What Is in Store for EPS Microalgae in the Next Decade?

molecules Review What Is in Store for EPS Microalgae in the Next Decade? Guillaume Pierre 1 ,Cédric Delattre 1,2 , Pascal Dubessay 1,Sébastien Jubeau 3, Carole Vialleix 4, Jean-Paul Cadoret 4, Ian Probert 5 and Philippe Michaud 1,* 1 Université Clermont Auvergne, CNRS, SIGMA Clermont, Institut Pascal, F-63000 Clermont-Ferrand, France; [email protected] (G.P.); [email protected] (C.D.); [email protected] (P.D.) 2 Institut Universitaire de France (IUF), 1 rue Descartes, 75005 Paris, France 3 Xanthella, Malin House, European Marine Science Park, Dunstaffnage, Argyll, Oban PA37 1SZ, Scotland, UK; [email protected] 4 GreenSea Biotechnologies, Promenade du sergent Navarro, 34140 Meze, France; [email protected] (C.V.); [email protected] (J.-P.C.) 5 Station Biologique de Roscoff, Place Georges Teissier, 29680 Roscoff, France; probert@sb-roscoff.fr * Correspondence: [email protected]; Tel.: +33-(0)4-73-40-74-25 Academic Editor: Sylvia Colliec-Jouault Received: 12 October 2019; Accepted: 15 November 2019; Published: 25 November 2019 Abstract: Microalgae and their metabolites have been an El Dorado since the turn of the 21st century. Many scientific works and industrial exploitations have thus been set up. These developments have often highlighted the need to intensify the processes for biomass production in photo-autotrophy and exploit all the microalgae value including ExoPolySaccharides (EPS). Indeed, the bottlenecks limiting the development of low value products from microalgae are not only linked to biology but also to biological engineering problems including harvesting, recycling of culture media, photoproduction, and biorefinery. Even respecting the so-called “Biorefinery Concept”, few applications had a chance to emerge and survive on the market. Thus, exploiting EPS from microalgae for industrial applications in some low-value markets such as food is probably not a mature proposition considering the competitiveness of polysaccharides from terrestrial plants, macroalgae, and bacteria. However, it does not imply drawing a line on their uses but rather “thinking them” differently. This review provides insights into microalgae, EPS, and their exploitation. Perspectives on issues affecting the future of EPS microalgae are also addressed with a critical point of view. Keywords: microalgae; exopolysaccharides; EPS; application; market 1. Introduction Polysaccharides which are the most abundant carbohydrates in nature are high molecular weight biopolymers (10 to 1000 kDa) with complex structures and various physico-chemical properties. They are mainly composed of pentoses and/or hexoses linked by glycosidic bonds leading to linear or ramified homo- and heteropolymers. Depending on the nature of monosaccharides, kinds of glycosidic bonds, presence of some non-sugar constituents (sulfates, organic acid, methyl, amino acids, or amine), they are rigid or flexible macromolecules with various levels of solubility in water. The monosaccharides which are most commonly present in their structures are d-xylose, d-glucose, d-galactose, and d-mannose and some corresponding N-acetylaminosugars and uronic acids. Compared to polysaccharides from terrestrial plants, fungi and macroalgae, eukariotic and prokariotic microbial polysaccharides have probably the higher structural diversity [1–3]. These microbial polysaccharides have various biological functions. They can be energetic reserve (starch or glycogen), structural components serving structural and protective purposes (β-glucans or peptidoglycan) or excreted Molecules 2019, 24, 4296; doi:10.3390/molecules24234296 www.mdpi.com/journal/molecules Molecules 2018, 23, x FOR PEER REVIEW 2 of 25 Molecules 2019, 24, 4296 2 of 25 glycogen), structural components serving structural and protective purposes (β-glucans or peptidoglycan) or excreted outside the cells to form (or not) mucilaginous layers with not well- definedoutside functions. the cells to Indeed, form (or some not) of mucilaginous the roles ascrib layersed to with these not exocellular well-defined microbial functions. polysaccharides Indeed, some alsoof the called roles exopolysaccharides ascribed to these exocellular (EPS) are microbialprotective polysaccharides barrier, sorption also of calledorganic exopolysaccharides and/or inorganic compounds,(EPS) are protective binding barrier, of enzymes, sorption sink of organic for excess and/ orenergy, inorganic adhe compounds,sion, biofilm, binding protection of enzymes, from antimicrobialsink for excess agents energy, including adhesion, predators, biofilm, protectionexportation from of cell antimicrobial components, agents water including retention predators, bacteria aggregation,exportation ofand cell components,nutrient source water for retention a bacterial bacteria community aggregation, [3]. and The nutrient marine source and for freshwater a bacterial environmentscommunity [ 3harbor]. The the marine main andpart freshwaterof the microbia environmentsl biomass on harbor Earth. Among the main this part microbial of the microbialbiomass, microbialbiomass onphotoautotrophs Earth. Among including this microbial microalgae biomass, and microbial cyanobacteria photoautotrophs have been poorly including investigated microalgae to produceand cyanobacteria metabolites have such been as EPS poorly despite investigated their potential. to produce Indeed, metabolites the number such asof EPSmicroalgae despite theirand cyanobacteriapotential. Indeed, species the has number been ofestimated microalgae to about and cyanobacteria 800,000 species. species Among has beenthem estimated only 50,000 to abouthave been800,000 identified species. [4–6], Among and less them than only 100 50,000 have havebeen described been identified to produce [4–6], EPS and [2]. less These than EPS 100 producers have been aredescribed mainly toCyanobacteria produce EPS rather [2]. These than EPSeukaryotic producers microalgae are mainly [2,7]. Cyanobacteria This number ratheris very than low compared eukaryotic tomicroalgae of bacteria [ 2producing,7]. This number EPS (Figure is very 1). lowNote compared that in the to last of decade, bacteria the producing number EPSof references (Figure1 ).on Note EPS inthat microalgae in the last are decade, equal theto that number on bacteria, of references suggesting on EPS that in microalgae microalgae are producing equal to thatEPS onare bacteria, not so overlooked.suggesting that microalgae producing EPS are not so overlooked. 5000 60 4500 50 4000 3500 40 3000 2500 30 2000 20 1500 1000 10 Polyaccharides and Polyaccharides bacteria 500 Polysaccharides and microalgae 0 0 2000 2002 2004 2006 2008 2010 2012 2014 2016 2018 Years Figure 1. Number of references per year between 2000 and 2018 using the key words “polysaccharides Figureand bacteria” 1. Number () of or references “polysaccharides per year and between microalgae” 2000 an (d 2018). using the key words “polysaccharides and bacteria” () or “polysaccharides and microalgae” (⬛). What is the explanation of this lack of knowledge about EPS from microalgae? Probably the bestWhat answer is the is that explanation the culture of this of theselack of microorganisms knowledge about is oftenEPS from complex microalgae? and diffi Probablycult (notably the best for answereukaryotic is that microalgae) the culture compared of these with microorgani heterotrophicsms cultureis often of complex non-photosynthetic and difficult microorganisms. (notably for eukaryoticTheir generation microalgae) time compared is high, most with of heterotrophi them are noc culture axenic, of some non-photosynthetic of them are very microorganisms. shear sensitive, Theirthe biomass generation concentration time is high, is most very lowof them after are autotrophic no axenic, cultures,some of them and some are very microalgae shear sensitive, can require the biomassunknown concentration (or poorly controlled) is very low culture after conditions autotrop (e.g.,hic cultures, irradiance and and some composition microalgae of culture can require media). unknownMoreover, (or the culturepoorly conditionscontrolled) to culture obtain EPSconditions by microalgae (e.g. irradiance are not always and thecomposition same as those of culture leading media).to biomass Moreover, production. the culture For example, conditions the well-known to obtain EPS red marineby microalgae microalgae, are abundantlynot always publishedthe same foras thosethe production leading ofto EPS,biomass required production. specific culture For exam conditionsple, the including well-known nitrogen red starvation marine and microalgae,/or specific abundantlyN/P ratios topublished produce exocellularfor the prod polysaccharidesuction of EPS, [required8]. There specific are numerous culture classical conditions culture including media nitrogenthat were starvation developed and/or for microalgae specific N/P maintenance ratios to produce or isolation exocellu butlar not polysaccharides for biomass and [8]. metabolites There are numerousproduction. classical The recent culture emergence media that of technologies were develo forped industrial for microalgae exploitation maintenance of microalgae or isolation is currently but notchanging for biomass this story. and metabolites The culture production. and processing The ofrecent microalgae emergence is not of reallytechno alogies problem for ofindustrial biology exploitationbut rather a of problem microalgae of biological is currently engineering. changing this The story. production The culture of metabolites and processing

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