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Applied and Environmental Microbiology, November 2009, p. 6864-6875, Vol. 75, No. 21
0099-2240/09/$08.00+0     doi:10.1128/AEM.01495-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Novel Features of the Polysaccharide-Digesting Gliding Bacterium Flavobacterium johnsoniae as Revealed by Genome Sequence Analysis{triangledown} ,{dagger}

Mark J. McBride,1* Gary Xie,2,3 Eric C. Martens,4,5 Alla Lapidus,3 Bernard Henrissat,6 Ryan G. Rhodes,1 Eugene Goltsman,3 Wei Wang,7 Jian Xu,4,7 David W. Hunnicutt,8 Andrew M. Staroscik,9 Timothy R. Hoover,10 Yi-Qiang Cheng,1 and Jennifer L. Stein10

University of Wisconsin—Milwaukee, Milwaukee, Wisconsin,1 Los Alamos National Laboratory, Bioscience Division, Los Alamos, New Mexico,2 Department of Energy Joint Genome Institute, Walnut Creek, California,3 Washington University School of Medicine, St. Louis, Missouri,4 University of Michigan Medical School, Ann Arbor, Michigan,5 Architecture et Fonction des Macromolécules Biologiques, UMR 6098, Centre National de la Recherche Scientifique and Universities of Aix-Marseille I & II, Marseille, France,6 BioEnergy Genome Center, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences (CAS-QIBET), Qingdao, China,7 St. Norbert College, DePere, Wisconsin,8 University of Rhode Island, Kingston, Rhode Island,9 University of Georgia, Athens, Georgia,10

Received 25 June 2009/ Accepted 22 August 2009

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.

* Corresponding author. Mailing address: Department of Biological Sciences, University of Wisconsin—Milwaukee, 3209 N. Maryland Ave., 181 Lapham Hall, Milwaukee, WI 53211. Phone: (414) 229-5844. Fax: (414) 229-3926. E-mail: mcbride{at}uwm.edu

{triangledown} Published ahead of print on 28 August 2009.

{dagger} Supplemental material for this article may be found at http://aem.asm.org/.

Applied and Environmental Microbiology, November 2009, p. 6864-6875, Vol. 75, No. 21
0099-2240/09/$08.00+0     doi:10.1128/AEM.01495-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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