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Marine Biosurfactants: Biosynthesis, Structural Diversity and Biotechnological Applications

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Marine Biosurfactants: Biosynthesis, Structural Diversity and Biotechnological Applications marine drugs Review Marine Biosurfactants: Biosynthesis, Structural Diversity and Biotechnological Applications Sonja Kubicki 1, Alexander Bollinger 1 , Nadine Katzke 1, Karl-Erich Jaeger 1,2 , 1, , 1, , Anita Loeschcke * y and Stephan Thies * y 1 Institute of Molecular Enzyme Technology, Heinrich-Heine-University Düsseldorf, Forschungszentrum Jülich, D-52425 Jülich, Germany 2 Institute of Bio- and Geosciences IBG-1: Biotechnology, Forschungszentrum Jülich GmbH, D-52425 Jülich, Germany * Correspondence: [email protected] (A.L.); [email protected] (S.T.) These authors contributed equally in conceptualising and coordinating activities. y Received: 17 June 2019; Accepted: 7 July 2019; Published: 9 July 2019 Abstract: Biosurfactants are amphiphilic secondary metabolites produced by microorganisms. Marine bacteria have recently emerged as a rich 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 deduced from biochemical analyses and genome sequences of marine microbes indicates a high structural diversity including a broad spectrum of fatty acid derivatives, lipoamino acids, lipopeptides and glycolipids. This review aims to summarise biosyntheses and structures with an emphasis on low molecular weight biosurfactants produced by marine microorganisms and describes various biotechnological applications with special emphasis on their role in the bioremediation of oil-contaminated environments. Furthermore, novel exploitation strategies are suggested in an attempt to extend the existing biosurfactant portfolio. Keywords: marine biosurfactants; structural diversity; glycolipids; lipopeptides; oil degradation; biotechnological application; biosynthetic mechanisms; heterologous expression; synthetic biology 1. 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 [1]. 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 [2,3]. More than 2000 distinct biosurfactant structures are currently known, covering chemically different families of compounds, but also groups of congeners, that is, structurally closely related compounds with minor structural variations [4]. 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 [5]. Bioactivities of biosurfactants include antibacterial, antifungal and anti-tumour effects. At the same time, ecological Mar. Drugs 2019, 17, 408; doi:10.3390/md17070408 www.mdpi.com/journal/marinedrugs Mar. Drugs 2019, 17, 408 2 of 30 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 [6,7]. These properties form the basis of the pronounced interest in this class of metabolites [8] 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 [8]. 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 [9–12]. This article aims to provide an overview of the structural diversity of low molecular-weight biosurfactants produced by marine microbes reported until May 2019. Furthermore, applications for the degradation of marine oil spills are expounded. Finally, strategies for future biotechnological exploitations of such compounds are discussed. 2. 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 by small hydroxyl, phosphate or carboxyl groups, or by 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 [4]. Besides the grouping by charge, surface-active secondary metabolites can be broadly classified into high and low molecular weight biosurfactants [13,14]. 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. 2.1. 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 [15], are produced by many bacteria of different species. They constitute polysaccharides, proteins, lipopolysaccharides, lipoproteins, or complex mixtures of these compounds referred to as lipoheteropolysaccharides. The prototypical HMW bioemulsifier emulsan is produced, for instance, by Acinetobacter calcoaceticus RAG-1, an isolate from the Mediterranean Sea [16,17]. 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 [4,18] 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 organised in a single wee gene cluster of 27 kilo base pairs [19]. 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 [20]. Hydrophobins are small proteins secreted by different filamentous fungi [21] which are also surface-active and may represent promising targets for biotechnology [22]. Mar. Drugs 2019, 17, 408 3 of 30 2.2. Low Molecular Weight Biosurfactants Low molecular weight (LMW) biosurfactants range from simple free fatty acids and phospholipids to amino acids linked to lipids, to 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 [23–25]. (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 [26–29]. 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 [30,31], with the antibiotics daptomycin from Streptomyces roseosporus and polymyxin B from Paenibacillus polymyxa as prominent examples [32,33]. 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 [34,35]. Glycolipids, similar to the emulsan repeating unit, consist of mono- or oligosaccharides and a lipid moiety.
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