Established Pseudomonas syringae pv. tomato infection disrupts immigration of leaf surface bacteria to the apoplast

Abstract

Bacterial disease alters the infection court creating new niches. The apoplast is an oasis from the hardships of the leaf surface and is generally inaccessible to nonpathogenic members of the phyllosphere bacterial community. Previously, we demonstrated that Salmonella enterica immigrants to the leaf surface can both enter the apoplast and replicate due to conditions created by an established Xanthomonas hortorum pv. gardneri (Xhg) infection. Here, we have expanded our investigation of how infection changes the host by examining the effects of another water-soaking pathogen, Pseudomonas syringae pv tomato (Pst), on immigrating bacteria. We discovered that, despite causing macroscopically similar symptoms as Xhg, Pst infection disrupts S. enterica colonization of the apoplast. To determine if these effects were broadly applicable to phyllosphere bacteria, we examined the fates of immigrant Xhg and Pst arriving on an infected leaf. We found that this effect is not specific to S. enterica, but that immigrating Xhg or Pst also struggled to fully join the infecting Pst population established in the apoplast. To identify the mechanisms underlying these results, we quantified macroscopic infection symptoms, examined stomata as a pinch point of bacterial entry, and characterized aspects of interbacterial competition. While it may be considered common knowledge that hosts are fundamentally altered following infection, the mechanisms that drive these changes remain poorly understood. Here, we investigated these pathogens to reach a deeper understanding of how infection alters a host from a rarely accessible, inhabitable environment to an obtainable, habitable niche. IMPORTANCEPathogens dramatically alter the host during infection. Changes in host physical and biochemical characteristics benefit the pathogen and can reshape the composition of the bacterial community. In fact, rare members of the plant microbiota, namely bacterial human pathogens, such as Salmonella enterica, thrive in some plant infection courts. The increased success of human pathogens results from the conversion of the rarely accessible, inhabitable apoplast to an obtainable, habitable niche following infection. Here, we compared two phytopathogens, Pseudomonas syringae pv. tomato and Xanthomonas hortorum pv. gardneri within a tomato host and uncovered relevant niche changes potentially overlooked by the similarity in macroscopic symptoms. We investigated mechanisms used to reshape the host environment to the pathogens benefit and either success or failure of newly arriving immigrant bacteria. This study reveals information about bacterial disease of leaves and key changes that remodel inhospitable niches to new, conducive environments in the diseased host.