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Microbial Exopolysaccharides: Main Examples of Synthesis, Excretion, Genetics

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Microbial Exopolysaccharides: Main Examples of Synthesis, Excretion, Genetics Carbohydrate Polymers 87 (2012) 951–962 Contents lists available at SciVerse ScienceDirect Carbohydrate Polymers jo urnal homepage: www.elsevier.com/locate/carbpol Review Microbial exopolysaccharides: Main examples of synthesis, excretion, genetics and extraction a,b,∗ a a a F. Donot , A. Fontana , J.C. Baccou , S. Schorr-Galindo a UMR Qualisud (CIRAD, Université Montpellier II, UM1, Sup Agro), Place E. Bataillon, 34095 Montpellier Cedex 5, France b Total Petrochemicals France, Pôle Recherche et Développement Mont/Lacq, 64170 Lacq, France a r t i c l e i n f o a b s t r a c t Article history: Exopolysaccharides (EPSs) produced by microorganisms represent an industrially untapped market. − Received 5 May 2011 1 Some microorganisms can produce and excrete over 40 g L of EPS in simple but costly production Received in revised form 18 August 2011 conditions. Accepted 24 August 2011 Approximately thirty strains of eukaryotic and prokaryotic microorganisms are notable for their EPS Available online 31 August 2011 production. EPSs are produced in response to biotic and abiotic stress factors and/or to adapt to an extreme environment. The main function of EPSs is to aid in protection against environmental pressures. Keywords: Heteropolysaccharides and some homopolysaccharides are synthesised in microbial cells and then Exopolysaccharides Microorganisms secreted into the extracellular environment. More currently, homopolysaccharide synthesis occurs out- Synthesis side of the cells after specific enzymes are exuded. Excretion Although natural secretory mechanisms exist in microorganisms, it is often necessary to resort to Industrial process physical or chemical extraction methods to improve the yield of EPSs at an industrial level. In light of growing interest, our basic understanding of microbial EPSs needs to be improved. © 2011 Elsevier Ltd. All rights reserved. Contents 1. Introduction ... 951 2. EPSs of microbial origin and their physiological roles. 952 3. Biosynthesis, exudation and genetics. 953 3.1. Homopolysaccharides . 953 3.1.1. Levan . 954 3.1.2. Pullulan . 955 3.1.3. Curdlan. 956 3.2. Heteropolysaccharides: the example of xanthan . 957 3.3. Genetics of EPS synthesis. 957 4. EPS extraction methods . 958 5. Prospects . 960 Acknowledgment . 960 References . 960 1. Introduction activities (Liu et al., 2010). They are derived from a wide variety of Polysaccharides are industrially used as thickeners, stabilis- sources: bacterial, fungal, algal and plant. Despite the many sources ers and gelling agents in food products. More recently they were of polysaccharides, the world market is dominated by polysaccha- used as depollution agents and there was a growing interest in rides from algae and higher plants (Jonas & Farrah, 1998; Leung, their biological functions like antitumor, antioxidant or prebiotic Liu, Koon, & Fung, 2006). These biopolymers are obtained by direct extraction from biomass and may be subjected to chemical hydrol- ysis or fermentation to obtain the smallest molecules able to be ∗ polymerised (Pichavant, 2009). Corresponding author at: UMR Qualisud (CIRAD, Université Montpellier II, UM1, Higher plants are the primary source of polysaccharides, which Sup Agro), Place E. Bataillon, 34095 Montpellier Cedex 5, France. E-mail address: fl[email protected] (F. Donot). include starch, cellulose, pectins and “gums”. Polysaccharides come 0144-8617/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.carbpol.2011.08.083 952 F. Donot et al. / Carbohydrate Polymers 87 (2012) 951–962 from plant cell walls in the form of cellulose or lignin. Polysaccha- absence of competition with arable land. Furthermore, EPSs are rides are also stored as starch for reserves (Reddy & Yang, 2005). naturally exuded by most microorganisms into the extracellular Cellulose, mainly from cotton plants (Gossypium sp.), is the most environment (Bejar, Llamas, Calvo, & Quesada, 1998; Chen, Hsu, exploited biopolymer today. Galactomannane, or “gum”, is another Lin, Lai, & Wu, 2006; Chi, Pyle, Wen, Frear, & Chen, 2007; Li, Schenk, commonly used polysaccharide in the food industry. It is produced Srivastava, Zhurina, & Ullrich, 2006; Ravella et al., 2010; Survase, from Guar (Cyamopsis tetragonolobus) and Locust Beans (Ceratonia Saudagar, & Singhal, 2006; Tsujisaka & Mitsuhashi, 1993), facili- siliqua) (Bourbon et al., 2010). tating their recovery. The main factors limiting EPS production by As for starch, 60 million tons are extracted per year from differ- microorganisms are linked to the costs of production. The main ent cereal crops, including maize and wheat, and roots and tubers, costs consist of purchasing substrate in certain cases and acquir- such as manioc and potatoes. Starch is used in various applications: ing the infrastructures required for production, which can include as a stabiliser for soups and frozen foods, a pill coating, a paper bioreactors and maintaining asepsis. covering and as a raw material to produce ethanol. The purpose of this bibliographical review is to make an inven- The principal polysaccharides from red algae (Rhodophyceae) tory of the EPSs of industrial interest produced by microorganisms and brown algae (Phaeophyceae) are the following classes: including bacteria, yeasts, moulds and microalgae. This review will carrageenans, derived from Kappaphycus alvarezii and Euchema present the principal pathways of EPS biosynthesis and describe denticulum; alginates, derived from Laminaria sp., Pelvetia sp., Sar- the mechanisms of naturally occurring excretion and of industrially gassum sp., Ecklonia sp. and Undaria sp.; agar, derived from Gelidium induced extraction. sp. and Gracilaria sp.; and fucans, derived from Stichopusc sp. and Laminaria sp. (De Ruiter & Rudolph, 1997; Li, Chen, Yi, Zhang, & Ye, 2010). Polysaccharides were first marketed in the 1930s in the 2. EPSs of microbial origin and their physiological roles United States. Today, annual world production of polysaccharides from marine biomass is approximately 25 000–30 000 tons per year As the first step of this review, an inventory was made of the (Pichavant, 2009). main EPSs produced by microorganisms, including yeasts, moulds, Polysaccharides derived from microorganisms, including bac- bacteria and microalgae (Tables 1 and 2). teria, yeasts and moulds, represent an unexploited market The microbial species are presented with their optimal EPS pro- (Sutherland, 2001). Polysaccharide biosynthesis and accumulation duction quantities and a description of the associated substrates generally take place after the growth phase of the microorganism. and growth conditions. The polysaccharides produced by microorganisms can be classi- The molecules are varied in nature and are produced in variable −1 fied into three main groups according to their location in the cell: concentrations, ranging from 0.0022 to 86.3 g L (Tables 1 and 2). (i) cytosolic polysaccharides, which provide a carbon and energy Both eukaryotic and prokaryotic microbial groups are repre- source for the cell; (ii) polysaccharides that make up the cell wall, sented, but bacteria produce the greatest diversity of molecules −1 including peptidoglycans, techoïd acids and lipopolysaccharides and produce quantities of over 10 g L . and (iii) polysaccharides that are exuded into the extracellu- Of the 35 inventoried strains, 15 belong to fungal or algal species. −1 lar environment in the form of capsules or biofilm, known as Among these species, only 4 are capable of producing over 10 g L . exopolysaccharides (EPSs). EPSs are divided into two groups: Half of the 20 bacterial strains cited produce EPSs in concentrations −1 homopolysaccharides and heteropolysaccharides. Homopolysac- of over 10 g L . charides are made up of a single type of monosaccharide, like The physiological role of EPSs depends on the biotope of dextran or levan. Heteropolysaccharides are made up of several the microorganisms producing them. EPS production is a direct types of monosaccharide like xanthans or gellans, have complex response to selective environmental pressures, including tem- structures and are usually synthesised inside the cell in the form perature, pressure and light intensity (Dudman, 1977; Otero & of repeating units (Bergmaier, 2002; Lahaye, 2006; Roger, 2002). Vincenzini, 2003). These EPSs affect the way in which microor- Heteropolysaccharides make up the majority of bacterial EPSs. EPS ganisms interact with the external environment, whether the biosynthesis can be divided into three main steps: (i) assimilation environment is liquid or solid. of a carbon substrate, (ii) intracellular synthesis of the polysaccha- Microorganisms are often associated in a biofilm of high cel- rides and (iii) EPS exudation out of the cell (Vandamme, De Baets, & lular density. The glycocalyx, which is mainly composed of EPSs, Steinbüchel, 2002). EPSs aid the cell in various functions. EPSs pro- is essential for the formation of a biofilm. The EPSs can influence tect against biotic stress, like competition, and abiotic stresses that the stability of a biofilm through interactions between the polysac- might include temperature, light intensity or pH. In the cases of aci- charide chains (Higgins & Novak, 1997). EPSs allow the microbial dophilic or thermophilic species and Archaea, EPSs aid in adapting flora to adhere to a biological support, which may constitute a sub- to extreme conditions. Despite the wide diversity of microbial EPSs strate for the microorganism growth. Apart from playing a role in with physicochemical properties
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