Abstract
Xyloglucans are highly substituted and recalcitrant polysaccharides found in the primary cell walls of vascular plants, acting as a barrier against pathogens. Here, we reveal that the diverse and economically relevant Xanthomonas bacteria are endowed with a xyloglucan depolymerization machinery that is linked to pathogenesis. Using the citrus canker pathogen as a model organism, we show that this system encompasses distinctive glycoside hydrolases, a modular xyloglucan acetylesterase and specific membrane transporters, demonstrating that plant-associated bacteria employ distinct molecular strategies from commensal gut bacteria to cope with xyloglucans. Notably, the sugars released by this system elicit the expression of several key virulence factors, including the type III secretion system, a membrane-embedded apparatus to deliver effector proteins into the host cells. Together, these findings shed light on the molecular mechanisms underpinning the intricate enzymatic machinery of Xanthomonas to depolymerize xyloglucans and uncover a role for this system in signaling pathways driving pathogenesis.
Highlights
Xyloglucans are highly substituted and recalcitrant polysaccharides found in the primary cell walls of vascular plants, acting as a barrier against pathogens
We reveal a link between this enzymatic system and bacterial virulence through a stimulatory effect of its products on the expression of several key virulence factors, including the type III secretion system (T3SS), a needle-like apparatus that inject effector proteins into the plant cell to modulate host responses in favor of bacterial colonization[10]
Genomic analysis revealed that most Xanthomonas species conserve a predicted XyG utilization loci (XyGUL) consisting of two outer membrane TonB-dependent transporters (TBDTs), four glycoside hydrolases belonging to the families GH74, GH31, GH35, GH95 and one esterase with no significant similarity with any carbohydrate esterase family (Fig. 1a, and Supplementary Tables 1 and 2)
Summary
Xyloglucans are highly substituted and recalcitrant polysaccharides found in the primary cell walls of vascular plants, acting as a barrier against pathogens. The sugars released by this system elicit the expression of several key virulence factors, including the type III secretion system, a membrane-embedded apparatus to deliver effector proteins into the host cells Together, these findings shed light on the molecular mechanisms underpinning the intricate enzymatic machinery of Xanthomonas to depolymerize xyloglucans and uncover a role for this system in signaling pathways driving pathogenesis. Our results show that Xanthomonas XyGUL encodes a highly elaborate enzymatic cascade including distinct activities (acetylesterase, α-L-fucosidase, β-galactosidase, α-xylosidase, and xyloglucanase), catalytic mechanisms (inverting and retaining), modes of action (endo and exo), and 3D architectures (multimodular and quaternary arrangements) This machinery notably differs from other known XyGULs, expanding the current knowledge about microbial molecular strategies associated with the depolymerization and utilization of recalcitrant plant polysaccharides. We reveal a link between this enzymatic system and bacterial virulence through a stimulatory effect of its products on the expression of several key virulence factors, including the type III secretion system (T3SS), a needle-like apparatus that inject effector proteins into the plant cell to modulate host responses in favor of bacterial colonization[10]
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