated with contamination by hydrophobic organopollutants.
This review provides an overview of the current state of knowledge regarding microbial surfactant production, mode of action in the biodegradation of hydrophobic organopollutants and biosynthetic pathways as well as their applications using emergent strategy tools to remove organopollutants from the environment. It is also specified for the first time that biosurfactants are produced either as growth-associated products or secondary metabolites, and are produced in different amounts by a wide range of microorganisms.
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Introduction
Increasing anthropogenic activity and industrialization have considerably increased environmental pollution from organic contaminants. Organic pollutants include a wide range of organic xenobiotic chemicals, which are minimally soluble in water and may be present in water, sediment or biota. They include compounds such as plastics, gasoline, paints, adhesives, polycyclic aromatic hydrocarbons (PAHs), benzene, polychlorinated biphenyls, toluene, ethylbenzene and pesticides, among others (Semple et al. 2003; Rasheed et al. 2019; Bhatt et al. 2021). The presence of these hydrophobic organic pollutants in the environment has caused concern due to their toxic effects in mammals, which include mutagenic, carcinogenic and teratogenic effects (Dsikowitzky and Schwarzbauer 2014; Sánchez 2021). In this context, a bioremediation approach using living systems represents an efficient and environmentally friendly strategy to manage pollutants. Microbes are present in diverse habitats, and some have developed extraordinary strategies that allow them to grow and adapt to extreme environments (Sarmiento et al. 2015; Sánchez et al. 2020). Microbial strategies include a powerful enzymatic system composed of stable enzymes produced under extreme conditions and an ability to produce natural surfactants as a means to increase the bioavailability of hydrophobic organopollutants (Kaczorek et al. 2018). These microbial strategies allow microbes to use complex substrates (i.e. hydrophobic organopollutants) as carbon and energy sources. Microbial surfactants (biosurfactants) can be found on the cell surface or are released into the extracellular space (Ward 2010). Biosurfactants provide increased hydrophobicity on the cell surface of the producing microorganisms, which facilitates the access and use of hydrophobic substrates by microbial cells (Perfumo et al. 2009; Satpute et al. 2010; Uzoigwe et al. 2015).
Some microbes secrete biosurfactants only when growing on hydrophobic substrates, whereas others produce these compounds during growth on both hydrophobic and hydrophilic substrates (Gautam and Tyagi 2006). The production of biosurfactants can be affected by growing substrate, temperature, pH, nitrogen and carbon sources (Sanches et al. 2021).
Biosurfactants have advantages in relation to their chemical analogs. Microbial surfactants are biodegradable, have high activity, are nontoxic and are stable under extreme conditions (i.e. pH, temperature and salinity) (Abdel-Mawgoud et al. 2010; Jahan et al. 2020). Therefore, biosurfactants have enormous potential in the development of significant biotechnological processes due to their unique properties (Santos et al. 2016). In addition to bioremediation, biosurfactants are employed in cosmetic formulations, food, biomedicine, pharmaceuticals, and nanotechnology (Jahan et al. 2020; Sanches et al. 2021). Biosurfactants are considered important biomolecules, and their production represents a key technology for development in the current century (Santos et al. 2016).
This review provides, for the first time, an overview of the current state of knowledge about microbial surfactant production, the mode of action in the biodegradation of hydrophobic organopollutants and the biosynthetic pathways of surfactants as well as their applications to hydrophobic organopollutant remediation using emergent strategy tools in a single document. It is also specified that biosurfactants are produced either as a growth-associated or secondary metabolites, and are produced in different amounts by a wide range of microorganisms.
Characteristics and mode of action of microbial surfactants
Microbial surface-active or microbial surfactant compounds are a structurally diverse group of molecules produced by many microorganisms. These compounds contain a hydrophobic component of saturated or unsaturated hydrocarbon chains or fatty acids and a hydrophilic component that includes an acid, peptide anions, cations, or mono-, di- or polysaccharides (Banat et al. 2010). The majority of these compounds are either neutral or anionic; only a few are cationic (e.g. those containing amine groups). In solutions, the shape of the micelles depends on the structure of the component molecules as previously reported (Israelachvili 1992). The size of the hydrophilic moiety in relation to the hydrophobic component has an impact on packing into cylindrical micelles, spherical micelles, inverted micelles or bilayers (Linder et al. 2005). An important chemical-physical parameter of surfactants is the critical micelle concentration (CMC), which refers to the minimum concentration of surfactant necessary to give the minimum surface tension in water and form micelles (Wijaya et al. 2016). The ability to decrease the surface and interfacial tensions is facilitated via the adsorption of the surfactant in different phases, allowing dissimilar phases to mix and interact more easily (Uzoigwe et al. 2015). Therefore, an efficient surfactant has a low CMC, requiring less surfactant to decrease surface tension (Rufino et al. 2014).
Microbial surfactants can be grouped into low molecular mass compounds, known as biosurfactants (glycolipids, lipopeptides) and high molecular mass compounds (lipopolysaccharides, lipoproteins, hydrophobic proteins), known as bioemulsifiers or bioemulsans (Fig. 1) (Rosenberg and Ron 1997; Smyth et al. 2010a, 2010b). Biosurfactants are able to reduce the surface and interfacial tensions between different phases (liquid–liquid, liquid–air, and liquid–solid) until the interface is saturated and micelles begin to form. In contrast, bioemulsifiers or bioemulsans are amphiphilic or polyphilic polymers that are able to efficiently stabilize oil-in-water emulsions; however, they do not substantially reduce surface tension (Smyth et al. 2010b).
Some types of microbial surfactants, which can be grouped into low molecular mass compounds, known as biosurfactants (e.g. glycolipids, lipopeptides, proteins), and high molecular mass compounds, known as bioemulsifiers or bioemulsans (i.e. polymers of lipopolysaccharide proteins or lipoproteins and polysaccharides) (Mondal et al. 2015; Mnif and Ghribi 2015; Dhanya 2021)
Several studies have reported that microorganisms produce their own surfactant (which can be induced) during the degradation of hydrophobic organopollutants (Table 1) or can be produced intrinsically on conventional substrates (e.g. glucose and sucrose), organic materials or organic wastes (Tables 2 and 3). Biosurfactants are generally composed of sugars, fatty acids, amino acids and functional groups such as carboxylic acids (Uzoigwe et al. 2015) and generally have a molecular weight of approximately 0.5–1.5 kDa (Santos et al. 2016). It has been reported that particular class of biosurfactants called hydrophobins, which are produced exclusively by fungi, have a molecular weight of approximately 10–17 kDa (Dąbrowska et al. 2021; Puspitasari et al. 2020; Pothiratana et al. 2020). However, some studies have shown that hydrophobins can have a higher molecular weight (i.e. 19–70 kDa) than those previously reported (Table 4). Several hydrophobins have been isolated from different fungi. These biomolecules are composed of some hydrophobic amino acids and also possess eight Cys residues (Shuren and Wessels 1990; Santacruz-Juarez et al. 2021). Based on their differences in hydrophobic properties, morphology and solubility, hydrophobins are divided in class I and class II. Class I hydrophobins are highly insoluble, while those of class II hydrophobins easily can be dissolved in a variety of solvents (Wessels, 1994) (Table 4).
Most natural surfactants reduce surface tension to approximately 30 mN/m (Table 2). It has been reported that synthetic surfactants such as modified heterogeneous alcohol ether, fatty alcohol methyl esters of ethoxylate and Tween 80 have surface tension values of 29.5, 33.6 and 37.8 mN/m, respectively, at their respective CMC values of 14, 80 and 14 mg/L (Li et al. 2017). Some microbial surfactants have a low CMC and are able to form stable emulsions. It has been reported that the CMCs of biosurfactants generally vary from 1 to 200 mg/L (Mulligan, 2005; Singh et al. 2018); however, recent studies have found higher CMC values for biosurfactants (Tables 1, 2). For example, CMCs of 1200, 1500 and 1700 mg/L have been reported for glycolipids, anionic surfactants, and glycoproteins produced during the degradation of pyrene, burned motor oil and diesel oil by Acinetobacter baumannii (Gupta et al. 2020), Serratia marcescens (Araújo et al. 2017, 2019) and Rhizopus arrhizus (Pele et al. 2019), respectively. However, the CMCs of a hydrophobin and a lipopeptide were 10 mg/L and 12.5 mg/L during the degradation of crude oil by Trichoderma harzianum and Bacillus subtilis, respectively (Nogueira-Felix et al. 2019; Pitocchi et al. 2020).
As shown in Fig. 2, the biodegradation of hydrophobic organopollutants occurs via the formation of a micellar structure with biosurfactants, in which the hydrophilic heads are oriented to the aqueous water stage, and the hydrophobic tails are attached to hydrophobic pollutants, facilitating pollutant adsorption into the microbial cell followed by intracellular enzymatic degradation of the pollutant (Sun et al. 2016; Zhong et al. 2016; Shao et al. 2017) (Fig. 2a). Alternatively, some studies have reported that the biodegradation of hydrophobic compounds takes place once the biosurfactants have surrounded the substrate, allowing microbial attachment and increased substrate availability, and microbial growth and specific enzyme secretion would then allow microbial colonization of the substrate and its degradation (Fig. 2b) (Sánchez 2020, 2021; Dąbrowska et al. 2021).
Schematic illustration of the mechanisms of microbial degradation of hydrophobic organopollutants using biosurfactants: a formation of micelles and incorporation of pollutants inside the microbial cell and b microbial attachment of hydrophobic pollutants
Microbial surfactant production for organopollutant biodegradation
Various levels of biodegradation of organopollutants by biosurfactant producers have been reported, mainly by bacteria from genera such as Pseudomonas, Klebsiella, Meyerozyma, Bacillus, Rhodococcus, Acinetobacter, Staphylococcus, and Achromobacter and from fungal genera such as Trichoderma, Aspergillus, Agrocybe, and Candida (Table 1).
Producers of microbial surfactants have been found in every habitat, including marine environments (psychrotolerant and halotolerant microorganisms) (Zakaria et al. 2019; Trudgeon et al. 2020; Pourfadakari et al. 2021; Cheffi et al. 2020), hydrophobic pollutant-contaminated soils (Ahmadi et al. 2021), wastewater (Nogueira-Felix et al. 2019; Cheffi et al. 2020), freshwater lake ecosystems (Phulpoto et al. 2021), lichens (Santos et al. 2019), and plants (Marchut-Mikolajczyk et al. 2018) (Table 2).
Some studies have reported that biosurfactants are microbial growth-associated products. Sharma and Pandey (2020) reported that B. subtilis RSL2 produced a lipopeptide biosurfactant that was released primarily within the exponential phase when grown on crude oil as a carbon source. Similarly, Datta et al. (2018) found that a lipopeptide (surfactin) produced by B. subtilis MG 495,086 as the primary metabolite reached maximum yield during the exponential phase using light paraffin oil as the carbon source. Moreover, B. subtilis A1 and Bacillus licheniformis AL 1.1 also produced a lipopeptide as a growth-associated metabolite, using sucrose and glucose as carbon sources, respectively (Coronel-León et al. 2015; Parthipan et al. 2017).
However, other biosurfactants such as glycolipids (i.e. rhamnolipids, trehalolipids) have been reported as compounds produced by microorganisms as secondary metabolites. Bacteria such as Acinetobacter calcoaceticus, Enterobacter asburiae and Pseudomonas aeruginosa produced rhamnolipids during their growth on medium containing sodium citrate as a carbon source, enhancing biosurfactant production during the late stationary phase (Hošková et al. 2015). Furthermore, Marinobacter sp. MCTG107b produced a mixture of different rhamnolipids when grown on glucose as a carbon source and were suggested to be secondary metabolites (Tripathi et al. 2019). Moreover, P. aeruginosa was able to produce rhamnolipids as secondary metabolites in a mineral medium containing olive oil (Leite et al. 2016). In addition, Fusarium fujikuroi produced α,β-trehalose containing glycolipid after 7 days of growth in a glucose medium and was reported as a secondary metabolite biosurfactant (Loureiro-Dos Reis et al. 2018). Additionally, Ustilago maydis, Schizonella melanogramma, Candida antarctica, and Geotrichum candidum have been reported to produce mannosylerythritol lipids (glycolipid biosurfactants) as secondary metabolites (Das et al. 2008).
In comparison, hydrophobins are produced by filamentous fungi and have been described as the most effective surface-active proteins (Cicatiello et al. 2016). It has been shown that these biomolecules are expressed at different developmental stages of fungal life, having a role as structural components in fungal growth and in environment-fungal interactions. Therefore, hydrophobins are found in vegetative hyphae, the fruit bodies of mushrooms and spores (Linder et al. 2005).
Biosurfactants can be produced by different microorganisms in different amounts using different substrates. As shown in Table 3, some species such as Aureobasidium thailandense, strains of Pseudomonas aeruginosa and Bacillus pumilus produced surfactants in amounts of approximately 0.09–0.8 g/L using glucose and/or other substrates (Slivinski et al. 2012; Leite et al. 2016; Meneses et al. 2017; Ahmadi et al. 2021). However, some Bacillus species, Stenotrophomonas sp Mucor hiemalis, Aspergillus niger, Rhizopus arrhizus, Fusarium sp, Candida tropicalis, Aureobasidium pullulans and others have been reported to produce between 1 and 10 g/L biosurfactant on a variety of substrates (Table 3) (Qazi et al. 2014; Dhanarajan et al. 2014; Bouassida et al. 2018; Datta et al. 2018; Mendes-de Souza et al. 2018; Saur et al. 2019; Silva-Ferreira et al. 2020; Asgher et al. 2020; Domdi et al. 2020; Patel and Patel, 2020; Phulpoto et al. 2020; Janek et al. 2021). Other studies have shown that bacteria such as Candida sphaerica, Pseudomonas aeruginosa and Starmerella bombicola were able to produce 21, 42 and 51.5 g/L of surfactant, respectively, using organic materials or organic wastes as substrates (Luna et al. 2015; Sodagari et al. 2018; Jadhav et al. 2019). It has been reported that P. aeruginosa produces 240 g/L of rhamnolipids under optimal production conditions using sunflower oil as the substrate (Bazsefidpar et al. 2019). A strain of Starmerella bombicola (strain ATCC 22214) produced 342 g/L surfactant (sophorolipids) using an efficient technology for biosurfactant separation and using corn steep liquor, rapeseed oil and glucose as substrates (Liu et al. 2019).
Studies on hydrophobin production have shown that Aspergillus oryzae produced a hydrophobin, which was extracted from the mycelium pellet using malt extract as the substrate (Puspitasari et al. 2020). Furthermore, Kulkarni et al. (2020) found that Pleurotus ostreatus produced higher amounts of hydrophobin in solid-state fermentation (3.8 mg/g biomass) than in submerged fermentation (1.86 mg/g biomass) using agro-industrial waste oil cakes of coconut and sesame vs. yeast maltose and glucose media, respectively. In addition, hydrophobin was extracted (9.4 mg/g of dry weight) from the fungal biomass of Trichoderma reesei grown on glucose using an improved extraction and production method (Vereman et al. 2021). These studies have shown that the type of biosurfactant and its production depend on the strain, the formulation of the culture medium (substrate) and the culture conditions in which the organism grows. As shown in Fig. 3, to optimize microbial surfactant production, it is necessary to use microorganisms with high production capabilities growing in optimal conditions on low-cost substrates employing an adequate system for fermentation (i.e. optimization of the fermentation process). The use of novel technological developments is also necessary to efficiently enhance biosurfactant production. In this context, the use of metabolomic and metagenomics approaches may allow identifying efficient biosurfactant producers as well as novel microbial surfactants. In addition, in silico analysis provides a versatile methodology for integrating multi-omics information to enhance the biosurfactant production (Occhipinti et al. 2018). Recombinant DNA technology also enables overproduction of microbial surfactants (Gaur et al. 2022). Furthermore, nanotechnology is a promising tool in the development of biosurfactant-based nanostructures (nano-adsorbent structures), which are efficient nanoparticles for environmental application (Kundu et al. 2016; Nitschke et al. 2022).
An overview of factors influencing biosurfactant production. The selection of microbial culture as well as the use of adequate fermentation systems and novel technological developments are important for the optimization of microbial surfactant production
Biosynthetic pathways of microbial surfactants
It has been reported that microorganisms use independent pathways to synthesize the hydrophobic and hydrophilic portions of biosurfactants, which are subsequently combined (Théatre et al. 2021). The biosynthetic pathway to be used depends on the carbon source in which the microorganism grows. For example, for glycolipid biosynthesis in the presence of carbohydrates as the sole carbon source, carbon flow is used in both the lipogenic and glycolytic pathways for lipid moiety and hydrophilic portion synthesis, respectively (Fig. 4). As illustrated in Fig. 4, when glucose is present in the growth medium, glucose-6 phosphate is the first intermediate of glucose metabolism, which is one of the principal precursors of carbohydrates that constitute the hydrophilic part of a biosurfactant (e.g. sophorose, trehalose, and mannose). The hydrophobic part of the surfactant is synthesized by the oxidation of glucose to pyruvate, which is then converted into acetyl-CoA. Acetyl-CoA is converted to malonyl-CoA, and then a series of reactions occurs to convert malonyl-CoA to fatty acids, which are then channeled into the lipid biosynthetic pathway (Parsons and Rock 2013; Fakas 2016). For example, for the sophorolipid biosynthesis, oleic acid is synthesized via de novo fatty acid biosynthesis, which is converted to ω-hydroxy fatty acid. UDP-glucose enters into the biosynthesis to form glucolipid and then a non-acetylated acid sophorolipid is formed. Subsequently, a series of reactions occur to convert this last compound to lactones both in monomeric or in dimeric structures, since sophorolipid exists in two forms acidic and lactonic (Van Bogaert et al 2011; Saerens et al 2015; Wongsirichot, et al 2021) (Fig. 5). Emulsan and hydrophobins can also be synthetized through de novo fatty acid biosynthesis and amino acid formation pathways, respectively (Fig. 4). The biosynthetic pathways of bioemulsifiers also have been proposed. For example, for emulsan biosynthesis, fructuose 6-P would be transformed into UDP-N-acetyl-D-glucosamine, which after a series of reactions would be converted to UDP-N-acetyl-L-galactosaminuronic acid and then to UDP-N-acetyl-D-galactosamine uronic acid. This last compound would undergo sequential transfer of sugars, acetylation, trans-amidation and trans-esterification of fatty acids, translocation and polymerization of repeat units to form emulsan (Singh et al 1990; Nakar and Gutnick, 2001) (Fig. 6).
Biosynthetic pathways for the production of different types of glycolipids (i.e. rhamnolipids, sophorolipds, etc.), lipopeptide (i.e. surfactin), hydrophobins and bioemulsifiers using carbohydrate substrates (redrawn and extended from Luft et al. 2020; Jimoh et al. 2021; Fernandes-Moutinho et al. 2021). Carbon flow is used in both the lipogenic and glycolytic pathways for lipid moiety and hydrophilic portion synthesis, respectively
Biosynthetic pathway for the production of sophorolipids. A series of reactions occur to convert non-acetylated acid sophorolipid to lactones both in monomeric or in dimeric structures. Sophorolipid exists in two forms acidic and lactonic (redrawn from Van Bogaert et al 2011; Saerens et al 2015; Wongsirichot, et al 2021)
Proposed biosynthetic pathway for the production of emulsan. Fructuose 6-P would be transformed into UDP-D-GlcNAc, which after a series of reactions would be converted to UDP-D-GalNAc. This last compound would undergo sequential reactions to form emulsan (redrawn from Singh et al 1990; Nakar and Gutnick, 2001). GlcNAc, N-acetylglucosamine; ManNAc, N-acetylmannosamine; GalNAc, N-acetylgalactosamine; GalNAc, N-acetylgalactosamine uronic acid
In contrast, when hydrocarbons are employed as a carbon source for biosurfactant biosynthesis, microorganisms employ the gluconeogenic pathway (the formation of glucose from nonhexose precursors) and the lipolytic pathway for the production of the hydrophilic part (saccharides) and the hydrophobic part (fatty acids), respectively (Fig. 7). The gluconeogenic pathway is activated for the production of saccharides, which begins with fatty acid β-oxidation to acetyl-CoA (or propionyl-CoA, for odd-chain fatty acids). Acetyl-CoA undergoes reactions inverse to those performed in glycolysis. Acetyl-CoA is converted to oxaloacetate, which is decarboxylated and then phosphorylated to form phosphoenolpyruvate. This compound is eventually converted into glyceraldehyde 3‐phosphate. Glyceraldehyde 3‐phosphate then transforms into fructose 1,6‐bisphosphate via either direct conversion or through the intermediate dihydroxyacetone phosphate. Fructose 1,6‐bisphosphate transforms into fructose 6‐phosphate, which forms glucose‐6‐phosphate. This compound is the precursor of the carbohydrates (the hydrophilic moiety) in the biosurfactant (Fig. 7) (Karmakar, 2017; Park et al. 2020; Luft et al. 2020; Jimoh et al. 2021).
Metabolic pathways for the synthesis of different types of glycolipids (i.e. rhamnolipids, sophorolipds, etc.), hydrophobins, bioemulsifiers, etc., using a hydrocarbon substrate (redrawn and extended from Luft et al. 2020; Jimoh et al. 2021). Microorganisms employ the gluconeogenic pathway (the formation of glucose from nonhexose precursors) and the lipolytic pathway for the production of the hydrophilic part (saccharides) and the hydrophobic part (fatty acids), respectively
Microbial biosurfactants are synthesized intracellularly or extracellularly, and their synthesis requires specific genes or enzymes to be activated in the presence of a particular substrate (Jimoh et al. 2021). For example, in P. aeruginosa, three enzymes (rhamnosyltransferase chain A, chain B and chain C) that catalyze rhamnolipid production in this bacterium are encoded by the rhlAB operon and the rhlC gene. The expression patterns of these genes have suggested that the synthesis of monorhamnolipids initially occurs early in the stationary phase followed by the conversion of some into dirhamnolipids (Wagner et al. 2003; Suh et al. 2019). In the fungus U. maydis, mannosylerythritol biosynthesis requires the enzymes mannosyltransferase, acetyltransferase and acyltransferase, which are encoded by the emt1, mat1 and mac1 genes, respectively (Hewald et al. 2006). Several studies have reported that surfactin is produced by Bacillus species (Tables 1, 2 and 3). The biosynthesis of this surfactant is catalyzed by surfactin synthase, which involves joining amino acids into the surfactin peptide component through a thiotemplate mechanism. This process includes the assembly of amino acids into a peptide chain. The lipopeptide is then formed by linking the hydroxyl fatty acid to a peptide using an acyltransferase (Jimoh et al. 2021). Specifically, it has been shown that in B. subtillis, surfactin biosynthesis involves srfA gene expression, which is regulated by repressor proteins and other transcriptional regulators (Sullivan, 1998; Roongsawang et al. 2010; Jimoh et al. 2021). In comparison, in the fungus T. reesei, the biosynthesis of hydrophobins depends on the hfb1 and hfb2 genes (Askolin et al. 2005), whereas Fusarium graminearum possesses five genes encoding hydrophobins (i.e. FgHyd1-5) (Quarantin et al. 2019). An increase in the expression of hydrophobin coding genes has been detected in studies on polyethylene terephthalate degradation by Trichoderma viride GZ1 (Dąbrowska et al. 2021).
Emergent strategy tools for biosurfactant applications in the biodegradation of hydrophobic organopollutants
Biosurfactants possess practical and efficient applications in the environmental biodegradation of hydrophobic organopollutants. Studies on the use of partially purified biosurfactant or biosurfactant producers for hydrophobic organopollutant biodegradation have been conducted ex situ (e.g. in the laboratory). In this context, investigations on benzo(a)pyrene biodegradation were performed in contaminated water and soil by adding a surfactant produced by Pseudomonas frederiksbergensis (Guo and Wen 2021). It was observed that the benzo(a)pyrene in contaminated water decreased by 66% (2 mg/L, initial concentration) when the dosed biosurfactant was 3 mg/L, whereas 84.8% of this pollutant was biodegraded in contaminated soil by adding 0.5% (w/w) biosurfactant (Guo and Wen 2021). Furthermore, the cell-free broth containing surfactants produced by Bacillus algicola, Rhodococcus soli, Isoptericola chiayiensis, and Pseudoalteromonas agarivorans was able to desorb crude oil in oil-polluted marine sediment (Lee et al. 2018). Moreover, the addition of a crude lipopeptide biosurfactant produced by Bacillus methylotrophicus to biodiesel-contaminated clayey soil at a low concentration (0.5% w/w) enhanced biodiesel removal by approximately 16% after 90 days (Decesaro et al. 2021). In addition, research on PAH biodegradation revealed that the addition of phenol (which frequently coexists with PAHs) and a biosurfactant extracted from the production of P. aeruginosa were able to enhance PAH bioavailability in sludge and improve biodegradation (Zang et al. 2021). Furthermore, the application of rhamnolipids in a fungal-cultured biotrickling filter for toluene removal showed significantly improved biodegradation of this hydrocarbon (˃ 96%) (Dewidar and Sorial 2022).
Additionally, a study on the biodegradation of petroleum wastewater was performed using an anoxic packed bed biofilm reactor that was inoculated with in situ biosurfactant-producing bacteria (Molaei et al. 2022). Biosurfactant (rhamnolipid and surfactin) production and dehydrogenase activity increased during biodegradation, showing efficient biodegradation of cyclic aliphatic, aliphatic, and aromatic hydrocarbons (Molaei et al. 2022). Moreover, the biosurfactant producers Bacillus sp. AKS2 and P. aeruginosa AKS1 isolated from refinery sediments were used in biodegradation experiments performed in microcosm sediments (125 mg crude oil/10 g sand) (Chettri et al. 2021). The half-lives for hydrocarbon biodegradation were 50 and 61 days for P. aeruginosa and Bacillus sp respectively (Chettri et al. 2021).
A study using immobilized Vibrio sp. LQ2, a biosurfactant (phospholipid) producer in the bioremediation of diesel oil-contaminated seawater, was conducted (Zhou et al. 2021). It was shown that the inoculation of biochar-immobilized LQ2 resulted in 94.7% diesel oil removal (reduction from 169.2 mg to 8.91 mg) after 7 days. This investigation also revealed an increase in the degradation-related genes alkB and CYP450-1, which were 3.8 and 15.2 times higher in the immobilized LQ2 experiment than those in the free-cell experiment (Zhou et al. 2021).
An analysis of the utilization of biosurfactants or microbial producers of biosurfactants in combination with other methods to improve organopollutant degradation has also been undertaken. In this context, a study on the use of a bacterial surfactant (lipopeptide) in electrokinetic remediation increased the degradation rate of crude oil-contaminated soil by approximately 92% (Prakash et al. 2020). In addition, an enhanced method for the treatment of oil-contaminated soil has also been reported using a biosurfactant (rhamnolipid and surfactin)-assisted washing mechanism coupled with hydrogen peroxide-stimulated microbial degradation (Fanaei et al. 2020). Furthermore, an effective remediation (84%) method for diesel-contaminated soil was reported by integrating electrokinetics with bioremediation using the biosurfactant-producing bacterium Staphylococcus epidermidis EVR4 (Vaishnavi et al. 2021). Moreover, a process in which aromatic hydrocarbons were removed from contaminated soil from industrial sites using a surface-modified lipopeptide biosurfactant (with enhancement of polar amino acids) produced by Bacillus malacitensis and an activated functionalized carbon matrix was investigated; a 62% total petroleum hydrocarbon removal efficiency was found after 28 days (Christopher et al. 2021).
Furthermore, studies using biosurfactants in situ (i.e. in polluted areas) have also shown biodegradation of hydrophobic organopollutants. For example, a field trial on LaTouche Island (in Alaska) demonstrated the effectiveness of the microbial surfactant PES-51, which was able to remove weathered crude oil from beach material. Hydrocarbons (semivolatile petroleum) were reduced by approximately 70% (Tumeo et al. 1994). In addition, a biodegradation experiment on crude oil-contaminated soil was undertaken near an oil production company, demonstrating that 77% of crude oil was degraded using a combination of rhamnolipids, nutrients and hydrocarbon-degrading bacteria (Tahseen et al. 2016). Furthermore, it was found that Enterobacter xiangfangensis STP-3 was capable of degrading 82% of petroleum hydrocarbons in 14 days during the biotreatment of real field petroleum oil sludge with the simultaneous production of metabolic enzymes and biosurfactants (Muneeswari et al. 2021).
Concluding remarks
Biosurfactants are produced either as growth-associated products or secondary metabolites with diverse chemical structures and in varying amounts by a wide range of microorganisms. Microbial surfactant production can be induced by the presence of hydrophobic substrates or they can be produced intrinsically using conventional organic materials or organic wastes as substrates. Biosurfactants are biodegradable and ecofriendly, and their microbial diversity in production, high stability and specific activity make them a promising technology to clean up polluted environments in a green manner. The use of microbial surfactants offers a promising strategy to overcome the problems associated with contamination by hydrophobic organopollutants. However, biosurfactant production must be optimized to increase yield and decrease production costs. For this reason, it is necessary to use microbial producers with high biosurfactant production capabilities on low cost substrates. Additionally, the use of novel technological developments (e.g. omic analysis, recombinant DNA technology, nanotechnology, computational modeling, efficient separation technology) in multidisciplinary research would enhance the efficient production of biosurfactants. Further studies are needed to fully understand the mechanisms of biosurfactant biosynthesis, in which the use of bioinformatics analysis is a promising tool. In addition, more research is required to understand the interaction of biosurfactants with cells in order to improve our knowledge of their mechanism of action for the organopollutants degradation. The development of integrated strategies that combine techniques and biosurfactants is an interesting approach to explore the most effective treatment technology for the remediation of hydrophobic organopollutant contamination.
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Sánchez, C. A review of the role of biosurfactants in the biodegradation of hydrophobic organopollutants: production, mode of action, biosynthesis and applications. World J Microbiol Biotechnol 38, 216 (2022). https://doi.org/10.1007/s11274-022-03401-6
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DOI: https://doi.org/10.1007/s11274-022-03401-6