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Molecular Aspects of Bacterial Nanocellulose Biosynthesis

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Molecular Aspects of Bacterial Nanocellulose Biosynthesis bs_bs_banner Molecular aspects of bacterial nanocellulose biosynthesis Paulina Jacek,1 Fernando Dourado,2 Brown, who observed the production of cellulose by Ace- Miguel Gama2,* and Stanisław Bielecki1 tobacter xylinum cells in the presence of oxygen and 1Institute of Technical Biochemistry, Lodz University of glucose (Brown, 1886). Meanwhile, classification of Technology, 4/10 Stefanowskiego Str 90-924, Lodz, acetic acid bacteria has changed, Acetobacter being Poland. reclassified as Gluconacetobacter, which has recently 2Centre of Biological Engineering, University of Minho, further moved to a new type of Komagataeibacter. The Campus de Gualtar, 4710-057 Braga, Portugal. current generic name as proposed in 2012 by Yuzo Yamada (Yamada et al., 2012) comes from the name of the Japanese microbiologist Kazuo Komagata. Summary Among the many BNC producers, we can distinguish nitrogen-binding bacteria (Rhizobium leguminosarum), Bacterial nanocellulose (BNC) produced by aerobic plant pathogens (Dickeya dadantii), Agrobacterium bacteria is a biopolymer with sophisticated technical tumefaciens, Escherichia coli, Salmonella enterica, Pseu- properties. Although the potential for economically domonas putida and bacteria of the genus Koma- relevant applications is huge, the cost of BNC still lim- gataeibacter, currently regarded as one of the most its its application to a few biomedical devices and the efficient producers of this exopolysaccharide (Romling€ edible product Nata de Coco, made available by tradi- and Galperin, 2015). Current literature indicates a particu- tional fermentation methods in Asian countries. Thus, lar interest in bacterial strains of the species Koma- a wider economic relevance of BNC is still dependent gataeibacter hansenii, which, due to an interesting on breakthrough developments on the production phenotype and high cellulose yield, became a model technology. On the other hand, the development of organism used for genetic, molecular and biochemical modified strains able to overproduce BNC with new studies (Florea, et al., 2016b). The number of reports of properties – e.g. porosity, density of fibres crosslink- bacteria producing BNC continues to grow, as well as the ing, mechanical properties, etc. – will certainly allow annotation of the putative operons of cellulose synthase in to overcome investment and cost production issues whole bacterial genome sequences, suggesting that more and enlarge the scope of BNC applications. This and wider groups of bacteria may be capable of producing review discusses current knowledge about the molec- cellulose (Solano et al., 2002; Chawla et al., 2009; Esa ular basis of BNC biosynthesis, its regulations and, et al., 2014; Matsutani et al., 2015; Keshk and El-Kott, finally, presents a perspective on the genetic modifi- 2016; Moniri et al., 2017; Reiniati et al., 2017). cation of BNC producers made possible by the new Of particular interest in Komagataeibacter strains is tools available for genetic engineering. the study of molecular aspects of BNC biosynthesis. Genetic engineering is a powerful tool being used to pro- duce valuable strains to increase the efficiency of BNC Introduction biosynthesis, as will be further presented below. Bacterial nanocellulose (BNC) is a linear polysaccharide b composed of -D-glucopyranose monomers linked by Molecular mechanisms of BNC biosynthesis by b -1,4-glycosidic linkages. The repeating unit is the Komagataeibacter genus disaccharide cellobiose (McNamara et al., 2015). Bacte- rial nanocellulose was first described in 1886 by A. J. The biochemical reactions of BNC biosynthesis by K. xylinus are very well characterized (Brown, 1987; Delmer and Amor, 1995). This is a precise and specifi- Received 25 October, 2018; revised 3 February, 2019; accepted 8 cally regulated multi-step process, involving numerous February, 2019. *For correspondence. E-mail [email protected]; individual enzymes and complexes of catalytic and regu- Tel. +351253604418; Fax +351253678986. latory proteins. However, their supramolecular structure Microbial Biotechnology (2019) 12(4), 633–649 has not yet been fully defined. The pathways and mech- doi:10.1111/1751-7915.13386 Funding Information anisms of the synthesis of uridine diphosphoglucose No funding information provided. (UDP-Glc) are relatively well known, while the molecular ª 2019 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 634 P. Jacek, F. Dourado, M. Gama and S. Bielecki mechanisms of glucose polymerization in long and since its activity in cellulose-producing bacteria is one unbranched chains still need to be further investigated. hundred times higher than in the non-producing counter- Bacterial nanocellulose is synthesized in two stages, parts (Valla et al., 1989). the first being the production of b-1,4-glucan chains and As shown in Fig. 1, the biosynthesis of BNC is closely the second the crystallization of cellulose (Brown and related to many metabolic pathways, such as the pentose- Saxena, 2000). The conversion of glucose to cellulose phosphate (PP) pathway, Embden–Meyerhof–Parnas requires four enzymatic steps (Fig. 1): phosphorylation (EMP) pathway, the Krebs cycle (TCA) and gluconeogen- of glucose by glucokinase to glucose-6-phosphate esis (GNG) (Lee et al., 2014; Nagashima et al., 2016). (G6P); isomerization of glucose-6-phosphate to glucose- Many different compounds, such as hexoses, glycerol, 1-phosphate (G1P) by phosphoglucomutase (PGM); con- dihydroxyacetone, pyruvate or dicarboxylic acids, can be version of glucose-1-phosphate to uridine diphosphate converted to cellulose. Pyruvate, like glycerol, dihydroxy- glucose (UDP-glucose) by UDP-glucose pyrophosphory- acetone and intermediates of the pentose monophos- lase; and finally, the synthesis of cellulose from UDP- phate cycle can be converted into glucose-6-phosphate glucose by cellulose synthase (Bcs), a complex of four by gluconeogenesis (Krystynowicz et al., 2005). On the subunits, BcsA, BcsB, BcsC and BcsD, which are other hand, disaccharides, such as sucrose or maltose, encoded by three (bcsAB, bcsC and bcsD) or four are first hydrolysed to monosaccharides and then also (bcsA, bcsB, bcsC and bcsD) genes (Ross et al., 1991; converted to glucose-6-phosphate (Lee et al., 2014). Jedrzejczak-Krzepkowska et al., 2016). UDP-glucose Due to the lack or very low phosphofructokinase (pfk) pyrophosphorylase is a key enzyme in this process, activity, certain cellulose-producing bacteria, such as Fig. 1. Pathways for the biosynthesis of BNC by K. xylinus and assembly of cellulose molecules into nanofibrils: (1) Glucokinase-ATP, (2) Phosphoglucomutase, (3) Glucose-6-phosphate dehydrogenase, (4) 6-phosphogluconate dehydrogenase, (5) Phosphorribulose isomerase, (6) Phosphorribulose epimeraase, (7) Transaketolase, (8) Transaldolase, (9) Phosphoglucoisomerase, (10) Fructokinase, (11) Fructokinase ATP, (12) Aldolase, (13) Triosephosphate isomerase, (14) Glyceraldehyde 3-phosphate dehydrogenase, (15) Phosphoglycerate mutase, (16) Eno- lase, (17) Pyruvate kinase (18) Pyruvate biphosphate kinase, (19) Pyruvate dehydrogenase, (20) Alcohol dehydrogenase and (21) Aldehyde dehydrogenase. ª 2019 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology., Microbial Biotechnology, 12, 633–649 Molecular biology of bacterial nanocellulose production in bacteria 635 K. xylinus, are unable to use EMP pathway for pyruvate glucanase (CMCax) flanking genes, a complementary synthesis from glucose. Alternatively, pyruvate is cellulose factor (CcpAx) and b-glucosidase (BglAx). Cel- obtained from acetate and is used to synthesize glucose lulose synthase is an enzymatic complex containing three through the GNG pathway (Velasco-Bedran and Lopez- (bcsAB, bcsC, bcsD) or four (bcsA, bcsB, bcsC, bcsD) Isunza, 2007; Sarkar et al., 2010; Zhong et al., 2013). subunits encoded by genes found in the bcs (bacterial The PP cycle involves the oxidation of carbohydrates, cellulose synthase) operon (Fig. 2). In 1994, the cellulose and the TCA cycle involves the oxidation of acetate- synthase complex bcsABCD was discovered in K. xyli- derived carbohydrates, fat and proteins, such as oxalo- nus (Saxena et al., 1994). The protein subunits included succinate and a-ketoglutarate. Nevertheless, K. xylinus in the cellulose synthase complex and the accessory pro- is not able to metabolize glucose anaerobically since it teins fulfil various functions identified in Table 1. lacks phosphofructose kinase, which is required for gly- The crystallographic structure of the BcsA and BcsB colysis (Lee et al., 2014). subunits of the cellulose synthase complex from The model of Komagataeibacter metabolism, proposed Rhodobacter sphaeroides was resolved for the first time by Velasco-Bedran and Lopez-Isunza, indicates the con- in 2013 (Morgan et al., 2013). The BcsA and BcsB sub- nection between catabolic pathways of ethanol, glucose units form the core of the cellulose synthase complex, and fructose (Velasco-Bedran and Lopez-Isunza, 2007). anchored in the inner cell membrane. This core is extre- The G6P can be metabolized into acetate via phospho- mely important for the production of BNC, both in vivo ketolase pathway, linking glucose and ethanol catabolic and in vitro (Romling€ and Galperin, 2015). The BcsA pathways.
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