Novel features of the polysaccharide-digesting gliding bacterium Flavobacterium johnsoniae as revealed by genome sequence analysis

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

Research output: Contribution to journalArticle

140 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)6864-6875
Number of pages12
JournalApplied and Environmental Microbiology
Volume75
Issue number21
DOIs
StatePublished - Nov 2009

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Flavobacterium johnsoniae
Flavobacterium
gliding
polysaccharide
Polysaccharides
Sequence Analysis
polysaccharides
sequence analysis
genome
Genome
Bacteria
bacterium
gene
bacteria
motility
Bacteroidetes
Genes
protein
adhesins
genes

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McBride, Mark J. ; Xie, Gary ; Martens, Eric C. ; Lapidus, Alla ; Henrissat, Bernard ; Rhodes, Ryan G. ; Goltsman, Eugene ; Wang, Wei ; Xu, Jian ; Hunnicutt, David W. ; Staroscik, Andrew M. ; Hoover, Timothy R. ; Cheng, Yi Qiang ; Stein, Jennifer L. / Novel features of the polysaccharide-digesting gliding bacterium Flavobacterium johnsoniae as revealed by genome sequence analysis. In: Applied and Environmental Microbiology. 2009 ; Vol. 75, No. 21. pp. 6864-6875.
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author = "McBride, {Mark J.} and Gary Xie and Martens, {Eric C.} and Alla Lapidus and Bernard Henrissat and Rhodes, {Ryan G.} and Eugene Goltsman and Wei Wang and Jian Xu and Hunnicutt, {David W.} and Staroscik, {Andrew M.} and Hoover, {Timothy R.} and Cheng, {Yi Qiang} and Stein, {Jennifer L.}",
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McBride, MJ, Xie, G, Martens, EC, Lapidus, A, Henrissat, B, Rhodes, RG, Goltsman, E, Wang, W, Xu, J, Hunnicutt, DW, Staroscik, AM, Hoover, TR, Cheng, YQ & Stein, JL 2009, 'Novel features of the polysaccharide-digesting gliding bacterium Flavobacterium johnsoniae as revealed by genome sequence analysis', Applied and Environmental Microbiology, vol. 75, no. 21, pp. 6864-6875. https://doi.org/10.1128/AEM.01495-09

Novel features of the polysaccharide-digesting gliding bacterium Flavobacterium johnsoniae as revealed by genome sequence analysis. / McBride, Mark J.; Xie, Gary; Martens, Eric C.; Lapidus, Alla; Henrissat, Bernard; Rhodes, Ryan G.; Goltsman, Eugene; Wang, Wei; Xu, Jian; Hunnicutt, David W.; Staroscik, Andrew M.; Hoover, Timothy R.; Cheng, Yi Qiang; Stein, Jennifer L.

In: Applied and Environmental Microbiology, Vol. 75, No. 21, 11.2009, p. 6864-6875.

Research output: Contribution to journalArticle

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T1 - Novel features of the polysaccharide-digesting gliding bacterium Flavobacterium johnsoniae as revealed by genome sequence analysis

AU - McBride, Mark J.

AU - Xie, Gary

AU - Martens, Eric C.

AU - Lapidus, Alla

AU - Henrissat, Bernard

AU - Rhodes, Ryan G.

AU - Goltsman, Eugene

AU - Wang, Wei

AU - Xu, Jian

AU - Hunnicutt, David W.

AU - Staroscik, Andrew M.

AU - Hoover, Timothy R.

AU - Cheng, Yi Qiang

AU - Stein, Jennifer L.

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N2 - 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.

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