GH25 lysozyme mediates tripartite interkingdom interactions and microbial competition on the plant leaf surface

Microbial communities inhabiting plants have emerged as crucial factors in regulating plant health and defense against disease-causing pathogens. The yeast <i>Moesziomyces bullatus</i> ex. <i>Albugo</i> (MbA) on <i>Arabidopsis</i> produces a glycoside hydrolase 25 (GH25) protein that regulates the leaf microbiome by antagonizing the pathogenic oomycete <i>Albugo laibachii</i>. Applying <i>MbA</i> or GH25 rescued <i>Arabidopsis thaliana</i> shoot fresh weight under <i>A. laibachii</i> infection, highlighting their crop protection potential. Interaction assays revealed no antagonistic activity of GH25 against other plant pathogenic oomycetes or fungi besides <i>A. laibachii</i>. We identified a community of bacteria closely associated with <i>A. laibachii.</i> Three of these bacteria are inhibited by GH25 and one of them, <i>Curtobacterium sp.</i> could override the inhibition of <i>A. laibachii</i> by <i>MbA</i>. This points to a tripartite antagonism where <i>Curtobacterium</i> and <i>A. laibachii</i> protect each other from <i>MbA</i>. Moreover, <i>Curtobacterium</i> selectively inhibits other <i>A. laibachii</i>-associated bacteria not targeted by <i>MbA</i> but that themselves suppress <i>A. laibachii</i>. This study uncovers an interkingdom network where GH25 lysozyme shapes microbial interactions between yeast, oomycete, and associated bacteria.