Cellulose in Bacterial Biofilms
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Many bacteria produce cellulose as an exopolysaccharide component of the extracellular matrix in biofilms, which are large aggregates of bacterial cells often attached to abiotic or biotic surfaces. Cellulose has been particularly well studied in two model bacteria, Komagataeibacter xylinus and Escherichia coli. The widely conserved bacterial cellulose synthase consists of a membrane-inserted core complex, whose BcsA subunit provides for a glucosyltransferase activity that is allosterically activated by the second messenger c-di-GMP and which, together with the BcsB subunit, forms a transmembrane channel for co-synthetic secretion of cellulose. Various accessory Bcs proteins further conduct cellulose to the cell surface, where glucan chains are aligned and assembled into higher order fibrils. The corresponding genes are generally organized in operons that are easily detected in genome sequences. K. xylinus produces highly crystalline cellulose, which alone or in technically generated composite materials is now widely used in food and paper technology or in medical applications. A surprise in the bacterial cellulose field was the recent discovery that E. coli and many other bacteria “decorate” their cellulose with a phospholipid-derived phosphoethanolamine (pEtN) group in a post-synthetic process catalyzed by BcsG at the outer side of the cytoplasmic membrane. This enzymatic process not only represents the first natural chemical modification of cellulose but enables pEtN-cellulose to form nanocomposites with amyloid fibers in the extracellular matrix of biofilms. The result is tissue-like cohesion and elasticity, which allow growing macrocolony or pellicle biofilms to buckle up and fold into macroscopic morphological patterns of wrinkles and high ridges. These recent discoveries hold promise that other types of modified cellulose with novel chemical and biomechanical properties are yet be found in nature or could even be generated by synthetic biology approaches.
Research in the Hengge lab mentioned in this review has been funded by the Deutsche Forschungsgemeinschaft (DFG grants He1556/17-1, He1556/20-1, and He1556/21-1 to RH), the European Research Council under the European Union’s Seventh Framework Programme (ERC-AdG 249780 to R.H.), and the Alexander von Humboldt Foundation (postdoctoral fellowship to DOS).
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