Xanthomonas Infection Transforms the Apoplast into an Accessible and Habitable Niche for Salmonella enterica

• Published in: Applied and environmental microbiology Vol. 88; no. 22; p. e0133022
• Main Authors: Dixon, Megan H, Cowles, Kimberly N, Zaacks, Sonia C, Marciniak, Isabel N, Barak, Jeri D
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 22.11.2022
• Subjects: Apoplast; Host plants; Immigration; Infections; Irradiation; Leaves; Niches; Plant bacterial diseases; Plant Diseases - microbiology; Plant Microbiology; Plants; Salmonella; Salmonella enterica; Solanum lycopersicum - microbiology; Spotlight Selection; Survival; Tomatoes; Water; Xanthomonas; Xanthomonas - physiology; food safety; plant-microbe interactions; plant disease; salmonellosis
• ISSN: 0099-2240; 1098-5336
• DOI: 10.1128/aem.01330-22

The physiology of plant hosts can be dramatically altered by phytopathogens. Xanthomonas hortorum pv. gardneri is one such pathogen that creates an aqueous niche within the leaf apoplast by manipulating the plant via the transcription activator-like effector AvrHah1. Simultaneous immigration of pv. gardneri and Salmonella enterica to healthy tomato leaves results in increased survival of S. enterica as infection progresses. However, the fate of S. enterica following arrival on actively infected leaves has not been examined. We hypothesized that the water soaking caused by pv. gardneri could facilitate the ingression of S. enterica into the apoplast and that this environment would be conducive for growth. We found that an altered apoplast, abiotically water congested or infected and water-soaked, enabled surface S. enterica to passively localize to the protective apoplast and facilitated migration of S. enterica to distal sites within the aqueous apoplast. contributed to the protection and migration of S. enterica early in pv. gardneri infection. -infected apoplasts facilitated prolonged survival and promoted S. enterica replication compared to the case with healthy apoplasts. Access to an aqueous apoplast in general protects S. enterica from immediate exposure to irradiation, whereas the altered environment created by infection provides growth-conducive conditions for S. enterica. Overall, we have characterized an ecological relationship in which host infection converts an unreachable niche to a habitable environment. Bacterial spot disease caused by species devastates tomato production worldwide. Salmonellosis outbreaks from consumption of raw produce have been linked to the arrival of Salmonella enterica on crop plants in the field via contaminated irrigation water. Considering that is difficult to eradicate, it is highly likely that S. enterica arrives on leaves precolonized by with infection under way. Our study demonstrated that infection and disease fundamentally alter the leaf, resulting in redistribution and change in abundance of a phyllosphere bacterial member. These findings contribute to our understanding of how S. enterica manages to persist on leaf tissue despite lacking the ability to liberate nutrients from plant cells. More broadly, this study reveals a mechanism by which physiochemical changes to a host environment imposed by a plant pathogen can convert an uninhabitable leaf environment into a hospitable niche for selected epiphytic microbes.