ABSTRACT En route to its intestinal target cells Salmonella enterica passes different host niches and encounters various environmental cues. These are expected to promote Salmonella in the decision of changing its extracellular life to intracellular. We find that prior incubation of bacteria in the presence of signals which are characteristic for the small intestine affects invasion in a model system: Salmonella grown at high osmotic pressure in the presence of bile or in amino acid rich medium, infect host cells most efficiently. Hence, Salmonella enterica modulates its infectivity in response to these stimuli which consequently determines the success of infection. Our results close the current gap between signal and actual behavior and may serve as a basis for further investigations for example if Salmonella has an adaptive prediction of environmental changes.
Cite this paper
J. Baumbach, H. Hoeke, F. Weege, A. Schmeisky and P. Neumann-Staubitz, "Salmonella enterica Modulates Its Infectivity in Response to Intestinal Stimuli," Open Journal of Medical Microbiology, Vol. 2 No. 2, 2012, pp. 41-45. doi: 10.4236/ojmm.2012.22006.
 J. A. Ibarra and O. Steele-Mortimer, “Salmonella—The Ultimate Insider. Salmonella Virulence Factors that Modulate Intracellular Survival,” Cellular Microbiology, Vol. 11, No. 11, 2009, pp. 1579-1586.
 A. Haraga, M. B. Ohlson and S. I. Miller, “Salmonellae Interplay with Host Cells,” Nature Reviews Microbiology, Vol. 6, No. 1, 2008, pp. 53-66. doi:10.1038/nrmicro1788
 A. Mitchell, G. H. Romano, B. Groisman, A. Yona, E. Dekel, M. Kupiec, O. Dahan and Y. Pilpel, “Adaptive Prediction of Environmental Changes by Microorganisms,” Nature, Vol. 460, No. 7252, 2009, pp. 220-224. doi:10.1038/nature08112
 D. Beier and R. Gross, “Regulation of Bacterial Virulence by Two-Component Systems,” Current Opinion Microbiology, Vol. 9, No. 2, 2006, pp. 143-152.
 C. Altier, “Genetic and Environmental Control of Salmonella Invasion,” The Journal of Microbiology, Vol. 43, Special Issue, 2005, pp. 85-92.
 M. Song, H. J. Kim, E. Y. Kim, M. Shin, H. C. Lee, Y. Hong, J. H. Rhee, H. Yoon, S. Ryu, S. Lim and H. E. Choy, “ppGpp-Dependent Stationary Phase Induction of Genes on Salmonella Pathogenicity Island 1,” The Journal of Biological Chemistry, Vol. 279, No. 33, 2004, pp. 34183-34190. doi:10.1074/jbc.M313491200
 C. A. Lee and S. Falkow, “The Ability of Salmonella to Enter Mammalian Cells Is Affected by Bacterial Growth State,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 87, No. 11, 1990, pp. 4304-4308. doi:10.1073/pnas.87.11.4304
 D. A. Schiemann, “Association with MDCK Epithelial Cells by Salmonella Typhimurium Is Reduced during Utilization of Carbohydrates,” Infection and Immunity, Vol. 63, No. 4, 1995, pp. 1462-1467.
 J. R. Ellermeier and J. M. Slauch, “Adaptation to the Host Environment: Regulation of the SPI1 Type III Secretion System in Salmonella enterica serovar Typhimurium,” Current Opinion in Microbiology, Vol. 10, No. 1, 2007, pp. 24-29. doi:10.1016/j.mib.2006.12.002
 B. D. Jones, “Salmonella Invasion Gene Regulation: A Story of Environmental Awareness,” The Journal of Microbiology, Vol. 43, Special Issue, 2005, pp. 110-117.
 R. L. Lucas, C. P. Lostroh, C. C. DiRusso, M. P. Spector, B. L. Wanner and C. A. Lee, “Multiple Factors Independently Regulate hilA and Invasion Gene Expression in Salmonella enterica Serovar Typhimurium,” Journal of Bacteriology, Vol. 182, No. 7, 2000, pp. 1872-1882.
 E. Fass and E. A. Groisman, “Control of Salmonella Pathogenicity Island-2 Gene Expression,” Current Opinion Microbiology, Vol. 12, No. 2, 2009, pp. 199-204.
 E. A. Groisman and C. Mouslim, “Sensing by Bacterial Regulatory Systems in Host and Non-Host Environments,” Nature Reviews Microbiology, Vol. 4, No. 9, 2006, pp. 705- 709. doi:10.1038/nrmicro1478
 O. Steele-Mortimer, “The Salmonella-Containing Vacuole: Moving with the Times,” Current Opinion Microbiology, Vol. 11, No. 1, 2008, pp. 38-45.
 O. Steele-Mortimer, S. Meresse, J. P. Gorvel, B. H. Toh and B. B. Finlay, “Biogenesis of Salmonella Typhimurium-Containing Vacuoles in Epithelial Cells Involves Interactions with the Early Endocytic Pathway,” Cellular Microbiology, Vol. 1, No. 1, 1999, pp. 33-49.
 C. A. Muller, I. B. Autenrieth and A. Peschel, “Intestinal Epithelial Barrier and Mucosal Immunity Innate Defenses of the Intestinal Epithelial Barrier,” Cellular and Molecular Life Sciences, Vol. 62, No. 12, 2005, pp. 1297-1307.
 C. L. Birmingham, A. C. Smith, M. A. Bakowski, T. Yoshimori and J. H. Brumell, “Autophagy Controls Salmonella Infection in Response to Damage to the Salmonella-containing Vacuole,” The Journal of Biology Che- mistry, Vol. 281, No. 16, 2006, pp. 11374-11383.
 C. R. Beuzon, S. P. Salcedo and D. W. Holden, “Growth and Killing of a Salmonella enterica Serovar Typhimurium sifA Mutant Strain in the Cytosol of Different Host Cell Lines,” Microbiology, Vol. 148, No. 9, 2002, pp. 2705-2715.
 H. Mizusaki, A. Takaya, T. Yamamoto and S. I. Aizawa, “Signal Pathway in Salt-Activated Expression of the Salmonella Pathogenicity Island 1 Type III Secretion System in Salmonella enterica Serovar Typhimurium,” Journal of Bacteriology, Vol. 190, No. 13, 2008, pp. 4624-4631. doi:10.1128/JB.01957-07
 C. Tartera and E. S. Metcalf, “Osmolarity and Growth Phase Overlap in Regulation of Salmonella Typhi Adherence to and Invasion of Human Intestinal Cells,” Infection and Immunity, Vol. 61, No. 7, 1993, pp. 3084-3089.
 W. F. Boron and E. L. Boulpaep, “Medical Physiology: A Cellular and Molecular Approach,” 2nd Edition, Saunders Elsevier, Philadelphia, 2009.
 A. M. Prouty and J. S. Gunn, “Salmonella enterica Serovar Typhimurium Invasion Is Repressed in the Presence of Bile,” Infection and Immunity, Vol. 68, No. 12, 2000, pp. 6763-6769.
 C. L. Wells, R. P. Jechorek and S. L. Erlandsen, “Inhibitory Effect of Bile on Bacterial Invasion of Enterocytes: Possible Mechanism for Increased Translocation Associated with Obstructive Jaundice,” Critical Care Medicine, Vol. 23, No. 2, 1995, pp. 301-307.
 J. A. Ibarra, L. A. Knodler, D. E. Sturdevant, K. Virtaneva, A. B. Carmody, E. R. Fischer, S. F. Porcella and O. Steele-Mortimer, “Induction of Salmonella Pathogenicity Island 1 under Different Growth Conditions Can Affect Salmonella-Host Cell Interactions in Vitro,” Microbiology, Vol. 156, No. 4, 2010, pp. 1120-1133.
 M. W. Bader, S. Sanowar, M. E. Daley, A. R. Schneider, U. Cho, W. Xu, R. E. Klevit, H. Le Moual and S. I. Miller, “Recognition of Antimicrobial Peptides by a Bacterial Sensor Kinase,” Cell, Vol. 122, No. 3, 2005, pp. 461-472.
 L. R. Prost and S. I. Miller, “The Salmonellae PhoQ Sensor: Mechanisms of Detection of Phagosome Signals,” Cellular Microbiology, Vol. 10, No. 3, 2008, pp. 576-582.
 W. Eisenreich, T. Dandekar, J. Heesemann and W. Goebel, “Carbon Metabolism of Intracellular Bacterial Pathogens and Possible Links to Virulence,” Nature Reviews Microbiology, Vol. 8, No. 6, 2010, pp. 401-412.
 J. H. Miller, “Experiments in Molecular Genetics,” Cold Spring Harbor Laboratory, New York, 1972.
 L. M. Schechter, S. M. Damrauer and C. A. Lee, “Two AraC/XylS Family Members Can Independently Counteract the Effect of Repressing Sequences Upstream of the hilA Promoter,” Moecularl Microbiology, Vol. 32, No. 3, 1999, pp. 629-642. doi:10.1046/j.1365-2958.1999.01381.x
 F. C. Soncini, E. G. Vescovi and E. A. Groisman, “Transcriptional Autoregulation of the Salmonella Typhimurium phoPQ Operon,” Journal of Bacteriology, Vol. 177, No. 15, 1995, pp. 4364-4371.