open access

Abstract

Biosurfactants are amphiphilic secondary metabolites produced by microorganisms. Marine bacteria have recently emerged as a potential source for these natural products which exhibit surface-active properties, making them useful for diverse applications such as detergents, wetting and foaming agents, solubilisers, emulsifiers and dispersants. Although precise structural data are often lacking, the already available information from biochemical analyses and genome sequences of marine microbes indicate a high structural diversity including a broad spectrum of fatty acid derivatives, lipoamino acids, lipopeptides and glycolipids. This article aims to provide an overview of the structural diversity of low molecular-weight biosurfactants produced by marine microbes reported until 2020. Furthermore, characterization of biosurfactants production in marine bacteria was carried out along with their potential for biotechnological applications.

Keywords: Marine biosurfactant, structural diversity, characterization, biotechnological applications

INTRODUCTION

Microorganisms produce a large variety of secondary metabolites that are of interest for the biotech and pharma industries. A prominent example comprises biosurfactants, a very diverse group of lipids which have a polar, amphiphilic character in common containing both hydrophilic and hydrophobic domains within one molecule. As a consequence of the amphiphilic structure, these compounds lower interfacial tension allows, for instance, solubilisation of hydrophobic substances in water (Kushner, 1978). In nature, the biosynthesis of amphiphilic substances could open ecological niches for the production of microorganisms in different habitats, for example, by exploitation of hydrophobic substrates, enabling motility, or avoiding competitors (Ron and Rosenberg 2001; Raaijmakers et al., 2010).

More than 2000 distinct biosurfactant structures are currently known, covering chemically different families of compounds, but also groups of congeners, that are structurally closely related compounds with minor structural variations (Hausmann and Syldatk, 2014). This structural diversity of biosurfactants implies a large variety of biological and physicochemical properties.

Frequently highlighted properties of biosurfactants include low critical micelle concentrations (CMC), strong surface tension reduction, metal ion complexation, prominent bioactivities, and low eco-toxicity. A low CMC implies that such biosurfactants exert their function at much lower concentrations than many chemically produced surfactants (Bhadoriya and Madoriya, 2013). Bioactivities of biosurfactants include antibacterial, antifungal and anti-tumour effects. At the same time, ecological aspects are considered as important, as biosurfactants can be produced from renewable resources and they exhibit low eco-toxicity in connection with supreme biological degradability preventing environmental accumulation (Poremba et al., 1991; Johann et al., 2016). These properties form the basis of the pronounced interest in this class of metabolites (Banat et al., 2000) for biotechnological applications, for example, as detergents, wetting agents for hydrophobic surfaces or fibres, and emulsifiers. In addition, they are used in food, cosmetics, and as pharmaceuticals (Banat et al., 2000).

To date, research regarding the technological access to biosurfactants has mostly focused on soil-isolated microbes, predominately species of Bacillus, Pseudomonas or yeasts. More recently, however, marine habitats are considered as a prolific source for the discovery of microorganisms with a specialized metabolism and physiology that produces a variety of useful compounds such as biosurfactants (Jensen and Fenical, 1994; Kennedy et al., 2011; Romanenko et al. 2008; Satpute et al., 2010).

This article aims to provide an overview of the structural diversity of low molecular-weight biosurfactants produced by marine microbes reported until 2020. Furthermore, characterization of biosurfactants production in marine bacteria and their potential for biotechnological applications are highlighted.

STRUCTURAL DIVERSITY OF BIOSURFACTANTS 

Biosurfactants produced by different microorganisms exhibit an immense spectrum of diverse chemical structures. The amphiphilic character of biosurfactants is typically formed by both hydrophobic and hydrophilic components with the hydrophobic part usually comprising saturated or unsaturated fatty acids, hydroxy fatty acids, or fatty alcohols with a chain length between 8 and 18 carbon atoms. The hydrophilic components are constituted either of small hydroxyl, phosphate or carboxyl groups, or of carbohydrate (such as mono-, oligo-, or polysaccharides) or (poly-)peptide moieties.

Biosurfactants are predominantly anionic and non-ionic compounds. It has been assumed that cationic biosurfactants exhibit higher toxicity and are thus found only rarely (Hausmann and Syldatk, 2014). Besides the grouping by charge, surface-active secondary metabolites can be broadly classified into high and low molecular weight biosurfactants (Rosenberg and Ron, 1999; Soberón-Chávez and Maier, 2011). The structural diversity of the latter group can be further subdivided into fatty acids, lipoamino acids, lipopeptides and glycolipids as outlined in more detail in the following section.

High Molecular Weight Polymeric Biosurfactants/Bioemulsifiers

High molecular weight polymeric (HMW) biosurfactants, suggested to be referred to as bioemulsifiers to distinguish them from low molecular weight metabolites (Uzoigwe et al., 2015), are produced by many bacteria of different species. They are constituted of polysaccharides, proteins, lipopolysaccharides, lipoproteins, or complex mixtures of these compounds referred to as lipo-heteropolysaccharides. The prototypical HMW bioemulsifier emulsan is produced, for instance, by Acinetobacter calcoaceticus RAG-1, an isolate from the Mediterranean Sea (Rosenberg and Ron 1997; Sar and Rosenberg, 1983). It consists of a heteropolysaccharide backbone with a repeating tri-saccharide unit. This repeating unit probably consists of N-acetyl-d-galactosamine, N-acetylgalactosamine uronic acid and a di-amino-6-deoxy-d-glucose (Hausmann and Syldatk, 2014; Zuckerberg et al., 1979) with fatty acids (FA) covalently linked to the polysaccharide through ester linkages.

In spite of the structural complexity, the genes encoding emulsan synthesis by A. calcoaceticus RAG-1 were identified and shown to be organized in a single wee gene cluster of 27 kilo base pairs (Nakar and Gutnick, 2001). Amphiphilic proteins may also be regarded as polymeric surfactants. They constitute a remarkable class of little-explored and biotechnologically hardly targeted biosurfactants. Naturally occurring foams often contain proteins with foam-stabilising properties. A particularly interesting example from the non-microbial world is ranaspumine produced by tropical frogs that use foam nests to protect their eggs. Another likewise foaming protein is latherin, mainly known from horse sweat (Cooper, and Kennedy, 2010). Hydrophobins are small proteins secreted by different filamentous fungi (Linder, 2009) which are also surface-active and may represent promising targets for biotechnology (Cox and Hooley, 2009).

Low Molecular Weight Biosurfactants

Low molecular weight (LMW) biosurfactants range from simple free fatty acids and phospholipids to amino acids linked to lipids, lipopeptides and glycolipids.

Fatty acid and phospholipid derivatives may act as surface-active substances. Strong reduction of surface and interfacial tensions were, for instance, observed for branched fatty acids known as corynomycolic acids with chain lengths of C12–C14 (Fujii et al., 1999; Käppeli and Finnerty, 1980; Kretschmer et al., 1982). (Hydroxy) fatty acids bound to proteinogenic or non-proteinogenic amino acids form lipoamino acid biosurfactants, for example, ornithine lipids, lysine lipids, N-acyltyrosines or cerilipin containing ornithine and taurine produced, for example, by Myroides sp., Gluconobacter cerinus and Nitrosomonas europaea (Tahara et al., 1976; Kishimoto et al., 1993; Thies et al., 2016; Williams et al., 2019).

Lipopeptides are a very prominent group of LMW biosurfactants derived from amino acids. These often cyclic depsipeptides are produced by various clades of microorganisms including the bacterial genera Bacillus, Lactobacillus, Streptomyces, Pseudomonas and Serratia. As a result of their non-ribosomal origin, they often contain non-proteinogenic amino acids such as d-enantiomers. Many lipopeptides show not only a reduction of surface tension, but also significant bioactivities (Baltz et al., 2005; Inès et al., 2015), with the antibiotics daptomycin from Streptomyces roseosporus and polymyxin B from Paenibacillus polymyxa as prominent examples (Tally and DeBruin, 2000; Trimble et al., 2016). Surfactin produced by different species of the genus Bacillus is considered as one of the most effective biosurfactants of all, stated to reduce the air/water surface tension from 72.5 mN/m down to 27 mN/m (Jacques, 2011; Yeh et al., 2008).

Glycolipids, similar to the emulsan repeating unit, consist of mono- or oligosaccharides and a lipid moiety. Typical sugars forming the hydrophilic part are glucose, mannose, galactose, glucuronic acid, or rhamnose, while the hydrophobic part consists of saturated or unsaturated fatty acids, hydroxy fatty acids or fatty alcohols. The best-explored groups comprise sophorolipids, mannosylerythritol lipids, trehalose lipids and rhamnolipids (Hausmann and Syldatk, 2014). Sophorolipids contain the di-saccharide sophorose and, predominantly, 17-hydroxyoleic acids. They usually form lactones, but also occur in the acidic form, that is, without ring closure (Nuñez et al., 2001). The yeast Starmerella bombicola is the most prominent producer of sophorolipid (Roelants et al., 2016). Mannosylerythritol lipids (MELs) are also mainly known from fungal species, such as Pseudozyma sp. and Ustilago maydis. MELs comprise 4-O-β-d-mannopyranosyl-d-erythritol in their carbohydrate moiety, which displays diverse acylation patterns and a variety of chain lengths of the acyl groups (Morita et al., 2009; Feldbrügge et al., 2013). Trehalose lipids contain the di-saccharide trehalose, which is acylated with long-chained, straight or β-branched 3-hydroxy fatty acids called mycolic acids and are mainly known from Actinobacteria like Mycobacterium, Arthrobacter and Rhodococcus species (Christova and Stoineva, 2014; Kügler et al., 2015). Rhamnolipids are best known from the pathogenic bacterium Pseudomonas aeruginosa but are also reported from different Burkholderia spp. (Abdel-Mawgoud et al., 2010). They comprise one or two β-l-rhamnose units, commonly coupled to two 3-hydroxy fatty acid moieties via a glycosidic linkage that defines different congeners with a chain length between 8 and 16 carbon atoms (Abdel-Mawgoud et al., 2010; Déziel et al., 2000).

The length of acyl chains within a certain range appears to be species-specific to some extent (Wittgens et al., 2018). Moreover, decorations like methylations and acetylations are reported occasionally (Abdel-Mawgoud et al., 2010). Further reported glycolipids include glucose lipids, cellobiose lipids, polyketide glycosides, isoprenoid and carotenoid glycolipids (Abdel-Mawgoud et al., 2018). The phylogeny of biosurfactant-producing microorganisms is as diverse as the chemical composition of these metabolites. Beyond the already mentioned examples, known biosurfactant producers are, for instance, Firmicutes like Lactococcus sp., Proteobacteria like different Pseudomonas or Serratia spp., Actinobacteria like Streptomyces spp., and fungi like Cryptococcus sp. (Cameotra et al., 2010). Producer strains were isolated from many different habitats, i.e. fresh water, soil, pathogen biofilms, leaf surfaces and industrial effluents, oil wells and marine environments (Gautam and Tyagi, 2006; Satpute et al., 2010).

Surfactants with diverse properties and low production costs are required to increase the applications of natural SACs, which gives greater incentive to develop surfactants of biological origin produced by microorganisms. Marine microorganisms are ubiquitous in the marine environment as well as extreme environments. The oceans have a relatively narrow range of pH, salinity and temperature while areas such as the volcanic vents face extreme conditions. These microorganisms are known to be metabolically and physiologically adapted to survive under extreme temperature, pressure, pH and salinity conditions (Das et al., 2010; Thavasi et al., 2014). For example, members of the Alcanivorax genus survive at low to mild hydrostatic pressure in hydrocarbon contaminated environments. The strains A. borkumensis SK2 and A. dieselolei KS 293 have developed different strategies to cope with environmental stress under high pressure. While the respiration and cell integrity is not affected in KS 293 at mild hydrostatic pressure, SK2 activates the production of the osmolyte ectoine to cope with hydrostatic pressure (Scoma et al., 2016a, b).

Marine bacteria secrete large molecules known as exopolysaccharides (EPS) consisting of proteins, polysaccharides, lipids, nucleic acids and uronic acids. EPS enhances the survival of microbial cells under changing environmental conditions through various mechanisms such as biofilm formation, enhancing substrate adhesion, protection against limited nutrient availability, detoxification of metals and the presence of antibiotics (Harimawan and Ting 2016; Pal and Paul 2008).

Some microorganisms specifically produce amphiphilic EPS, particularly BS as a mechanism to increase the bioavailability of hydrophobic substrates such as hydrocarbons, these BS enhance the growth of indigenous bacteria capable of degrading aliphatic and aromatic hydrocarbons. BS produced from marine bacteria can facilitate hydrocarbon dispersion, degradation, emulsification and bioavailability (Das et al., 2010; Mapelli and Scoma, 2017). BS from cold adapted marine microorganisms or psychrophilic organisms can work efficiently at cold and freezing temperatures, and are therefore suitable in laundry detergent formulations where low temperature washing conditions have become a priority for energy conservation (Perfumo et al. 2018; Marchant and Banat 2012b). The potential uses of BS are further improved by their low-toxicity, meaning they are applicable for large-scale industrial production and subsequent environmental disposal where they can be readily biodegraded (Irorere et al. 2017; Uzoigwe et al. 2015). Hence marine bacteria offer an excellent opportunity for the discovery of new SAC molecules with distinctive properties.

Although highly attractive, the biosynthesis of BS from marine organisms has largely been overlooked. The mechanism of their regulation during synthesis is also not fully understood adding further difficulties to the process for their production. Several approaches are required before the widespread application of marine-derived BS can be achieved: (i) Isolation and identification of novel, nonpathogenic marine BS producing bacteria (ii) Optimization of culture conditions to achieve sufficient yields of BS and (iii) Characterization of genes involved in BS production from marine organisms. These will allow the use of marine strains in large scale BS production processes while improving yield and cost-efficiency of BS production.

CHARACTERIZATION OF BS PRODUCTION IN MARINE BACTERIA 

The identification of possible genes involved during BS synthesis is necessary in order to understand BS synthesis and develop robust BS producing strains with high production capacity. The most well characterized low-molecular weight BS is rhamnolipid, produced by several species of Pseudomonas and Burkholderia. The genes rhlA, rhlB and rhlC, which are responsible for the biosynthesis of rhamnolipids have been found in P. aeruginosa as well as non pathogenic B. thailandensis. These three genes are localized within a single gene cluster in Burkholderia while, the rhlC gene is located at two different, remote position within the P. aeruginosa genome (Dubeau et al., 2009; Perfumo et al., 2013). Recently, homologues to P. aeruginosa rhamnolipid genes rhlA and rhlB were identified in a non-pathogenic marine Pseudomonas species MCTG214(3b1) (Twigg et al., 2018). Most of the genetic studies of BS production are limited to well characterised BS molecules, but the expression of genes involved in BS synthesis is not well studied in marine bacteria. The genes and regulatory pathways are not necessarily identical in different BS producers. Different species can produce a BS with totally different chemical structure and even small variations in the congener composition of a surfactant can greatly affect its functional property. To fully understand how SAC synthesis is regulated in these marine strains, it is important to characterise the chemical structure and necessary genes required for BS synthesis. The chemical composition of the SAC molecules can be determined by electrospray ionization mass spectrometry (ESI–MS), high performance liquid chromatography mass spectrometry (HPLC–MS) and nuclear magnetic resonance (NMR) techniques (Smyth et al., 2010).

Few reports have been published regarding BS synthesis during hydrocarbon degradation in marine bacteria. It was reported that P. aeruginosa JP-11 isolated from the marine environment utilized 98.8% ± 2.3% of biphenyl within 72 h from contaminated sites. Although P. aeruginosa can not be considered a true marine bacterium, it is a common organism isolated from the marine environment. The production of BS was confirmed by the expression of the rhamnolipid synthesizing genes rhlAB (Chakraborty and Das, 2016). Bacillus species are known to produce BS such as lichenysin, surfactin, fengycin, pumilacidin, iturin and bacillomycin (Vater et al., 2002). BS production was seen during anthracene degradation by a marine alkaliphile Bacillus licheniformis (MTCC 5514). The strain degraded 95% of 300 ppm anthracene and showed tolerance up to 500 ppm of anthracene concentration. The gene involved in the BS lichenysin production was licA3, followed by degradation through the catabolic degradative enzyme, catechol 2,3 dioxygenase(C23O) (Swaathy et al., 2014). Acinetobacter species are also known to produce high-molecular weight emulsifiers (Ortega-de la Rosa et al., 2018).

In Acinetobacter lwoffii RAG-1, the genes encoding the biosynthesis of emulsan (a polysaccharide BE) were reported to be clustered within a 27-kbp region termed, wee cluster (Nakar and Gutnick 2001). The bioemulsan alasan produced by A. radioresistens is a complex mixture of anionic polysaccharides and protein. The alnA gene which codes for the surface active protein of alasan was cloned, sequenced, and expressed in E. coli. Significant sequence similarity (21%) between the recombinant emulsifier protein AlnA of A. radio resistens and OmpA of E. coli was seen. However, no emulsifying or hydrocarbon solubilizing activities have been observed with E. coli OmpA (Toren et al., 2002). It has also been reported that the marine hydrocarbonoclastic bacterium Alcanivorax borkumensis synthesizes glycolipids for hydrocarbon degradation (Abraham et al., 1998; Yakimov et al., 1998). The genome sequence of A. borkumensis SK2 revealed its capacity for BS production. The glycosyltransferase (ABO 1783) similar to RhlB from P. aeruginosa and glycosyl transferase protein family 9 (ABO_2215) were found to be potentially involved in BS production. The A. borkumensis SK2 genome encodes other proteins involved in emulsifier production namely, OmpA (ABO_0822), OprG/OmpW (ABO_1922) and OmpH (ABO_1152) (Schneiker et al. 2006).

Similarly, genes involved in BS production were reported in the marine bacterium Achromobacter sp. HZ01. The genome of strain HZ01 harbours OmpH (gene_1336) and OmpA (gene_2469) which are both related to emulsifier production (Hong et al., 2017). Similar genes involved in biosynthesis of BS were found in the genome of Cobetia sp. MM1IDA2H-1 (Ibacache-Quiroga et al., 2017).

A significant problem in using genetic information from one organism to another is the lack of sequence homology between genes which may lead to the production of similar products. The rhamno lipid production genes in P. aeruginosa PAO1 and B. thailandensis have only about 50% sequence homology (Dubeau et al., 2009). While in a marine Pseudomonas species MCTG214(3b1), unrelated to P. aeruginosa, which produces di-rhamnolipids identical in structure to P. aeruginosa, the rhlA and rhlB genes have very high sequence homology while it has so far been impossible to find an rhlC homologue which indicates the presence of second novel rhamnosyl transferase (Twigg et al., 2018). This suggests that it will be necessary to search for specific domains within the genes rather than whole gene sequences when investigating such capabilities.

POTENTIAL BIOTECHNOLOGICAL APPLICATIONS 

All surfactants are synthesized chemically. Nevertheless, ample thought has been newly directed toward biosurfactants. They have been preferred over artificial surfactants attribute to their broad capabilities, the synthetic capacity of biodegradable microbes, and lower toxicity. Some of the industrial properties of biosurfactants have been predicted (Tan and Li, 2018).

Anti-Microbial Activity

Marine surfactants have been shown to exert bacteriostatic and bactericidal activities, by destabilizing the cell wall or outer membranes of the pathogens. More specifically, lipidic moieties can be inserted in these structures, changing their charge and morphology, ultimately leading to pore formation and cell death (Naughton et al., 2019). Furthermore, these interactions with the cellular surface, prevent planktonic cells from forming biofilms, by disrupting quorum sensing mechanisms and preventing attachment to biotic or abiotic surfaces. Lastly, some glycolipid marine-derived biosurfactants can also dislocate and terminate bacterial cells from mature biofilms (Banat et al., 2014). There is a plethora of marine-derived lipopeptidic surfactants with antimicrobial potential. The most powerful anti-microbial surfactant, described so far, is surfactin produced by Bacillus velezensis H3. To this end, nC14- and anteiso-C15-surfactins were effective against S. aureus and K. pneumoniae, however, without being able to outperform the antibiotic polymyxin B. On the other hand, their antifungal properties against C. albicans were greater than that of vancomycin (Liu et al., 2010). In addition, C15-surfactin is also synthesized by Bacillus amyloliquefaciens strain MB199 and has been shown to act synergistically with ketoconazole against fungal pathogens like C. albicans. Nonetheless, as with all surfactins, this isoform also exhibits strong hemolytic activity due to its ability to disrupt membranes (Liu et al., 2012). Two other surfactins (CS30-1 and -2) synthesized by Bacillus sp. CS30 are also associated with anti-fungal activity against the plant fungus Magnaporthe grisea, which causes rice crops to wither, thus resulting in economic loss (Wu et al., 2019).

Apart from surfactin, other lipopeptides produced by marine microorganisms have also presented anti-microbial and anti-biofilm potential, including lipoptides produced by (i) the marine actinobacterium Brevibacterium aureum MSA13 capable of exerting a broad-spectrum antibiotic activity with a most profound effect against C. albicans (Kiran et al., 2009); (ii) a strain of B. circulans shown to be more effective than penicillin and streptomycin, especially against Micrococcus flavus NCIM 2376, E. coli NCIM 2931, Mycoplasma segmatis NCIM 5138, Bacillus pumilus MTCC 2296, and Klebsiella sp. (Das et al., 2008), in addition to limiting the growth of other pathogens like Proteus vulgaris, S. aureus, A. niger, and C. albicans (Das et al., 2009), while a B. circulans producing lipopeptide of the fengycin family had bactericidal effects against Citrobacter fruendii, Alcaligenes faecalis, Serratia marcesens and Klebsiella aerogenus (Sivapathasekaran et al., 2009); (iii) the actinobacterium Nesterenkonia sp. MSA31, which exhibited anti-biofilm activity against S. aureus (Kiran et al., 2017) and Vibrio harveyi (a fish pathogen) (Selvin et al., 2016). Furthermore, aneurinifactin is another novel lipopeptidic surfactant produced by Aneurinibacillus aneurinilyticus strain SBP-11 with anti-microbial activity against K. pneumoniae, E. coli, S. aureus, P. aeruginosa, B. subtilis and Vibrio cholerae. This surfactant molecule can anchor to the bacterial membrane, disrupting its continuity and metabolic activity, resulting in the production of hydroxyl radicals, which in turn cause lipid peroxidation and pore formation on the membrane (Balan et al., 2017). In addition, the same group isolated and characterized pontifactin, a surfactant lipopeptide produced by a newly identified bacterium, Pontibacter korlensis strain SBK-47, that exhibited both antibacterial activity against Streptococcus mutans, M. luteus, Salmonella typhi and Klebsiella oxytoca, as well as anti-adhesion potential against B. subtilis, S. aureus, S. typhi and V. cholerae (Balan et al., 2016).

Finally, an amphiphilic lipopeptide (Rn-Glu1-Leu/Ile2-Leu3-Val4-Asp5-Leu6-Leu/Ile7) produced from Bacillus licheniformis was capable of demonstrating significant bacteriostatic activity against E. coli, V. cholerae, Vibrio paraheamolyticus, V. harveyi but weaker activity against P. aeruginosa, S. aureus and Proteus sp. (Chen et al., 2017). The literature also reports the antimicrobial efficacy of glycolipid surfactants produced by marine organisms. To this end, a biosurfactant glycolipid produced by Streptomyces sp. MAB36 showed anti-bacterial action against Bacillus megaterium, B. cereus, S. aureus, E. faecalis, Shigella dysenteriae, Shigella boydii, C. albicans and A. niger (Manivasagan et al., 2014). Another glycolipid purified from extracts of the marine halotolerant bacterium Buttiauxella sp. M44 also showed anti- C. albicans, A. niger and anti-E. coli activity, as well as mild antagonistic activity against Salmonella enterica, B. cereus,B. subtilis and S. aureus (Marzban et al., 2015). Similarly, another glycolipid produced from the epizootic Serratia marcescens (isolated from the hard coral Symphylia sp.) exhibited anti-adhesive and inhibitory activity against C. albicans BH, P. aeruginosa PAO1 and B. pumilus TiO1, as well as a damaging potential against pre-formed B. pumilus biofilms (Dusane et al., 2011).

On another note, staphylosan, a glycolipid biosurfactant produced by Staphylococcus saprophyticus SBPS-15, was documented to possess significant surface tension-lowering activity and complete inhibition of biofilm formation for B. subtilis BHKG-7 and Serratia liquefaciens BHKH-23. Additionally, it managed to dislodge bacteria from pre-formed P. aeruginosa BHKH-19 and S. liquefaciens BHKH-23 single-strain biofilms (Balan et al., 2019). Lastly, BS-SLSZ2 (a biosurfactant glycolipid isolated from the marine epizootic bacterium Staphylococcus lentum) prevented the adhesion of V. harveyi and P. aeruginosa (two common agricultural pathogens that infect Altemia salina), thereby limiting their ability to form biofilms, but without exerting biocidal and/or bacteriostatic activities (Hamza et al., 2017).

Other broad categories of bacterial metabolites with surface-active potential and antimicrobial actions are glycoproteins, peptides and fatty acids. A sponge-associated marine fungus isolated from Aspergillus ustus (MSF3) was capable of producing a bioactive glycolipoprotein surfactant with broad-spectrum bacteriostatic activity. More specifically, the ethyl acetate extract of MSF3 was effective in limiting the growth of C. albicans, E. coli, M. luteus and S. epidermidis (Kiran et al., 2009). Additionally, in another study, the marine isolate B. pumilus SF214 produced a small molecule of 3 kDa with anti-S. aureus activity and surface-active properties which was later identified as pumilacidin composed of a cyclic heptapeptide, a fatty acid with a variable chain length and a peptide (Glu-Leu-Leu-Leu-Asp-Leu-[(Leu/Ile)/Val]) (Saggese et al., 2018). Similarly, the marine bacteria Cobetia sp. MM1IDA2H-1 can be stimulated to produce fatty acids that form micelles, which have been shown to interfere with the fish pathogen Aeromonas salmonicida subsp. Salmonicida, either by directly affecting the pathogen or by indirectly neutralizing the pathogenic effect via their lipophilic N-acyl homoserine lactones. Either way, this does not affect the viability of the pathogens themselves but rather affects biofilm formation (Ibacache-Quiroga et al., 2013). Lastly, some marine microorganisms excrete mixtures of bioactive compounds that have a surface-lowering ability. For instance, the biosurfactant fraction produced by the marine actinomycete strains of Strepromyces B3 is a complex mixture of proteins, carbohydrates and lipids possessing anti-microbial activity against B. subtilis, E. coli, S. aureus, P. aeruginosa and C. albicans (Khopade et al., 2012). Moreover, B. amyloliquefacients SR1 produces a surfactant mixture of surfactin, iturin and fengycin molecules, each of which is known for their surface-active properties and their ability to stabilize emulsions. This mixture was found to be effective in inhibiting phytopathogens like Rhizoctonia solani, Sclerotium rolfsii, Fusarium oxysporum and Alternaria solani (Nanjundan et al., 2019). In the same way, Oceanobacillus iheyensis BK6 (isolated from a naturally occurring biofilm on the coastal region of Sikka, India) produces large amounts of exopolysaccharides (EPS) comprised of mannose, glucose and arabinose. This polysaccharide mixture has emulsifying properties and was shown to inhibit S. aureus biofilm formation by disrupting bacteria–bacteria and bacteria–surface interactions, thereby destabilizing the structure of the biofilm (Kavita et al., 20114).

Anti-Cancer Activity

Various SAAs have been described to exert anti-cancer properties (Gudiña et al., 2016). To this end, surfactin was shown to exert an anti-cancer potency against colon cancer (LoVo) cells by inhibiting their proliferation through mediation of pro-apoptotic activities and cell cycle arrest via suppression of extracellular signal-regulated kinases (ERK) and phosphatidyl inositol-3 kinase (PI3K)/v-akt murine thymoma viral oncogene homologue: protein kinase B (AKT) cell-survival signaling pathways (Kim et al., 2007).

A purified biosurfactant product (containing surfactin and fengycin isoforms; isolated from Bacillus circulans DMS-2 (MTCC 8281), was shown to possess selective anti-proliferative activity against human colon tumor (HT-29 and HCT-15) cell lines (Sivapathasekaran et al., 2010). Likewise, two fengycin isoforms, named iso-C16 fengycin B and anteiso-C17 fengycin B, extracted from marine Bacillus mojavensis B0621A, induced cytotoxicity against human leukemia (HL-60) cells (Ma et al., 2012). Iturin A, isolated from marine bacterium Bacillus megaterium, was shown to inhibit growth of MDA-MB-231 and MCF-7 breast cancer cells through reduction of phosphorylated Akt kinase levels in addition to exerting an anti-cancer capacity against MDA-MB-231 xenograft model in nude mice. The anti-cancer capacity was documented as tumor volume reduction, decreased expression levels of Ki-67 (a marker of proliferation), cluster of differentiation 31 (CD-31), phospho-Akt, P-MAPK, phosphorylated glycogen synthase kinase-3 beta (P-GSK3β) and phosphorylated fork-head box class O 3β (P-FoxO3) (Dey et al., 2015). Moreover, iturin A extracted from the same bacterium strain, re-sensitized docetaxel resistant MDA-MB-231 and MDA-MB-468 breast cancer cells by reducing phosphorylated-Akt expression levels thus leading to the subsequent inactivation of Akt (Dey et al., 2017). Rhamnolipids, a class of glycolipids derived from marine bacteria Pseudomonas aeruginosa, were also reported for their anti-tumor capacity (Chen et al., 2017). In a recent study, the cytotoxic effect of three different monorhamnolipids (Rha-C10-C10, Rha-C10-C12, and Rha-C14-C10), isolated from the arctic marine Pseudomonas sp. strain M10B774, was reported against human melanoma (A2058), breast (MCF-7) and colon (HT-29) cancer cell lines by unidentified underlined mechanisms (Kristoffersen et al., 2018).

Marine-derived surfactants appear to exert considerable anti-cancer activities in both in vitro and in vivo models, targeting a variety of molecular components implicated in major signaling and cell cycle progression pathways.

Food Applications

Surfactants and emulsifiers are exploited in foods for their surface active properties (which aid in the formation of emulsions and foams) to control dough strength in bread, modify viscosity and control fat crystallization (Orthoefer et al., 2019; Euston and Go, 2019; Ahmad et al., 2014; Young, 2014; Dickinson, 2009). Emulsifiers used in foods include proteins, polysaccharides or their varying amalgams of the two (e.g., proteoglycans, glycoproteins, etc.). For polysaccharides, the term emulsifier is something of a misnomer, and most are better described as stabilizers and while most polysaccharides can stabilize emulsions, only a few are able to emulsify oils. This is because the majority lack an amphiphilic structure, are not surface active and cannot adsorb to fluid interfaces.

The stabilizing ability of polysaccharides is associated with their ability to thicken solutions, which slows down destabilization of emulsions and foams (Dickinson, 2009). The most widely used surfactants in the food industry are mono- (MGs) and diglycerides (DGs), either mixed (MDGs), or as distilled monoglycerides (MAGs) (Young, 2014; Dickinson, 2009; Hasenhuettl, 2019). Although MDGs are the most used of food surfactants, they are under scrutiny due to perceptions of their environmental impact. Palm oil is a major source of triglycerides used in the production of MDGs. However, it has received considerable attention in the press due to extensive deforestation activities in South East Asia to enable establishment of palm oil plantations (Linder and Palkovitz, 2016; Gatti et al., 2019), and thus MDGs are under scrutiny due to perceptions of their environmental impact. Deforestation has led to extensive loss of habitat for several critically endangered species in the locale, especially the orangutan. Food manufacturers have responded, driven by consumer pressure, through reduced use of palm oil-derived products including MDGs. The concern over the sustainability and environmental impact of palm oil products is such that the European Union (EU) has considered a ban on the use of non-sustainably produced palm oil. Thus, MDGs are a major target for replacement with environmentally friendly, sustainable biosurfactants. MDGs are the main surfactants used in baked goods (breads, cakes, biscuits). In these products, the functions of surfactants are (i) emulsification of bakery fats (shortening); (ii) synergistic interactions with flour; (iii) enhancement of the properties of the shortenings; and (iv) improved aeration (Orthoefer; Kim, 2019; Ahmad, 2014; Young, 2014). MAGs are also found in several dairy products including ice-cream and whipping cream mixtures where surfactants are added to help stabilize the initial foam and to destabilise fat emulsion droplets during aeration (Euston, 2019), to act as nucleation points for the crystallization of triglycerides during cooling and to help in the air-incorporation process by promoting partial coalescence of fat globules both at the air bubble surface and in the bulk of the ice-cream/cream (Euston, 2019).

A range of surfactants have several roles in sugar confectionary, as emulsifiers in toffee, fudge and caramel (Hartel and Firoozmand, 2019), as a lubricant to control viscosity and flow properties in chocolate processing and to control fat crystallization, and in particular to reduce fat bloom, a quality flaw in chocolate. There are many examples where biosurfactants have been suggested to be potential emulsifiers, foamers and surface tension lowering agents (Campos et al., 2013; Mnif and Ghribi, 2016; Sharma, 2016; Nitschke and Silva, 2018) in food applications, but to date there have been very few reports where this has been explicitly demonstrated in food formulations.

The most common food systems where biosurfactants have been trialled are baked goods. This is perhaps not surprising as it has been known for over 60 years (Carter, 1956) that galactolipids found in wheat flour act as surfactants and improve the volume, texture, and reduce staling of bread (Selmair and Koehler, 2008; Selmair and Koehler, 2010). This suggests that glycolipids could be useful replacers for MAGs that are added to bread for the same function. While the galactolipids in wheat flour are not marine derived, galactolipids are common to all photosynthetic organisms, being found in the thylakoid membrane of the chloroplast (Kates, 1990). Thus, photosynthetic marine microorganisms such as microalgae and cyanobacteria are potential sources of galactolipids, although to date they have not been widely explored nor exploited for this.

Reports of the use of biosurfactants in foods are not explicitly for those derived from marine organisms, although biosurfactants of the types tested in foods have been identified from marine bacteria. Patented applications of rhamnolipids (although not explicitly from a marine source) in bakery products include improvement of dough stability in breads and batter stability in cakes, increased volume of bread loaf or cakes, a better structure of the crumb or crust, and an overall improvement in the shape of the product. The improved dough or batter stability gives the product additional resistance to mechanical shock during the process, so the product is less likely to collapse during fermentation or baking. When compared to common synthetic surfactants such as DATEM (diacetyl tartaric acid ester of mono- and diglycerides), which is used at levels of 0.1–0.5% to impart these improvements, rhamnolipids require only 0.025% addition levels for the same effect (Van Haesendonck and Vanzeveren, 2004). A similar improvement in bread quality was noted when the lipopeptide surfactant SPB1 (from Bacillus subtilis) was substituted for lecithin at a concentration of 0.075%. SPB1 also provided a significant anti-staling and antimicrobial effect (Mnif et al., 2012). In addition, another study has reported an improvement in cookie dough texture and overall baked cookie quality when the same SPB1 lipopeptide is used in place of GMS as a dough improver (Zouari, 2016).

Cosmetic Applications

The cosmetic industry is a growing sector believed to reach a value of 430 billion dollars by 2022 (Corinaldesi et al., 2017). To be able to assume this volume of business, the sector needs new sources of assets that are mainly oriented towards the search for ingredients of natural origin (Corinaldesi et al., 2017). One of the fundamental components of the cosmetic formulation are surfactants which are used to (i) either eliminate (cleansing) or add (emulsification) oils to the skin or hair; (ii) produce foam; (iii) obtain transparent solutions (solubilization); (iv) improve the appearance and touch after application (conditioning); and as (v) preservatives (assuming they possess anti-microbial properties) (Varvaresou & Iakovou, 2015).

Chemical surfactants are classified according to the type of the polar group present, including: (i) anionics, (ii) acyl-amino acids and salts, (iii) cationic, (iv) amphoteric surfactants, and finally (v) non-ionic surfactants, widely used as cleansing, foaming, emulsifiers, stabilizers and thickening agents (Lukic et al., 2016). However, most of the surfactants used by the cosmetic industry have been synthesized from petroleum derivatives, entailing biodegradability (due to the action of microorganisms), bioaccumulation and biocompatibility issues for the environment as well as the human health. In the latter case, several studies have demonstrated that synthetic surfactants can alter the natural barrier of the skin (causing damage and irritation) as it is the case for sodium lauryl sulphate (SLS) and sodium laureth sulphate (SLES), two widely used surfactants in the formulation of cosmetic products (Bujak et al., 2015; Lu & Moore, 2012; Morita et al., 2013). To this end, and based on the growing interest (driven by consumer demand and new environmental control legislation), cosmetic companies have switched to labelled “sulphate-free” shampoos by replacing surface-active chemical agents by naturally derived counterparts (biosurfactants). Indeed, a variety of biosurfactants (e.g., saponins, surfactin as well as rhamnolipid, sophorolipid and mannosylerythritol lipids (MEL) have been widely used in cosmetic formulations as anti-aging, anti-oxidant and anti-microbial ingredients possessing a safe profile with low toxicity (Morita et al., 2013; Draelos, 2013).

Among the potential characteristics described for biosurfactants, their property as emulsifiers is one of the most relevant for cosmetics since it facilitates the application of the product and can lower its cost given that water is the major component of such solution. For instance, Nesterenkonia sp. MS31 is an actinobacterium isolated from the marine sponge Fasciospongia cavernosa. This strain produces a lipopeptide with emulsifying capacity that is thermo-stable at a range of temperatures (4.0–121.0°C), which is of great value in the formulation and preservation of cosmetic products (Kiran et al., 2017). Furthermore, Liposan and Yansan are biosurfactants synthesized from the Brazilian marine strain of Yarrowia lipolytica, IMUFRJ50682, when grown on n-alkanes or aliphatic/aromatic hydrocarbons and perfluorocarbons respectively. Although both molecules form stable oil/water emulsions, Yansan has a higher emulsification activity and stability ranging from very acidic (pH 3.0) to very basic (pH 9.0) (Chakrabarti, 2012; Amaral et al., 2006).

Evaluation of how acidic or basic a solution is, represents a very important property for toothpaste formulation since an acidic pH can cause an abrasive effect and deteriorate dentin while a neutral or basic pH is essential for good oral health. Tooth paste formulation with a biosurfactant obtained from the marine actinobacteria Nocardiopsis VITSISB showed a more basic pH optimum than that formulated with SLS the most commonly commercially used biosurfactant (Resende et al., 2019).

In summary, data from numerous studies support the use of biosurfactants for skin care and cosmetic products formulation based on their relevant properties including, but not limited, biodegradability, biocompatibility and various relevant biological activities (e.g., antioxidant, anti-wrinkle, anti-aging, etc.).

Pharmaceutical/Biomedical Applications

In pharmaceutics and medicine, the use of biosurfactants is aimed at solubilizing poorly water-soluble drugs and to stabilize encapsulated therapeutic compounds to increase their delivery through cell membranes and biological barriers. For instance, Nifedipine and Cyclosporine are two examples of poorly water-soluble drugs. However, preparation of both compounds in aqueous solutions containing the fungal hydrophobin, SC3, results in an (i) increase of their solubility, (ii) improvement of their bioavailability, and consequently (iii) the long-lasting delivery of cyclosporine (Akanbi et al., 2010). Some biomedical applications (e.g., diagnostics (i.e., imaging), gene therapy and drug delivery) require materials at the nanoscale range (i.e., nanomaterials) that possess high stability (Pajic et al., 2017). To generate self-emulsifying delivery systems, at the nanoscale range, surfactants have been used in formulations with good emulsifying properties controlling factors such as size, shape and stability of generated nanomaterial structures thus avoiding aggregation and allowing facilitation of a uniformed morphology (Patra et al., 2018; Gudiña et al., 2013; Lawrence & Rees, 2012). In addition, surfactants such as (i) n-alkyl amine N-oxides (either on their own or in combination with lecithin), (ii) sugar surfactants (e.g., alkyl glucosides and sucrose), and (iii) polyglycerol fatty acid esters were shown to be safe and biodegradable (Lawrence & Rees, 2012). Moreover, glycolipids are the biosurfactants mostly used in the synthesis and stabilization of nanoparticles (NPs). In addition, other biosurfactants reported to be acting as stabilizers and protecting agents, for silver NPs, are the rhamnolipids (Farias et al., 2014). Finally, silver NPs synthesized from a laboratory biosurfactant (derived from Pseudomonas aeruginosa and produced from agro-industrial waste) have been reported to be “promising alternatives” to the ones using commercial rhamnolipids (Farias et al., 2014). On the other hand, metallic (mainly gold and silver) NPs are heavily used in the biomedical field with emphasis in applications related to drug delivery, photodynamic and photodermal therapy and X-ray imaging and sensing (gold NPs), as well as in antimicrobial functions (silver NPs) (Elahi et al., 2018; Qing et al., 2018). To these ends, surfactin (produced by several strains of Bacillus subtilis) has been involved in the biological synthesis of gold and silver NPs (Reddy et al., 2010; Santos et al., 2016) while sophorolipids have been reported as effective capping and reducing agents, in the synthesis of gold and silver NPs, without any observed cytotoxicity and/or genotoxicity when tested in Fusarium oxysporum, Pseudomonas stutzeri AG259, Klebsiella penumoniae, Escherichia coli, Enterobacter cloacae. However, these NPs were generated at a much lower rate than using purified surface-active agents in the reaction (Kiran et al., 2011).

Biosurfactants can also be employed as plasticizers improving flexibility in solid dosage formulations, as lubricant, wetting agents and dispersants. The anti-adherent properties of some biosurfactants make them a reliable alternative for capsule and tablet formulations. The use of sucrose fatty acids as surfactants in tablet manufacturing has resulted in better flowability and disintegration than by adding magnesium stearate, a chemical surfactant normally used for tableting (Hayes, 2011; Nakamura et al., 2017). Furthermore, biosurfactants have been also characterized for transferring genes to cells and tissues in the context of medical applications (Sekhon, 2013). For instance, mannosylerythritol lipid (MEL)-based cationic liposomes offer a promising way for gene delivery. This is a biosurfactant produced by the yeast strain Candida antarctica T-34 and has been shown to promote the interface of the liposome/nucleic acid transfection complex with a (-vely) charged cell membrane thus improving the overall gene transfection efficiency (Kitamoto et al., 2002; Nakanishi et al., 2009).

It has also been reported that cationic liposomes complexed to lipid helper cholesterol (L-dioleoylphosphatidylethanolamine (DOPE) together with the biosurfactant b-sitosterol b-D-glucoside) resulted in an improved efficiency of transferring the luciferase marker gene even in the presence of serum (which normally interferes with complex formation) (Maitani et al., 2006). Biosurfactant’s antimicrobial activity is also relevant to industrial and medical applications although currently have a limited use. Some biosurfactants (e.g., those obtained from Pediococcus acidilactici and Lactobacillus plantarum strains) have been shown to exert anti-adhesive and anti-microbial properties especially against Staphylococcus aureus CMCC26003 biofilm-related infections (Yan et al., 2019). For instance, Daptomycin (a branched cyclic lipopeptide isolated from Streptomyces roseosporus has reached a commercial use under the name of Cubicin®.This biosurfactant exerts bactericidal activity against all clinically relevant Gram (+ve) bacteria like vancomycin-resistant enterococci (VRE), methicillin-resistant Staphylococcus aureus (MRSA), intermediately susceptible Staphylococcus aureus (GISA), coagulase-negative staphylococci (CNS) and penicillin-resistant Streptococcus pneumoniae (PRSP). In addition, it can be helpful in treating endocarditis and bacteraemia caused by S. aureus as well as infections in the skin epidermis and the underlying soft tissues (Tally et al., 1999).

Finally, although marine bacteria are an unlimited source of biosurfactants they are difficult to grow under standard microbiological conditions which further limits the development of biodiscovery research. Despite that, several health-related properties have been shown for biosurfactants obtained from microorganisms growing under such conditions including anti-microbial, anti-adhesive and anti-biofilm activities against various human Gram (+ve) and Gram (-ve) bacteria as well as the yeast Candida albicans. In this context, several glycoproteins (derived from Brevibacterium casei MSA19, Serratia marcescens, Spreptomyces sp. B3, Streptomyces sp. MAB36, Aspergillus ustus MSF3) and lipopeptides (isolated from Bacillus circulans DMS-2, Bacillus licheniformis NIOT-AMKV06, Brevibacterium aureum MSA13, Nocardiopsis alba MSA10) were shown to act as antimicrobial agents (Kim et al., 2007). However, in most of the cases, the antimicrobial activity of these glycopeptide and lipopeptide fractions were only partially characterized. Even more so, the biosurfactant composition that makes Nocardiopsis dassonvillei MAD08 to be effective against several organisms is still unknown since its antimicrobial activity was studied with the crude extracts rather than the purified molecule(s). On the other hand, the lipopeptide fraction produced by Bacillus circulans is the only one described to be effective against multidrug resistance (MDR) clinical isolates (E. coli, K. pneumoniae and S. aureus), thereby making this lipopeptide an alternative to existing drugs in treating infections caused by these pathogens (Kim et al., 2007).

Other biological properties reported for marine bacteria are related to tissue remodeling. For example, the polysaccharide HE800 EPS (produced by the bacteria Vibrio diabolicus) was found to restore injured bone in rats and to promote repair and healing of a connective tissue, in vitro. Furthermore, a branched acidic heteropolysaccharide EPS GY785 (isolated from Alteromonas infernus) induced the proliferation of chondrocytes grown on a hydrogel containing the biosurfactant (Senni et al., 2011). Biocides against biocorrosion. Corrosion poses a serious hazard on the mechanical structure of buildings, transportation, piping, and automotive parts, among others. The microbiologically induced corrosion (MIC; biocorrosion) caused by both the aerobic and anaerobic bacteria is the most popular in different industrial sectors. Monitoring and control of biocorrosion cost billions of dollars every year.

In the last few years, the restrictions on the use of traditional pretreatments and organic coating for corrosion protection have been strictly limited due to both human health and environmental concerns. The threshold values for the dangerous and hazardous substances involved in the production of the most common pretreatments and organic coatings are becoming more stringent year by year. However, most of the traditional chemical inhibitors, such as amines, amides, and quaternary ammonium salts are toxic and harmful. They do not have a favorable environmental profile, and they are able to get bioaccumulated. Most chemicals also lack the required level of biodegradability imposed by legislation. The corrosion inhibitor component is now classified as environmentally friendly according to the following criteria: toxicity, bioaccumulation, and biodegradation.

Considering the increasing environmental concerns, the research studies are focused on producing and testing corrosion inhibitors that meet these conditions. The need of alternatives to conventional protection systems promoted a huge number of studies and investigations aiming at the development of innovative and effective solutions with low environmental impact. The known hazardous effects of most synthetic organic inhibitors and the need to develop cheap, nontoxic, and eco-friendly processes have now urged researchers to focus on the use of natural products. There is a need to develop new generation coatings for improved performance and environmental protection. The current strategies using chemical biocides to kill microbes, especially sulphate-reducing bacteria (SRB), have shown great success (Amaral et al., 2010). However, the use of chemical-based materials imposes hazards on the environment and humans, and current research is focusing on producing green naturally synthetized biocides. This has prompted the search for green corrosion inhibitors as eco-friendly. There are several papers that describe the use of natural resources, ranging from waste materials to plant extracts, as green corrosion inhibitors (Amaral et al., 2010; Marchant et al., 2012; De et al., 2015; Scott & Jones, 2000; Sriram et al., 2011; Mukherjee et al., 2006). Due to the limitations related with the use of chemical biocides, it is urgent to find new products with antimicrobial properties based on natural sources. This will allow us to replace the risks associated to chemical products. Therefore, the solution for this problem can be solved with the use of natural compounds with antimicrobial properties mainly produced by metabolic mechanism of microorganisms. In fact, it can be an effective alternative solution for the traditional chemical biocides’ substitution. In particular, biosurfactants are biological surface-active compounds, which present environmentally friendly properties, such as low toxicity and high biodegradability.

Potential Use in Bioremediation

As a non-renewable resource, petroleum will gradually decrease with its continuous exploration. Three methods are usually used for petroleum exploration in oil reservoir fields: primary (5–10%), secondary (30–40%), and tertiary, which is also called enhanced oil recovery (EOR) (Datta et al., 2018; Geetha et al., 2018). After primary and secondary exploration, approximately 50% of the petroleum remains underground. Thus, EOR is necessary to improve the use of petroleum in oil reservoir fields. EOR includes physical, chemical, and biological methods (Sen, 2008; Li et al., 2011; Mozhdehei et al., 2019). Physical and chemical methods mainly aim to decrease the viscosity of the petroleum to enhance petroleum recovery. However, these methods have their own limitations, such as high cost, environmental unfriendliness, and complicated operation. Thus, biological methods, which are environmentally friendly, low in cost, and easy to operate, have always attracted significant attention (She et al., 2019). Microbial enhanced oil recovery (MEOR) is the main biological method. MEOR mainly enhances oil recovery by using the life activities of microorganisms. The degradation of petroleum and the production of biosurfactant are the two key mechanisms by which microbes can enhance oil recovery (Geetha et al., 2018). Therefore, the isolation and identification of crude oil-degrading and biosurfactant-producing microorganisms are important parts of MEOR.

To date, numerous bacterial strains that can degrade petroleum or produce biosurfactant have been isolated from different oil-contaminated environments worldwide. Such strains include Chelatococcus daeguensis HB-4 from Baolige Oilfield in China (Ke et al., 2019), Rhodococcus erythropolis OSDS1 isolated from a solid waste management unit (SWMU) contaminated with petroleum hydrocarbons and heavy metals in the United States (Xia et al., 2019), Bacillus subtilis RI4914 from an oil field in Brazil (Fernandes et al., 2016), Bacillus licheniformis from oil-contaminated water samples in Egypt (El-Sheshtawy et al., 2015), Pseudomonas putida DB1 and Bacillus cereus DB2 isolated from petroleum contaminated soil in India (Vinothini et al., 2015), and B. subtilis B30 from oil-contaminated soils in Oman (Al-Wahaibi et al., 2014). As an important part of MEOR and bioremediation, biosurfactant-producing strains have been studied under different conditions (e.g., pH, temperature, salinity, and nutrition) to find the optimal conditions for biosurfactant production. In some cases, MEOR or bioremediation must occur in relatively high-salt and high-temperature conditions (Nicholson and Fathepure, 2004). Thus, salt-tolerant and thermotolerant biosurfactant producing bacteria are needed. Previously, Hua et al. (2010) introduced a salt-tolerant Enterobacter cloacae mutant that could degrade petroleum under high-salt conditions at a 7.5% NaCl concentration.

Biocides against Biocorrosion

Corrosion influenced by microbes, commonly known as microbiologically induced corrosion (MIC), is associated with biofilm, which has been one of the problems in the industry. The damages of industrial equipment or infrastructures due to corrosion lead to large economic and environmental problems. Synthetic chemical biocides are now commonly used to prevent corrosion, but most of them are not effective against the biofilms, and they are toxic and not degradable. Biocides easily kill corrosive bacteria, which are as the planktonic and sessile population, but they are not effective against biofilm. New antimicrobial and eco-friendly substances are now being developed. Biosurfactants are proved to be one of the best eco-friendly anticorrosion substances to inhibit the biocorrosion process and protect materials against corrosion. Biosurfactants have recently became one of the important products of bioeconomy with multiplying applications, while there is scare knowledge on their using in biocorrosion treatment.

Bacillus species are able to form biofilms and efficiently secrete a wide range of antimicrobial compounds, such as polymyxin B, gramicidin S, and biosurfactants, which belong to the lipopeptides family. They seem to be promising candidates to produce antimicrobials against sulphate-reducing bacteria (SRB). Jayaraman et al. (1999) and Zuo et al. (2004) reported that Bacillus species (naturally or genetically constructed) can produce antimicrobial compounds within the biofilm, resulting in the inhibition of the growth of corrosion-causing SRB and the decrease in corrosion rate of mild steel. Supernatants of the gramicidin S producers, as well as purified gramicidin S, were shown to inhibit the growth of the SRB (Zuo et al., 2004). The mechanism of action of these antimicrobial substances was shown to involve outer and cytoplasmic membrane disruption. Therefore, the use of bacteria which produce antimicrobial peptides within the biofilm complex to inhibit SRB colonisation within the biofilm is an attractive and promising preventative technique. The successful implementation of this technique would provide saving in practical applications due to the decreased use of high biocide and corrosion-inhibitor concentrations. The role of various types of biosurfactants produced by microorganisms is summarized in Table 1.

In Dagbert et al., (2006), the corrosion of stainless steel in the presence of biosurfactant produced by Gram-negative bacteria Pseudomonas fluorescens was studied. Stainless steel is frequently used in the maritime field. The biosurfactant solution delayed the corrosion of stainless steels. Zin et al. (2018) studied the influence of surface-active rhamnolipid biocomplex produced by the Pseudomonas sp. PS-17 on the corrosion and the repassivation of a freshly cut Al-Cu-Mg aluminum alloy surface. It was established that rhamnolipid biosurfactant complex, consisting of monorhamnolipid, dirhamnolipid, and polysaccharide biopolymer, effectively inhibited the alloy in synthetic acid rainwater. The efficiency of inhibition became stronger with the increase of biosurfactant concentration. However, the inhibition was minor over the critical micelle concentration. Probably the mechanism of corrosion inhibition was related to the adsorption of biosurfactant on the aluminum alloy surface, with the formation of monolayer barrier film.

Previously, it was found that both rhamnolipid biocomplex and the supernatant culture from Pseudomonas sp. PS-17 inhibited the corrosion of aluminum D16T alloy in distilled water and in 0.1% sodium chloride (Pokhmurs’kyi et al., 2014). Parthipan et al. (2018) used glycolipid biosurfactant as an eco-friendly microbial inhibitor (biocide) for the corrosion of carbon steel (API 5LX), which is extensively used in many sectors of the gas and petroleum industry. Carbon steel is the preference for the gas and oil industry because of its high resistance capacity to corrosion. However, the resistance to corrosion is changed in presence of corrosive microbial species such as sulphate reducing bacteria (SRB), acid producers, manganese oxidizing bacteria (MOB), or iron bacteria (IB).

As estimated, microbial corrosion takes place about 30%–40% of the total corrosion problems in the oil and gas industry. The Authors estimated that biosurfactant produced by Pseudomonas stutzeri F01 has the antibacterial properties of corrosive bacterial strains with a low level of concentration. Astuti et al. (2018) described the study to screen biosurfactants that had the potential to be used as an alternative biocide for biofilm associated with biocorrosion, particularly in the oil and gas industry. Eight biosurfactants belonging to glycolipid and rhamnolipid were obtained from indigenous biosurfactant-producing bacteria isolated from an oil reservoir, and their antibiofilm activity against biofilm associated biocorrosion was determined. Through this research, the biosurfactants can be used in the oil industry not only for enhanced oil recovery but also as alternative biocides. The study of Purwasena et al. (2019) showed that biosurfactant produced by indigenous oil reservoir bacteria Bacillus sp. is a good candidate for a new anticorrosion agent.

A new antimicrobial agent was being developed by using biosurfactant with antibiofilm activity, to combat biocorrosion. The minimum inhibitory concentration (MIC), minimum biofilm inhibitory concentration (MBIC), and minimum biofilm eradication concentration for 50% eradication (MBEC50) of biosurfactant against biofilm forming bacteria isolated from oil reservoir were determined, along with their effect on biofilm community structure and ability to inhibit the corrosion rate of carbon steel.

Another area where the biosurfactants and their producers are used is built heritage. It is of vital importance to develop proper remediation actions in conservation treatment based on environmentally innocuous alternatives for microbiologically contaminated historic materials. The environmentally safe and innocuous alternatives to chemical biocides are needed to commonly use during the conservative interventions. The innovative biological method, in the case of historic materials, is called either biocleaning or bioconsolidation (Fidanza et al., 2019). As presented in the literature, bacteria of the genera Bacillus are emerging as an alternative due to their capacity to produce biosurfactants with antagonistic activities against many fungal pathogens (Silva et al., 2015; Silva et al., 2016; Silva et al., 2017; Soffritti et al., 2019). Therefore, these selected microorganisms, or their products, are a potential candidate to be used as a safe, natural green biocide for cultural heritage artworks’ safeguard.

Application in the detergent industry

Biosurfactants can also be used in the detergent industry, which is considered one of the largest consumers of biosurfactants (Banat et al., 2010). The detergent field requires biosurfactants with stability at alkaline pH and thermophilic temperatures because of the washing process and performance (Grbavčić et al., 2011). Aiming at this application, Zarinviarsagh et al. (2017) observed that Ochrobactrum intermedium strain MZV101, isolated from the Gheynarje Nir hot springs in Ardebil, Iran, produced a biosurfactant with an index of emulsification of 62.2% at 60 °C and pH 10.0 and a positive result for the drop collapse assay and oil spreading assay. Additionally, the biosurfactant remained stable under alkaline conditions of pH (5.0–13.0), presenting the best results at pH 10.0–13.0 and high temperatures of 60–90 °C.

In recent years, the detergent industry has assessed the environmental impact of their products, and new directions have been established, such as the development of formulations for washing products containing biosurfactants for an effective detergency at lower temperatures, which will help laundry practices to save energy and reduce the environmental impact (Perfumo et al., 2018). Low-temperature microbiology has recently become an area of interest for this biotechnological application.

Challenges and future directions

The production of biosurfactants from extremophiles presents challenges that must be overcome to make production and commercialization feasible on a commercial scale for application in different biotechnological aspects. Some limitations are the same as mesophilic microorganisms and are widely discussed, such as the costs of biosurfactant production, productivity on a large scale, foaming production and product loss in the recovery and purification processes and final price of the product (Winterburn and Martin, 2012; Banat et al., 2014). Specifically, for the production of biosurfactant by extremophiles, it should be acknowledged that although micro-organisms from extreme environments have attractive characteristics for biotechnological applications, it is difficult to find microbial strains that produce high yields when grown in the particular environments for industrial applications. Part of the challenge is due to the difficulty of mimicking extreme conditions in the laboratory that allow these micro-organisms to synthesize the target bioproducts (Adrio and Demain, 2014). This attempt requires a large investment of funds, energy, development and adaptation of the necessary cropping methods, which makes the process more expensive and not marketed widely due to excessive cost (Coker, 2016; Krüger et al., 2018).

Currently, to overcome the challenges of extremophile cultivation and to verify the capacity of biosurfactant production by cultivated and noncultivated species from extreme environments, we have sought the assistance of omic tools, such as metagenomic and metatranscrip-tomic analysis (Perfumo et al., 2018), that have allowed us to make considerable leaps in understanding the remarkable complexity and versatility of extremophiles (Cowan et al., 2015). These technologies allow rapid identification of the genetic potentials and new metabolites that can also be used for the generation of new synthetic products and knowledge of metabolic pathways with optimal performance, without the necessity of cultivating the microorganism (Khan and Kihara, 2014).

For the mining of (new) biosurfactants in metagenomes, the total DNA is directly extracted from the environmental sample and sequenced, offering the opportunity to explore all the operons and coding genes for biosurfactant bio-synthesis presented in the sample (Sachdev and Cameotra, 2013). According to the authors, the genes related to the biosynthesis of bacterial surfactants lie in a gene cluster of approximately 3000–7000 bp. With technological advances and the evolution of tools for data processing and analysis, it is possible to analyze a substantial number of gene-encoding bioproducts that are of interest for basic and applied research, and bioinformatic tools, such as anti-SMASH, aid in the gene mining that is involved in the synthesis of biosurfactants in these metagenomes (Aleti et al., 2015).Research can also be carried out based on the similarity of the metagenomic sequences against a gene or protein database, requiring a complete and cured database of information relevant to biomolecule producers, such as biosurfactants. With this demand, Oliveira et al., (2015) developed BioSurf DB, a database designed that models key concepts and relations in the areas of biosurfactant production as well as biodegradation, providing data on 3736 genes, 3430 proteins, 1077 organisms, and 58 pathways and a list of 96 cured biosurfactants grouped by producing microorganisms, name and class of the surfactant. The existence of cured databases for biosurfactant producers of and tools for analysis is an answer to the necessity for functional analysis of the microbial community and the screening of biosurfactant producers isolated from extreme environments, as it will aid in the development of pipelines for the mass analysis of metagenomes and will allow specificity in the search for this biomolecule.

Recently, it has been possible to recover genomes from metagenomes (MAG) by binning metagenomic contigs according to their coverage and tetranucleotide frequency, followed by an estimation of the bin quality (Ramos-Barbero et al., 2019) and bioinformatic tools allow specific microbes to be linked to their metabolic capacities (Sangwan et al., 2016). The first reconstructed MAG was Leptospirillum GII and Ferroplasma t.II from an acidophilic biofilm from acid mine drainage (Tyson et al., 2004).

In the same way as the metagenomic analysis, the mining of genetic capacities for the production of biosurfactant can be used in the MAGs. There is also metagenomic library screening, which provides access to new bioactive molecules, such as biosurfactants, but requires the combination of adequate host organisms with a functional expression system and an effective screening pathway (Gabor et al. 2007). According to Sachdev and Cameotra (2013), this functional metagenomic approach seems a promising technique for biosurfactant mining. The first study with this approach was developed by Thies et al., (2016) and used Escherichia coli DH10b as a host to express the metagenomic genes encoding biosurfactants, which was subsequently submitted to high-through-put screening for biosurfactants, producing clones to identify N-acyltyrosine. The use of this method for metagenomes from extreme environments is an opportunity that has not been explored.

When the cultivation of extremophiles with culture medium that mimics the conditions of the extreme environment is possible in the laboratory, complete sequencing of the isolate genome can be performed. By the mining techniques described above, the genes involved in biosurfactant production can be searched and visualized in pathways, and the corresponding metabolisms can be related. Advances in biosurfactant knowledge at the genome level will also significantly improve our ability to interpret metagenomic data since functional metagenomics may lead to the discovery of unknown biosurfactants and is especially suitable for extreme habitats (Cowan et al., 2014; Jackson et al., 2015).

CONCLUSION 

Marine environments are a promising source for a large variety of surface-active metabolites. Undoubtedly, their chemical diversity is much larger than described until today and the structures of many biosurfactants still remain unknown. Furthermore, the oceans comprise a large diversity of habitats and should contain many more biosurfactant producing organisms to be discovered, in particular, in promising niches like communities associated with filter-feeding invertebrates or sites affected by toxic pollution. Here, sampling and subsequent enrichment culturing of biosurfactant producing microbes or culture-independent methods, like functional or sequence-based metagenomics, will allow retrieval of surfactant biosynthetic DNA from these niches. The availability of affordable and fast sequencing methods and bioinformatic tools for the analysis of biosynthetic pathways and metabolic networks will furthermore facilitate the elucidation of the yet largely unknown biosynthesis pathways for marine biosurfactants thereby enabling the development of synthetic biology derived concepts to construct efficient recombinant production strains. All these interdisciplinary research efforts will contribute to the identification, production and application of novel marine biosurfactants.

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