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Applied and Environmental Microbiology, October 2009, p. 6076-6086, Vol. 75, No. 19
0099-2240/09/$08.00+0     doi:10.1128/AEM.01084-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Internalization of Salmonella enterica in Leaves Is Induced by Light and Involves Chemotaxis and Penetration through Open Stomata{triangledown} ,{dagger}

Yulia Kroupitski,1,4 Dana Golberg,1 Eduard Belausov,2 Riky Pinto,1 Dvora Swartzberg,3 David Granot,3 and Shlomo Sela1*

Microbial Food Safety Research Unit, Department of Food Sciences, Institute for Technology and Storage of Agricultural Products, Agricultural Research Organization, The Volcani Center, P.O. Box 6, Beth-Dagan 50250, Israel,1 Confocal Microscopy Unit, Agricultural Research Organization, The Volcani Center, Beth-Dagan, Israel,2 Institute of Plant Sciences, Agricultural Research Organization, The Volcani Center, Beth-Dagan 50250, Israel,3 Department of Human Microbiology, Sackler School of Medicine, Tel-Aviv University, Tel-Aviv, Israel4

Received 12 May 2009/ Accepted 27 July 2009

Outbreaks of salmonellosis related to consumption of fresh produce have raised interest in Salmonella-plant interactions leading to plant colonization. Incubation of gfp-tagged Salmonella enterica with iceberg lettuce leaves in the light resulted in aggregation of bacteria near open stomata and invasion into the inner leaf tissue. In contrast, incubation in the dark resulted in a scattered attachment pattern and very poor stomatal internalization. Forcing stomatal opening in the dark by fusicoccin had no significant effect on Salmonella internalization. These results imply that the pathogen is attracted to nutrients produced de novo by photosynthetically active cells. Indeed, mutations affecting Salmonella motility and chemotaxis significantly inhibited bacterial internalization. These findings suggest a mechanistic account for entry of Salmonella into the plant's apoplast and imply that either Salmonella antigens are not well recognized by the stoma-based innate immunity or that this pathogen has evolved means to evade it. Internalization of leaves may provide a partial explanation for the failure of sanitizers to efficiently eradicate food-borne pathogens in leafy greens.

* Corresponding author. Mailing address: Microbial Food Safety Research Unit, Department of Food Science, Agricultural Research Organization, The Volcani Center, P.O. Box 6, Beth-Dagan 50250, Israel. Phone: 972-3-9683750. Fax: 972-3-9683692. E-mail: shlomos{at}volcani.agri.gov.il

{triangledown} Published ahead of print on 31 July 2009.

{dagger} Supplemental material for this article may be found at http://aem.asm.org/.

Applied and Environmental Microbiology, October 2009, p. 6076-6086, Vol. 75, No. 19
0099-2240/09/$08.00+0     doi:10.1128/AEM.01084-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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