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Novel Features of the Polysaccharide-Digesting Gliding Bacterium Flavobacterium johnsoniae as Revealed by Genome Sequence Analysis
Authors:Mark J McBride  Gary Xie  Eric C Martens  Alla Lapidus  Bernard Henrissat  Ryan G Rhodes  Eugene Goltsman  Wei Wang  Jian Xu  David W Hunnicutt  Andrew M Staroscik  Timothy R Hoover  Yi-Qiang Cheng  Jennifer L Stein
Abstract:The 6.10-Mb genome sequence of the aerobic chitin-digesting gliding bacterium Flavobacterium johnsoniae (phylum Bacteroidetes) is presented. F. johnsoniae is a model organism for studies of bacteroidete gliding motility, gene regulation, and biochemistry. The mechanism of F. johnsoniae gliding is novel, and genome analysis confirms that it does not involve well-studied motility organelles, such as flagella or type IV pili. The motility machinery is composed of Gld proteins in the cell envelope that are thought to comprise the “motor” and SprB, which is thought to function as a cell surface adhesin that is propelled by the motor. Analysis of the genome identified genes related to sprB that may encode alternative adhesins used for movement over different surfaces. Comparative genome analysis revealed that some of the gld and spr genes are found in nongliding bacteroidetes and may encode components of a novel protein secretion system. F. johnsoniae digests proteins, and 125 predicted peptidases were identified. F. johnsoniae also digests numerous polysaccharides, and 138 glycoside hydrolases, 9 polysaccharide lyases, and 17 carbohydrate esterases were predicted. The unexpected ability of F. johnsoniae to digest hemicelluloses, such as xylans, mannans, and xyloglucans, was predicted based on the genome analysis and confirmed experimentally. Numerous predicted cell surface proteins related to Bacteroides thetaiotaomicron SusC and SusD, which are likely involved in binding of oligosaccharides and transport across the outer membrane, were also identified. Genes required for synthesis of the novel outer membrane flexirubin pigments were identified by a combination of genome analysis and genetic experiments. Genes predicted to encode components of a multienzyme nonribosomal peptide synthetase were identified, as were novel aspects of gene regulation. The availability of techniques for genetic manipulation allows rapid exploration of the features identified for the polysaccharide-digesting gliding bacteroidete F. johnsoniae.Flavobacterium johnsoniae (formerly Cytophaga johnsonae) is a member of the large and diverse phylum of gram-negative bacteria known as the Bacteroidetes. Members of this group of organisms have a number of unique characteristics that distinguish them from other bacteria. Some have novel cell surface machinery to utilize polysaccharides (85, 95, 96). Rapid gliding motility over surfaces is also common among these bacteria (59), as are unusual outer membrane sulfonolipids (29) and flexirubin pigments (78). Bacteroidete gene expression and regulation also have novel aspects (10, 11, 20, 39, 92). The many unusual features of these common but understudied bacteria provide numerous avenues for further exploration, which can be greatly aided by analysis of genome sequences.F. johnsoniae digests many polysaccharides and proteins, but it is best known for its ability to rapidly digest insoluble chitin (87). Chitin is one of the most abundant biopolymers on earth (63). F. johnsoniae and other members of the Bacteroidetes phylum are thought to play important roles in the turnover of this compound in many environments (47). F. johnsoniae has become a model system for the study of bacteroidete gliding motility biochemistry and molecular biology (20, 27-29, 59, 72). This paper highlights novel features of the F. johnsoniae genome, with particular emphasis on genes and proteins likely to be involved in polysaccharide utilization, gliding motility, and the novel biochemistry of this organism.
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