Common scab disease: structural basis of elicitor recognition in pathogenic Streptomyces species

Abstract

In Streptomyces scabiei, the main causative agent of common scab disease of root and tuber crops, the interaction between the substrate-binding protein (SBP) CebE (CebEscab) and cellotriose released by the plant host (KD in the nanomolar range) is the first event for the onset of its pathogenic lifestyle. Here we report the structure of CebEscab in complex with cellotriose at a 1.55 [A] resolution, adopting a general fold of the B subcluster of SBPs. The interaction between CebEscab and cellotriose involves multiple direct or water-mediated hydrogen bonds and hydrophobic interactions, the glucose monomer at the non-reducing end occupying the most conserved part of the substrate-binding cleft. As main interactions between the two domains of CebE involve cellotriose itself, the closed conformational state of CebE is performed via an induced-fit ligand binding mechanism where cellotriose binding triggers the domain movement. Analysis of regulon predictions revealed that the signaling pathway from the CebE-mediated cellotriose transport to the transcriptional activation of thaxtomin phytotoxin biosynthesis is conserved in Streptomyces spp causing common scab, except for Streptomyces ipomoeae that specifically colonizes sweet potatoes and responds to other and yet unknown virulence elicitors. Interestingly, strains belonging to pathogenic species turgidiscabies and caniscabies have a cellotriose-binding protein orthologous to the CebE protein of the saprophytic species Streptomyces reticuli with lower affinity for its substrate (KD in the micromolar range), suggesting higher cellotriose concentrations for perception of their host. Our work also provides the structural basis for the uptake of cellobiose and cellotriose by non-pathogenic cellulose-decomposing Streptomyces species. ImportanceCommon scab is a disease caused by few Streptomyces species that affects important root and tuber crops including potato, beet, radish, and parsnip, resulting in major economic losses worldwide. In this work we unveiled the molecular basis of host recognition by these pathogens by solving the structure of the sugar-binding protein CebE of S. scabiei in complex with cellotriose, the main elicitor of the pathogenic lifestyle of these bacteria. We further revealed that the signaling pathway from CebE-mediated transport of cellotriose is conserved in all pathogenic species except S. ipomoeae that causes soft rot disease on sweet potatoes. Our work also provides the structural basis of the uptake of cellobiose and cellotriose in saprophytic Streptomyces species, the first step activating the expression of the enzymatic system degrading the most abundant polysaccharide on earth, cellulose. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=125 SRC="FIGDIR/small/540135v1_ufig1.gif" ALT="Figure 1"> View larger version (34K): org.highwire.dtl.DTLVardef@1915dd1org.highwire.dtl.DTLVardef@a65aaforg.highwire.dtl.DTLVardef@18bc293org.highwire.dtl.DTLVardef@937d2f_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LICellotriose uptake triggers common scab in tuber/root crops by Streptomyces scabiei C_LIO_LICrystal structure of CebE of S. scabiei interacting with cellotriose is solved C_LIO_LICellotriose triggers the closed conformational state of CebE C_LIO_LIThe CebE/cellotriose route to pathogenicity is conserved in Streptomyces species C_LIO_LICebE-type background may affect the cellotriose concentration eliciting virulence C_LI