Carbohydrate Polymers 205 (2019) 8–26 Contents lists available at ScienceDirect Carbohydrate Polymers journal homepage: www.elsevier.com/locate/carbpol Extremophilic exopolysaccharides: A review and new perspectives on engineering strategies and applications T ⁎ ⁎ Jia Wanga,d, David R. Salema,b,c, , Rajesh K. Sania,c,d, a Department of Chemical and Biological Engineering, South Dakota School of Mines and Technology, Rapid City, SD 57701, USA b Department of Materials and Metallurgical Engineering, South Dakota School of Mines and Technology, Rapid City, SD 57701, USA c Composite and Nanocomposite Advanced Manufacturing – Biomaterials Center (CNAM-Bio Center), Rapid City, SD 57701, USA d BuG ReMeDEE consortium, South Dakota School of Mines and Technology, Rapid City, SD 57701, USA ARTICLE INFO ABSTRACT Keywords: Numerous microorganisms inhabiting harsh niches produce exopolysaccharides as a significant strategy to Extremophile survive in extreme conditions. The exopolysaccharides synthesized by extremophiles possess distinctive char- Exopolysaccharide acteristics due to the varied harsh environments which stimulate the microorganisms to produce these biopo- Exopolysaccharide property lymers. Despite many bioprocesses have been designed to yield exopolysaccharides, the production of exopo- Exopolysaccharide biosynthesis lysaccharides by extremophiles is inefficient compared with mesophilic and neutrophilic exopolysaccharide Exopolysaccharide application producers. Meanwhile, the industrial development of novel extremophilic exopolysaccharides remains con- strained due to the lack of exploration. In this review, we summarize the structure and properties of various exopolysaccharides produced by extremophiles, and also discuss potential metabolic and genetic engineering strategies for enhanced yield and modified structure of extremophilic exopolysaccharides. Special focus is given to the applications of extremophilic exopolysaccharides in the areas of biomedicine, food industry, and bio- materials via nano-techniques, casting and electrospinning. 1. Introduction studied during the past several decades and applied in a variety of in- dustrial areas. In addition to xanthan gum, dextran and gellan gum are In the past few decades, extremophilic microorganisms and some of currently being used in the food industry (Donot, Fontana, Baccou, & their metabolites were reported in light of their particular biosynthetic Schorr-Galindo, 2012; Rehm, 2010). Bacterial polysaccharides possess a mechanisms, functions, and properties which can permit the strains to great diversity of properties that may not be found in more traditional be habitant in extreme niches. Among all the products from ex- polymers of plant origin. Several EPSs have also demonstrated them- tremophiles, exopolysaccharides (EPSs) have led to significant interest selves as useful materials without the environmental disadvantages due to the increasing demand for natural polymers in various industrial associated with synthetic polymers (Chawla, Bajaj, Survase, & Singhal, fields. EPSs are high molecular weight carbohydrate biopolymers, 2009; Freitas, Alves, & Reis, 2011; Guezennec, 2002). composed of sugar residues, and are secreted by microorganisms into Currently, it is widely accepted that extremophilic microorganisms the surrounding environment, providing certain properties and func- will provide a valuable resource for exploitation in novel biotechnolo- tions useful to the microorganisms (Nicolaus, Kambourova, & Oner, gical processes, including synthesis of unique EPSs (Bhalla, Bansal, 2010; Poli, Anzelmo, & Nicolaus, 2010). The EPS molecular chains have Kumar, Bischoff, & Sani, 2013; Nicolaus et al., 2010). The environments a broad range of molecular weights, and different microorganisms can that extremophiles inhabit are obviously more inhospitable than the synthesize a wide variety of EPSs with a diverse range of functions, such environmental pressures inducing common mesophilic and neutrophilic as intercellular signal transduction, molecular recognition, protection microbes to secrete their EPSs. Extremophiles have to adapt to hostile against predation, adhesion, biofilm formation, construction of a com- environments through unique mechanisms, and the biosynthesis of fortable extracellular environment, and pathogenic processes (Moriello EPSs is one of their vital survival mechanisms. Extremophilic micro- et al., 2003; Nicolaus et al., 1999). Some of the EPSs with valuable organisms inhabiting different extreme environments have been re- physicochemical properties have already been utilized in industry. For cognized as promising producers of EPSs, and the examination of EPS instance, among all the reported EPSs, xanthan gum has been most production by extremophiles (thermophiles, halophiles, alkaliphiles, ⁎ Corresponding authors at: Department of Chemical and Biological Engineering, South Dakota School of Mines and Technology, Rapid City, SD 57701, USA. E-mail addresses: [email protected] (D.R. Salem), [email protected] (R.K. Sani). https://doi.org/10.1016/j.carbpol.2018.10.011 Received 2 August 2018; Received in revised form 20 September 2018; Accepted 4 October 2018 Available online 09 October 2018 0144-8617/ © 2018 Elsevier Ltd. All rights reserved. J. Wang et al. Carbohydrate Polymers 205 (2019) 8–26 Fig. 1. The EPS from different kinds of extremophiles and potential applications. psychrophiles, and acidophiles) has revealed an abundance of novel microorganisms can survive in high temperatures, and their EPS pro- properties that may have strong potential in industrial applications duction has been a proposed adaptation mechanism to enable their (Fig. 1). survival in these extreme conditions. Although more and more novel extremophiles have been isolated, The growth media for thermophiles, containing sugars as carbon and their unique EPSs characterized, the research depth of ex- and energy sources, have always been considered a primary target to be tremophilic EPSs is still not comparable with EPSs from mesophilic or optimized for maximum production of EPSs. Disaccharides such as neutrophilic microorganisms with regard to biosynthetic pathways, maltose, lactose and sucrose are the optimized carbon source for most regulatory mechanisms, and engineering strategies. It is necessary to of thermophilic bacteria for EPS production. Besides chemical compo- make a comprehensive summarization concerning the structures and sition and molecular weight, thermophilic EPSs have been character- characteristics of the recently described extremophilic EPSs, which can ized mostly in terms of thermostability. The highest decomposition provide crucial fundamentals for further exploitation of engineering temperature of 280 °C is from an EPS produced by Geobacillus tepida- strategies to obtain tailor-made extremophilic EPSs with desired yield mans (Table 1). The summarized data suggest that the type of sugar and functions. The targeted cultivation of extremophilic bacteria subunits present in the EPS may affect their thermostability. The through metabolic and genetic engineering will eventually pave the modification of monomer sugars or some other residues in EPSs can be way for industrial level applications of extremophilic EPSs. utilized to find out the active sites for certain functions (e.g., thermo- This article reviews the EPSs produced by various kinds of ex- stability) of EPSs. Although a relatively unexplored area with a sparse tremophilic bacteria, including an inventory of extremophilic EPSs of database, there is already significant evidence that EPSs from thermo- industrial interest, as well as promising engineering strategies for philes possess a broad range of interesting properties for industrial higher yield or modified molecular structure of extremophilic EPSs. applications (Nicolaus et al., 2004, 2010). The literature to date in- Moreover, the recent advances in the actual and potential applications dicates that further screening and systematic investigation of EPSs of EPSs produced by extremophilic bacteria are presented. produced by thermophiles, in conjunction with advances in under- standing the biochemistry of microbial EPS synthesis, will result in the 2. EPSs produced by different extremophile types discovery of novel biopolymers of commercial importance. 2.1. EPSs produced by thermophiles 2.2. EPSs produced by psychrophiles Elevated temperature generally increases the rate of most chemical Psychrophiles can be isolated from Antarctic, Arctic, or deep-sea reactions and improves cumulative production in a given time frame. sediment, and they predominate in marine ecosystems (Ewert & Thus, thermophiles can be of commercial value in the synthesis of Deming, 2013; Li, Zhou, Zhang, Wang, & Zhu, 2008; Nevot, Deroncele, important compounds, and are of growing interest to many sectors of Montes, & Mercade, 2008; Nichols, Bowman, & Guezennec, 2005). The industry. Although EPS production is lower than most of the meso- EPSs from psychrophilic marine bacteria are generally carboxylated philes, the uncommonly short fermentation process, which is usually no polysaccharides, and the carboxyl groups confer a net negative charge more than 24 h, makes thermophiles important contenders as com- and acidic properties to the EPSs at the pH of seawater (pH around 8) mercially competitive EPS producers (Kambourova et al., 2009; (Caruso et al., 2017; Casillo, Parrilli et al., 2017). The negative charge Radchenkova et al., 2013; Yildiz et al., 2014). The thermophilic strains of psychrophilic