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PMID: 17311090 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Plant carbohydrate scavenging through tonB-dependent receptors: a feature shared by phytopathogenic and aquatic bacteria.

PloS one ·Vol. 2 ·No. 2 ·2007-02-21 ·Pages e224

Blanvillain S, Meyer D, Boulanger A, Lautier M, Guynet C, Denancé N, Vasse J, Lauber E, Arlat M

Abstract

TonB-dependent receptors (TBDRs) are outer membrane proteins mainly known for the active transport of iron siderophore complexes in Gram-negative bacteria. Analysis of the genome of the phytopathogenic bacterium Xanthomonas campestris pv. campestris (Xcc), predicts 72 TBDRs. Such an overrepresentation is common in Xanthomonas species but is limited to only a small number of bacteria. Here, we show that one Xcc TBDR transports sucrose with a very high affinity, suggesting that it might be a sucrose scavenger. This TBDR acts with an inner membrane transporter, an amylosucrase and a regulator to utilize sucrose, thus defining a new type of carbohydrate utilization locus, named CUT locus, involving a TBDR for the transport of substrate across the outer membrane. This sucrose CUT locus is required for full pathogenicity on Arabidopsis, showing its importance for the adaptation to host plants. A systematic analysis of Xcc TBDR genes and a genome context survey suggested that several Xcc TBDRs belong to other CUT loci involved in the utilization of various plant carbohydrates. Interestingly, several Xcc TBDRs and CUT loci are conserved in aquatic bacteria such as Caulobacter crescentus, Colwellia psychrerythraea, Saccharophagus degradans, Shewanella spp., Sphingomonas spp. or Pseudoalteromonas spp., which share the ability to degrade a wide variety of complex carbohydrates and display TBDR overrepresentation. We therefore propose that TBDR overrepresentation and the presence of CUT loci designate the ability to scavenge carbohydrates. Thus CUT loci, which seem to participate to the adaptation of phytopathogenic bacteria to their host plants, might also play a very important role in the biogeochemical cycling of plant-derived nutrients in marine environments. Moreover, the TBDRs and CUT loci identified in this study are clearly different from those characterized in the human gut symbiont Bacteroides thetaiotaomicron, which allow glycan foraging, suggesting a convergent evolution of TBDRs in Proteobacteria and Bacteroidetes.

MeSH Terms
Bacteria/metabolism Bacterial Outer Membrane Proteins/chemistry,genetics,physiology Bacterial Proteins/physiology Biological Transport, Active Brassicaceae/microbiology Carbohydrate Metabolism Conserved Sequence Gene Expression Regulation, Bacterial Genes, Bacterial Inverted Repeat Sequences Iron/metabolism Membrane Proteins/physiology Mutagenesis, Insertional Phylogeny Plant Diseases/microbiology Protein Structure, Tertiary Regulon/genetics Species Specificity Sucrose/metabolism Virulence Water Microbiology Xanthomonas campestris/genetics,metabolism,pathogenicity
Chemicals
Bacterial Outer Membrane Proteins Bacterial Proteins Membrane Proteins tonB protein, Bacteria Sucrose Iron
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Blanvillain Servane
Laboratoire des Interactions Plantes-Microorganismes, Centre National de la Recherche Scientifique (CNRS)/Institut National de la Recherche Agronomique (INRA) UMR2594/441, Castanet-Tolosan, France.
Meyer Damien
Boulanger Alice
Lautier Martine
Guynet Catherine
Denancé Nicolas
Vasse Jacques
Lauber Emmanuelle
Arlat Matthieu
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Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
DOI
10.1371/journal.pone.0000224
Published
2007-02-21
Epub
2007-00-21
Pages
e224
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC1790865
Subset
IM
External Links
PubMed source DOI: 10.1371/journal.pone.0000224 PMC Full Text View journal details
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