Abstract
Agrobacterium tumefaciens pathogens genetically modify their host plants to drive the synthesis of opines in plant tumors. Opines are either sugar phosphodiesters or the products of condensed amino acids with ketoacids or sugars. They are Agrobacterium nutrients and imported into the bacterial cell via periplasmic-binding proteins (PBPs) and ABC-transporters. Mannopine, an opine from the mannityl-opine family, is synthesized from an intermediate named deoxy-fructosyl-glutamine (DFG), which is also an opine and abundant Amadori compound (a name used for any derivative of aminodeoxysugars) present in decaying plant materials. The PBP MotA is responsible for mannopine import in mannopine-assimilating agrobacteria. In the nopaline-opine type agrobacteria strain, SocA protein was proposed as a putative mannopine binding PBP, and AttC protein was annotated as a mannopine binding-like PBP. Structural data on mannityl-opine-PBP complexes is currently lacking. By combining affinity data with analysis of seven x-ray structures at high resolution, we investigated the molecular basis of MotA, SocA, and AttC interactions with mannopine and its DFG precursor. Our work demonstrates that AttC is not a mannopine-binding protein and reveals a specific binding pocket for DFG in SocA with an affinity in nanomolar range. Hence, mannopine would not be imported into nopaline-type agrobacteria strains. In contrast, MotA binds both mannopine and DFG. We thus defined one mannopine and two DFG binding signatures. Unlike mannopine-PBPs, selective DFG-PBPs are present in a wide diversity of bacteria, including Actinobacteria, α-,β-, and γ-proteobacteria, revealing a common role of this Amadori compound in pathogenic, symbiotic, and opportunistic bacteria.
Highlights
Agrobacterium tumefaciens pathogens have adapted a strategy of niche construction inside the plant hosts
This work establishes a structural basis for the high mannopine specificity of the periplasmic binding proteins (PBPs) MotA, encoded by the Ti-plasmid of octopine/mannityl opines-type and agrocinopine/mannityl opines-type Agrobacterium strains
No DFG transporter has been characterized in a mannopine-assimilating agrobacteria strain
Summary
MotA belongs to the mannopine transport system encoded by the Ti plasmid of the A. tumefaciens strain B6 (Fig. 1) [24]. MotA and the mannopine-degrading enzyme MocC are not present in this strain, which cannot grow when mannopine is the sole source of carbon and nitrogen. A. tumefaciens strain C58 can grow when DFG is the sole resource [25]. The constitutive expression of the mannopine-degrading enzyme MocC in A. tumefaciens C58 conferred upon this strain the capability to grow on mannopine. Baek et al [25] identified the region of the pAt carrying the socA gene (encoding the PBP SocA) and socB gene (encoding the associated ABC transporter) as responsible for both DFG and mannopine import in wild-type strain C58 and its MocC-expressing derivative, respectively. This work led to the identification of fingerprint sequences that define mannopine and/or DFG binding PBPs and provides new insights into the utilization of mannopine and DFG in host-interacting bacteria
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