Trends in Microbiology
Volume 23, Issue 9, September 2015, Pages 545-557
Journal home page for Trends in Microbiology

Review
Bacterial cellulose biosynthesis: diversity of operons, subunits, products, and functions

https://doi.org/10.1016/j.tim.2015.05.005Get rights and content

Highlights

  • Cellulose is produced by a wide variety of environmental and pathogenic bacteria.

  • There are at least four distinct types of cellulose biosynthesis and export operons.

  • Cellulose is a key component of bacterial biofilms, and it regulates virulence.

  • Some cellulose synthase subunits have known structures, others remain uncharacterized.

  • The properties of cellulose fibers make cellullose an attractive material for bionanotechnology.

Recent studies of bacterial cellulose biosynthesis, including structural characterization of a functional cellulose synthase complex, provided the first mechanistic insight into this fascinating process. In most studied bacteria, just two subunits, BcsA and BcsB, are necessary and sufficient for the formation of the polysaccharide chain in vitro. Other subunits – which differ among various taxa – affect the enzymatic activity and product yield in vivo by modulating (i) the expression of the biosynthesis apparatus, (ii) the export of the nascent β-D-glucan polymer to the cell surface, and (iii) the organization of cellulose fibers into a higher-order structure. These auxiliary subunits play key roles in determining the quantity and structure of resulting biofilms, which is particularly important for the interactions of bacteria with higher organisms – leading to rhizosphere colonization and modulating the virulence of cellulose-producing bacterial pathogens inside and outside of host cells. We review the organization of four principal types of cellulose synthase operon found in various bacterial genomes, identify additional bcs genes that encode components of the cellulose biosynthesis and secretion machinery, and propose a unified nomenclature for these genes and subunits. We also discuss the role of cellulose as a key component of biofilms and in the choice between acute infection and persistence in the host.

Section snippets

Cellulose production

Cellulose, poly-β-(1→4)-D-glucose, is the key component of plant cell walls and the most abundant biopolymer on this planet. In fact, it was the sight of the cellulose ‘cells’ in cork that prompted Robert Hooke to coin the term ‘cell’ in the first place. Cellulose is incredibly stable and can withstand washing in strong hot acid or alkali, heating, stretching, and other challenges. You are probably reading this text printed on paper, wearing a cotton T-shirt, and sitting in a wooden chair by a

Diversity of the bcs operons

Substrate synthesis for cellulose production starts from the glycolytic intermediate glucose-6-phosphate. The first committed reaction, isomerization of glucose-6-phosphate to glucose-1-phosphate, is catalyzed by phosphoglucomutase (EC 5.4.2.2). Glucose-1-phosphate then reacts with UTP, forming uridine-5′-diphosphate-α-D-glucose (UDP-glucose) in a rate-limiting reaction catalyzed by UTP–glucose-1-phosphate uridylyltransferase (EC 2.7.7.9). Finally, cellulose synthase (BCS, EC 2.4.1.12)

Structure and functions of individual subunits

Bacterial synthesis of cellulose occurs at the cytoplasmic side of the (inner) membrane, and elongation of the nascent molecule must be tightly linked to its secretion. Accordingly, in addition to the catalytic glucosyltransferase subunit BcsA, BCS complexes include a variety of subunits that ensure orderly export of the growing polysaccharide chain. We present here a brief description of the BCS subunits.

Diversity of cellulose products

The diversity of the bcs operons and the respective enzymes might reflect the diversity of their cellulose products. Some bcs-like operons encode BcsA-like glucosyltransferases that produce alternative polysaccharides, such as the β-(1→3)-D-glucan curdlan [45] or the mixed-linkage (1→3,1→4)-β-D-glucan [46]. Another example is acetylated cellulose produced by Pseudomonas fluorescens 8, 47. But even if the glucan product is a chemically simple β-1,4-glucose polymer, glucan chains become arranged

Regulation of cellulose biosynthesis

Bacterial cellulose biosynthesis is regulated on both transcriptional and post-translational levels. Expression of the bcs genes appears to be controlled by different regulators in different bacteria (e.g., by Fis in D. dadantii), but is generally stimulated during biofilm formation, as compared with the log phase 21, 49. The BCS activity in vivo depends on the presence of both BCS subunits and its allosteric regulator c-di-GMP. Accordingly, transcriptional regulators such as Salmonella enterica

Ecology of cellulose biosynthesis

Besides stability and rigidity, bacterial cellulose has a high capacity for water retention. As a common exopolysaccharide component in the extracellular biofilm matrix of ecologically diverse bacteria, from the thermophilic cyanobacterium T. vulcanus to the gastrointestinal pathogen S. enterica 21, 30, cellulose mediates cell–cell interactions, cell adherence, and biofilm formation on biotic and abiotic surfaces 8, 21, 60. A gradual increase in cellulose production prepares bacteria for

Applications of cellulose synthase

From the bioengineering perspective, bacterial cellulose has certain advantages over plant cellulose, including its high purity, high capacity for water retention, and the nano-scale arrangement of the cellulose fibrils. These features make bacterial cellulose an attractive biocompatible material, which is already commercially available as a wound dressing material for complicated wounds such as skin ulcers 77, 78. Potential applications of bacterial cellulose and its derivatives also include

Concluding remarks

Plant-derived cellulose is not just the most abundant biopolymer on Earth, it is also the only fully renewable one. Understanding the mechanisms of its synthesis – and using this knowledge to optimize energy generation and production of novel industrial and medical materials – has long been the dream of many biologists and engineers. Bacterial cellulose biosynthesis, while taking place on a somewhat smaller scale, is of geochemical, ecological, agricultural, and medical importance. The recent

Acknowledgments

We thank the members of the Römling laboratory for comments on this manuscript. This work was supported by the Swedish Research Council Natural Sciences and Engineering, the Karolinska Institutet and Petrus and Augusta Hedlund Foundation (to U.R.), and the NIH Intramural Research Program at the U.S. National Library of Medicine (M.Y.G.).

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