Impact of phytopathogen infection and extreme weather stress on internalization of Salmonella Typhimurium in lettuce

International Journal of Food Microbiology

Volumn 168-169, Issue , 2014, Pages 24-31

  Ge, Chongtao ^a   Lee, Cheonghoon ^a   Nangle, Ed ^a   Li, Jianrong ^a   Gardner, David ^a   Kleinhenz, Matthew ^a   Lee, Jiyoung ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Internalization; Lettuce; Lettuce mosaic virus; Salmonella Typhimurium; Water stress

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ARTICLE; BIOTIC STRESS; CONFOCAL LASER MICROSCOPY; CONTAMINATED PLANT; CONTROLLED STUDY; DROUGHT STRESS; INTERNALIZATION; LEAF SURFACE; LETTUCE; LETTUCE MOSAIC VIRUS; MOSAIC VIRUS; NONHUMAN; PLANT ROOT; PLATE COUNT; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA TYPHIMURIUM; WATER STRESS;

LACTUCA; LETTUCE MOSAIC VIRUS; SALMONELLA; SALMONELLA TYPHIMURIUM;

EID: 84887513121     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2013.10.010     Document Type: Article

References (38)

1. Bernstein N., Sela S., Neder-Lavon S. Assessment of contamination potential of lettuce by Salmonella enterica serovar Newport added to the plant growing medium. J. Food Prot. 2007, 70:1717-1722.
2. Centers for Disease Control, Prevention CDC 2011 Estimates: Findings http://www.cdc.gov/foodborneburden/2011-foodborne-estimates.html.
3. Chen J., Zhang L., Paoli G.C., Shi C., Tu S.-I., Shi X. A real-time PCR method for the detection of Salmonella enterica from food using a target sequence identified by comparative genomic analysis. Int. J. Food Microbiol. 2010, 137:168-174.
4. Cooley M., Miller W., Mandrell R. Colonization of Arabidopsis thaliana with Salmonella enterica or enterohemorrhagic Escherichia coli O157:H7 and competition by an Enterobacter asburiae. Appl. Environ. Microbiol. 2003, 69:4915-4926.
5. Davies W.J., Kudoyarova G., Hartung W. Long-distance ABA signaling and its relation to other signaling pathways in the detection of soil drying and the mediation of the plant's response to drought. J. Plant Growth Regul. 2005, 24:285-295.
6. Dhar A.K., Roux M.M., Klimpel K.R. Quantitative assay for measuring the Taura syndrome virus and yellow head virus load in shrimp by real-time RT-PCR using SYBR Green chemistry. J. Virol. Methods 2002, 104:69-82.
7. Erickson M.C., Webb C.C., Diaz-Perez J.C., Phatak S.C., Silvoy J.J., Davey L., Payton A.S., Liao J., Ma L., Doyle M.P. Surface and internalized Escherichia coli O157:H7 on field-grown spinach and lettuce treated with spray-contaminated irrigation water. J. Food Prot. 2010, 73:1023-1029.
8. Franz E., Visser A.A., Van Diepeningen A.D., Klerks M.M., Termorshuizen A.J., Van Bruggen A.H.C. Quantification of contamination of lettuce by GFP-expressing Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium. Food Microbiol. 2007, 24:106-112.
9. Garrood M.J., Wilson P.D., Brocklehurst T.F. Modeling the rate of attachment of Listeria monocytogenes, Pantoea agglomerans, and Pseudomonas fluorescens to, and the probability of their detachment from, potato tissue at 10 degrees C. Appl. Environ. Microbiol. 2004, 70:3558-3565.
10. Gautam D., Ma L., Bruton B.D., Fletcher J. Erwinia tracheiphila colonization of cantaloupe fruits through flower inoculation. 2011 APS-IPPC Joint Meeting abstract 101 2011, S59.
11. Ge C., Lee C., Lee J. The impact of extreme weather events on Salmonella internalization in lettuce and green onion. Food Res. Int. 2012, 45:1118-1122.
12. German-Retana S., Walter J., Le Gall O. Lettuce mosaic virus: from pathogen diversity to host interactors. Mol. Plant Pathol. 2008, 9:127-136.
13. Golberg D., Kroupitski Y., Belausov E., Pinto R., Sela S. Salmonella Typhimurium internalization is variable in leafy vegetables and fresh herbs. Int. J. Food Microbiol. 2011, 145:250-257.
14. Guo X., Chen J., Brackett R.E., Beuchat L.R. Survival of salmonellae on and in tomato plants from the time of inoculation at flowering and early stages of fruit development through fruit ripening. Appl. Environ. Microbiol. 2001, 67:4760-4764.
15. Hare P.D., Cress W.A., Van Staden J. The involvement of cytokinins in plant responses to environmental stress. Plant Growth Regul. 1997, 23:79-103.
16. Heaton J.C., Jones K. Microbial contamination of fruit and vegetables and the behavior of enteropathogens in the phyllosphere: a review. J. Appl. Microbiol. 2008, 104:613-626.
17. Hirano S.S., Upper C.D. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae-a pathogen, ice nucleus, and epiphyte. Microbiol. Mol. Biol. Rev. 1999, 64:624-653.
18. Hunter P.J., Hand P., Pink D., Whipps J.M., Bending G.D. Both leaf properties and microbe-microbe interactions influence within-species variation in bacterial population diversity and structure in the lettuce (Lactuca species) phyllosphere. Appl. Environ. Microbiol. 2010, 76:8117-8215.
19. International Organization for Standardization Soil quality - determination of dry matter and water content on a mass basis - gravimetric method 1993, 11464. ISO.
20. Josephson K.L., Gerba C.P., Pepper I.L. Polymerase chain reaction detection of nonviable bacterial pathogens. Appl. Environ. Microbiol. 1993, 59:3513-3515.
21. Kroupitski Y., Golberg D., Belausov E., Pinto R., Swartzberg D., Granot D., Sela S. Internalization of Salmonella enterica in leaves is induced by light and involves chemotaxis and penetration through open stomata. Appl. Environ. Microbiol. 2009, 75:6076-6086.
22. Kroupitski Y., Pinto R., Brandl M.T., Belausov E., Sela S. Interactions of Salmonella enterica with lettuce leaves. J. Appl. Microbiol. 2009, 106:1876-1885.
23. Kyle J.L., Parker C.T., Goudeau D., Brandl M.T. Transcriptome analysis of Escherichia coli O157:H7 exposed to lysates of lettuce leaves. Appl. Environ. Microbiol. 2010, 76:1357-1387.
24. Lynch M.F., Tauxe R.V., Hedberg C.W. The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiol. Infect. 2009, 137:307-315.
25. Melotto M., Underwood W., Koczan J., Nomura K., He S.Y. Plant stomata function in innate immunity against bacterial invasion. Cell 2006, 126:969-980.
26. Mitra R., Cuesta-Alonso E., Wayadande A., Talley J., Gilliland S., Fletcher J. Effect of route of introduction and host cultivar on the colonization, internalization, and movement of the human pathogen Escherichia coli O157:H7 in spinach. J. Food Prot. 2009, 72:1521-1530.
27. Nyachuba D.G. Foodborne illness: is it on the rise?. Nutr. Rev. 2010, 68:257-269.
28. Pink D.A.C., Kostova D., Walkey D.G.A. Differentiation of pathotypes of lettuce mosaic virus. Plant Pathol. 1992, 41:5-12.
29. Pu S., Beaulieu J.C., Prinyawiwatkul W., Ge B. Effects of plant maturity and growth media bacterial inoculum level on the surface contamination and internalization of Escherichia coli O157:H7 in growing spinach leaves. J. Food Prot. 2009, 72:2313-2320.
30. Quilliam R.S., Williams A.P., Jones D.L. Lettuce cultivar mediates both phyllosphere and rhizosphere activity of Escherichia coli O157:H7. PLoS ONE 2012, 7(3):e33842.
31. Refsum T., Handeland K., Baggesen D.L., Holstad G., Kapperud G. Salmonellae in avian wildlife in Norway from 1969 to 2000. Appl. Environ. Microbiol. 2002, 68:5595-5599.
32. Revers F., Van Der Vlugt R.A.A., Souche S., Lanneau M., Lot H., Candresse T., Le Gall O. Nucleotide sequence of the 3' terminal region of the genome of four lettuce mosaic virus isolates from Greece and Yemen. Arch. Virol. 1999, 144:1619-1626.
33. Rosenblueth M., Martinez-Romero E. Bacterial endophytes and their interactions with hosts. Mol. Plant-Microbe 2006, 19:827-837.
34. Sapers G.M. Efficacy of washing and sanitizing methods for disinfection of fresh fruit and vegetable products. Food Technol. Biotechnol. 2001, 39:305-311.
35. Schikora A., Carreri A., Charpentier E., Hirt H. The dark side of the salad: Salmonella Typhimurium overcomes the innate immune response of Arabidopsis thaliana and shows an endopathogenic lifestyle. PLoS One 2009, 3:e2279.
36. Talley J.L., Wayadande A.C., Wasala L.P., Gerry A.C., Fletcher J., DeSilva U., Gilliland S.E. Association of Escherichia coli O157:H7 with filth flies (Muscidae and Calliphoridae) captured in leafy greens fields and experimental transmission of E. coli O157:H7 to spinach leaves by house flies (Diptera: Muscidae). J. Food Prot. 2009, 72:1547-1552.
37. Tournas V.H. Spoilage of vegetable crops by bacteria and fungi and related health hazards. Crit. Rev. Microbiol. 2005, 31:33-44.
38. Warriner K., Namvar A. The tricks learnt by human enteric pathogens from phytopathogens to persist within the plant environment. Curr. Opin. Biotechnol. 2010, 21:131-136.