Plant carbohydrate scavenging through tonB-dependent receptors: a feature shared by phytopathogenic and aquatic bacteria.
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.
Blanvillain
Servane
S
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
D
Boulanger
Alice
A
Lautier
Martine
M
Guynet
Catherine
C
Denancé
Nicolas
N
Vasse
Jacques
J
Lauber
Emmanuelle
E
Arlat
Matthieu
M
D001419:Bacteria / Q000378:metabolism; D001425:Bacterial Outer Membrane Proteins / Q000737:chemistry / Q000235:genetics / Q000502:physiology*; D001426:Bacterial Proteins / Q000502:physiology*; D001693:Biological Transport, Active; D019607:Brassicaceae / Q000382:microbiology*; D050260:Carbohydrate Metabolism; D017124:Conserved Sequence; D015964:Gene Expression Regulation, Bacterial; D005798:Genes, Bacterial; D055029:Inverted Repeat Sequences; D007501:Iron / Q000378:metabolism; D008565:Membrane Proteins / Q000502:physiology*; D016254:Mutagenesis, Insertional; D010802:Phylogeny; D010935:Plant Diseases / Q000382:microbiology*; D017434:Protein Structure, Tertiary; D018085:Regulon / Q000235:genetics; D013045:Species Specificity; D013395:Sucrose / Q000378:metabolism*; D014774:Virulence; D014871:Water Microbiology; D016959:Xanthomonas campestris / Q000235:genetics / Q000378:metabolism* / Q000472:pathogenicity
D001425:Bacterial Outer Membrane Proteins; D001426:Bacterial Proteins; D008565:Membrane Proteins; C057616:tonB protein, Bacteria; D013395:Sucrose; D007501:Iron