Enzymatic quorum quenching alters the phyllosphere microbiome and suppresses a bacterial-induced plant disease

Bacterial plant pathogens cause hundreds of millions of dollars in annual crop losses in the United States alone, further stressing an already strained global food supply. Numerous bacteria in the phyllosphere use N-acyl homoserine lactone (AHL)-mediated quorum sensing (QS) systems to coordinate behaviors and shape microbial communities. Strategies that interfere with bacterial QS systems employ enzymes to degrade or transform AHLs in a process called quorum quenching (QQ). This interference results in altered microbial community structure and function. We previously isolated and engineered SsoPox, a highly stable AHL-degrading lactonase that interferes with QS. Here, we evaluated the effects of SsoPox-mediated QS disruption on the Zea mays phyllosphere in a Goss's wilt infection model caused by Clavibacter nebraskensis. In this proof-of-concept work, we found that infection significantly altered the composition and structure of the leaf microbial community. SsoPox QQ lactonase treatment substantially reduced this shift, resulting in a leaf surface community resembling the uninfected controls. qPCR experiments revealed a small, yet significant reduction of pathogen abundance on plant leaves following enzymatic treatment. As a result, the formulated QQ lactonase spray reduced disease severity. This study demonstrates the critical role of microbial signaling in the phyllosphere and highlights the potential of QQ lactonases to control plant diseases.