1887

Abstract

Incidences of bacterial foodborne illness caused by ingestion of fresh produce are rising. Instead of this being due to incidental contamination, the animal pathogen utilizes specific molecular mechanisms to attach to and colonize plants. This work characterizes two genes of unknown function: a putative periplasmic protein, STM0278, and a putative protein with a hydrolase in the C-terminus, STM0650. STM0278 and STM0650 are important for seedling colonization but appear to have different roles during the process of colonization. Mutants of either STM0278 or STM0650 showed reduced colonization of alfalfa seedlings at 24 h, and the STM0278 mutant also showed reduced colonization at 48 h. Both genes were expressed at 4 h following inoculation of 3-day-old seedlings and at 72 h after seed inoculation. This suggests that the role of STM0650 in seedling colonization is less important later in the process or is duplicated by other mechanisms. Mutants of STM0278 and STM0650 were defective in swarming. The STM0278 mutant failed to swarm in 24 h, while swarming of the STM0650 mutant was delayed. Addition of surfactant restored swarming of the STM0278 mutant, suggesting that STM0278 is involved in surfactant or osmotic agent production or deployment. Alfalfa seed exudates as the sole nutrient source were capable of perpetuating swarming. Sequence analysis revealed sequences homologous to STM0278 and STM0650 in plant-associated bacteria, but none in . Phylogenetic analysis of STM0650 showed similar sequences from diverse classes of plant-associated bacteria. Bacteria that preferentially colonize roots, including , may use a similar hydrolase for swarming or biofilm production on plants. Multicellular behaviours by appear central to plant colonization. genes involved in plant colonization and survival outside of a host are most likely among the ‘function unknown’ genes of this bacterium.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.032029-0
2009-11-01
2019-10-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/11/3701.html?itemId=/content/journal/micro/10.1099/mic.0.032029-0&mimeType=html&fmt=ahah

References

  1. Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S. & Vivanco, J. M. ( 2006; ). The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57, 233–266.[CrossRef]
    [Google Scholar]
  2. Barak, J. D., Whitehand, L. C. & Charkowski, A. O. ( 2002; ). Differences in attachment of Salmonella enterica serovars and Escherichia coli O157 : H7 to alfalfa sprouts. Appl Environ Microbiol 68, 4758–4763.[CrossRef]
    [Google Scholar]
  3. Barak, J. D., Gorski, L., Naraghi-Arani, P. & Charkowski, A. O. ( 2005; ). Salmonella enterica virulence genes are required for bacterial attachment to plant tissue. Appl Environ Microbiol 71, 5685–5691.[CrossRef]
    [Google Scholar]
  4. Barak, J. D., Jahn, C. E., Gibson, D. L. & Charkowski, A. O. ( 2007; ). The role of cellulose and O-antigen capsule in the colonization of plants by Salmonella enterica. Mol Plant Microbe Interact 20, 1083–1091.[CrossRef]
    [Google Scholar]
  5. Boureau, T., Jacques, M. A., Berruyer, R., Dessaux, Y., Dominquez, H. & Morris, C. E. ( 2004; ). Comparison of the phenotypes and genotypes of biofilm and solitary epiphytic bacterial populations on broad-leaved endive. Microb Ecol 47, 87–95.[CrossRef]
    [Google Scholar]
  6. CDC ( 2009; ). Surveillance for foodborne disease outbreaks – United States, 2006. MMWR Morb Mortal Wkly Rep 58, 609–615.
    [Google Scholar]
  7. Charkowski, A. O., Barak, J. D., Sarreal, C. Z. & Mandrell, R. E. ( 2002; ). Differences in growth of Salmonella enterica and Escherichia coli O157 : H7 on alfalfa sprouts. Appl Environ Microbiol 68, 3114–3120.[CrossRef]
    [Google Scholar]
  8. Cooley, M. B., Miller, W. G. & Mandrell, R. E. ( 2003; ). Colonization of Arabidopsis thaliana with Salmonella enterica and enterohemorrhagic Escherichia coli O157 : H7 and competition by Enterobacter asburiae. Appl Environ Microbiol 69, 4915–4926.[CrossRef]
    [Google Scholar]
  9. Gorski, L., Palumbo, J. D. & Mandrell, R. E. ( 2003; ). Attachment of Listeria monocytogenes to radish tissue is dependent upon temperature and flagellar motility. Appl Environ Microbiol 69, 258–266.[CrossRef]
    [Google Scholar]
  10. Gorski, L., Duhã, J. M. & Flaherty, D. ( 2009; ). The use of flagella and motility for plant colonization and fitness by different strains of the foodborne pathogen Listeria monocytogenes. PLoS One 4, e5142 [CrossRef]
    [Google Scholar]
  11. Harshey, R. M. & Matsuyama, T. ( 1994; ). Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells. Proc Natl Acad Sci U S A 91, 8631–8635.[CrossRef]
    [Google Scholar]
  12. Inami, G. B. & Moler, S. E. ( 1999; ). Detection and isolation of Salmonella from naturally contaminated alfalfa seeds following an outbreak investigation. J Food Prot 62, 662–664.
    [Google Scholar]
  13. Jeter, C. & Matthysse, A. G. ( 2005; ). Characterization of the binding of diarrheagenic strains of E. coli to plant surfaces and the role of curli in the interaction of the bacteria with alfalfa sprouts. Mol Plant Microbe Interact 18, 1235–1242.[CrossRef]
    [Google Scholar]
  14. Kim, W. & Surette, M. G. ( 2004; ). Metabolic differentiation in actively swarming Salmonella. Mol Microbiol 54, 702–714.[CrossRef]
    [Google Scholar]
  15. Kim, W. & Surette, M. G. ( 2006; ). Coordinated regulation of two independent cell-cell signaling systems and swarmer differentiation in Salmonella enterica serovar Typhimurium. J Bacteriol 188, 431–440.[CrossRef]
    [Google Scholar]
  16. Kim, W., Killam, T., Sood, V. & Surette, M. G. ( 2003; ). Swarm-cell differentiation in Salmonella enterica serovar Typhimurium results in elevated resistance to multiple antibiotics. J Bacteriol 185, 3111–3117.[CrossRef]
    [Google Scholar]
  17. Klerks, M. M., van Gent-Pelzer, M., Franz, E., Zijlstra, C. & van Bruggen, A. H. C. ( 2007; ). Physiological and molecular responses of Lactuca sativa to colonization by Salmonella enterica serovar Dublin. Appl Environ Microbiol 73, 4905–4914.[CrossRef]
    [Google Scholar]
  18. Miller, W. G., Leveau, J. H. & Lindow, S. E. ( 2000; ). Improved gfp and inaZ broad-host-range promoter-probe vectors. Mol Plant Microbe Interact 13, 1243–1250.[CrossRef]
    [Google Scholar]
  19. Mohle-Boetani, J. C., Farrar, J., Bradley, P., Barak, J. D., Miller, M., Mandrell, R., Mead, P., Keene, W. E., Cummings, K. & other authors ( 2009; ). Salmonella infections associated with mung bean sprouts: epidemiological and environmental investigations. Epidemiol Infect 137, 357–366.[CrossRef]
    [Google Scholar]
  20. Rauprich, O., Matsushita, M., Weijer, C., Siegert, F., Esipov, S. & Shapiro, J. ( 1996; ). Periodic phenomena in Proteus mirabilis swarm colony development. J Bacteriol 178, 6525–6538.
    [Google Scholar]
  21. Smith, J. N., Dyszel, J. L., Soares, J. A., Ellermeier, C. D., Altier, C., Lawhon, S. D., Adams, L. G., Konjufca, V., Curtiss, R., III & other authors ( 2008; ). SdiA, an N-acylhomoserine lactone receptor, becomes active during the transit of Salmonella enterica through the gastrointestinal tract of turtles. PLoS One 3, e2826 [CrossRef]
    [Google Scholar]
  22. Teplitski, M., Robinson, J. B. & Bauer, W. D. ( 2000; ). Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant Microbe Interact 13, 637–648.[CrossRef]
    [Google Scholar]
  23. Toguchi, A., Siano, M., Burkart, M. & Harshey, R. M. ( 2000; ). Genetics of swarming motility in Salmonella enterica serovar Typhimurium: critical role for lipopolysaccharide. J Bacteriol 182, 6308–6321.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.032029-0
Loading
/content/journal/micro/10.1099/mic.0.032029-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error