Colonization and internalization of salmonella enterica in tomato plants

Applied and Environmental Microbiology

Volumn 79, Issue 8, 2013, Pages 2494-2502

  Zheng, Jie ^a   Allard, Sarah ^a   Reynolds, Sara ^b   Millner, Patricia ^b   Arce, Gabriela ^a   Blodgett, Robert J ^a   Brown, Eric W ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PATHOGENIC BACTERIUM; PLANT-MICROBE INTERACTIONS; SALMONELLA ENTERICA; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA SEROVAR; SALMONELLA SEROVARS; SOLANUM LYCOPERSICUM; TOMATO CULTIVATION;

CONTAMINATION; FRUITS; PLANTS (BOTANY); SOIL CONDITIONERS; SOILS;

SALMONELLA;

COLONIZATION; DISEASE PREVALENCE; GROWTH; LOAM; MICROBIAL COMMUNITY; NICHE; PATHOGENICITY; PLANT COMMUNITY; SANDY SOIL; SURVIVAL; VEGETABLE;

ARTICLE; CLASSIFICATION; FLOWER; FOOD CONTROL; FRUIT; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIOLOGY; MOLECULAR TYPING; PLANT LEAF; PLANT ROOT; RHIZOSPHERE; SALMONELLA ENTERICA; TOMATO;

FLOWERS; FOOD MICROBIOLOGY; FRUIT; HUMANS; LYCOPERSICON ESCULENTUM; MOLECULAR TYPING; PLANT LEAVES; PLANT ROOTS; RHIZOSPHERE; SALMONELLA ENTERICA; SOIL MICROBIOLOGY;

LYCOPERSICON ESCULENTUM; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM;

EID: 84876170942     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03704-12     Document Type: Article

References (35)

1. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 17:7-15.
2. CDC. 2011. Vital signs: incidence and trends of infection with pathogens transmitted commonly through food-foodborne diseases active surveil-lance network, 10 U.S. sites, 1996 -2010. MMWR Morb. Mortal. Wkly. Rep. 60:749 -755.
3. CDC. 2011. Surveillance for foodborne disease outbreaks-United States, 2008. MMWR Morb. Mortal. Wkly. Rep. 60:1197-1202.
4. Guo X, van Iersel MW, Chen J, Brackett RE, Beuchat LR. 2002. Evidence of association of salmonellae with tomato plants grown hydro-ponically in inoculated nutrient solution. Appl. Environ. Microbiol. 68: 3639-3643.
5. Guo X, Chen J, Brackett RE, Beuchat LR. 2001. 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. 67:4760-4764.
6. Gu G, Hu J, Cevallos-Cevallos JM, Richardson SM, Bartz JA, van Bruggen AH. 2011. Internal colonization of Salmonella enterica serovar Typhimurium in tomato plants. PLoS One 6:e27340. doi:10.1371/journal.pone.0027340.
7. Hintz LD, Boyer RR, Ponder MA, Williams RC, Rideout SL. 2010. Recovery of Salmonella enterica Newport introduced through irrigation water from tomato (Lycopersicum esculentum) fruit, roots, stems, and leaves. HortScience 45:675-678.
8. Barak JD, Liang AS. 2008. Role of soil, crop debris, and a plant pathogen in Salmonella enterica contamination of tomato plants. PLoS One 3:e1657. doi:http://dx.doi.org/10.1371/journal.pone.000165710.1371/journal.pone.0001657.
9. Jablasone J, Brovko LY, Griffiths MW. 2004. A research note: the potential for transfer of Salmonella from irrigation water to tomatoes. J. Sci. Food Agric. 84:287-289.
10. Miles JM, Sumner SS, Boyer RR, Williams RC, Latimer JG, McKinney JM. 2009. Internalization of Salmonella enterica serovar Montevideo into greenhouse tomato plants through contaminated irrigation water or seed stock. J. Food Prot. 72:849-852.
11. Barak JD, Kramer LC, Hao LY. 2011. Colonization of tomato plants by Salmonella enterica is cultivar dependent, and type 1 trichomes are preferred colonization sites. Appl. Environ. Microbiol. 77:498-504.
12. Cheng CM, Van Khanh T, Lin W, Ruby RM. 2009. Interlaboratory validation of a real-time PCR 24-hour rapid method for detection of Salmonella in foods. J. Food Prot. 72:945-951.
13. Fitzgerald C, Collins M, van Duyne S, Mikoleit M, Brown T, Fields P. 2007. Multiplex, bead-based suspension array for molecular determination of common Salmonella serogroups. J. Clin. Microbiol. 45:3323-3334.
14. McQuiston JR, Waters RJ, Dinsmore BA, Mikoleit ML, Fields PI. 2011. Molecular determination of H antigens of Salmonella by use of a microsphere-based liquid array. J. Clin. Microbiol. 49:565-573.
15. Franz E, Visser AA, Van Diepeningen AD, Klerks MM, Termorshuizen AJ, van Bruggen AH. 2007. Quantification of contamination of lettuce by GFP-expressing Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium. Food Microbiol. 24:106-112.
16. CDC. 2009. Standard protocol molecular determination of serotype in Salmonella, workshop on molecular determination of serotype of Salmonella. Centers for Disease Control and Prevention, Atlanta, GA.
17. Clopper CJ, Pearson ES. 1934. The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 26:404-413.
18. Hanning IB, Nutt JD, Ricke SC. 2009. Salmonellosis outbreaks in the United States due to fresh produce: sources and potential intervention measures. Foodborne Pathog. Dis. 6:635-648.
19. Patchanee P, Molla B, White N, Line DE, Gebreyes WA. 2010. Tracking Salmonella contamination in various watersheds and phenotypic and genotypic diversity. Foodborne Pathog. Dis. 7:1113-1120.
20. Gorski L, Parker CT, Liang A, Cooley MB, Jay-Russell MT, Gordus AG, Atwill ER, Mandrell RE. 2011. Prevalence, distribution, and diversity of Salmonella enterica in a major produce region of California. Appl. Environ. Microbiol. 77:2734-2748.
21. Bell RL, Cao G, Meng J, Allard MW, Keys C, Hill T, Ottesen A, Brown EW. 2012. Salmonella Newport contamination of produce: ecological, genetic, and epidemiological aspects. In Monte AS, Santos PED (ed), Salmonella: classification, genetics and disease outbreaks. Nova Science Publishers, Inc., Hauppauge, NY.
22. Micallef SA, Rosenberg Goldstein RE, George A, Kleinfelter L, Boyer MS, McLaughlin CR, Estrin A, Ewing L, Jean-Giles Beaubrun J, Hanes DE, Kothary MH, Tall BD, Razeq JH, Joseph SW, Sapkota AR. 2012. Occurrence and antibiotic resistance of multiple Salmonella serotypes recovered from water, sediment and soil on mid-Atlantic tomato farms. Environ. Res. 114:31-39.
23. Greene SK, Daly ER, Talbot EA, Demma LJ, Holzbauer S, Patel NJ, Hill TA, Walderhaug MO, Hoekstra RM, Lynch MF, Painter JA. 2008. Recurrent multistate outbreak of Salmonella Newport associated with tomatoes from contaminated fields, 2005. Epidemiol. Infect. 136:157-165.
24. Shi X, Namvar A, Kostrzynska M, Hora R, Warriner K. 2007. Persistence and growth of different Salmonella serovars on pre- and postharvest tomatoes. J. Food Prot. 70:2725-2731.
25. Bernstein N, Sela S, Neder-Lavon S. 2007. Effect of irrigation regimes on persistence of Salmonella enterica serovar Newport in small experimental pots designed for plant cultivation. Irrig. Sci. 26:1-8.
26. Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW. 1997. Bacterial endophytes in agricultural crops. Can. J. Microbiol. 43:895-914.
27. Weaver JE, Bruner WE. 1927. Chapter XXVI: tomato. In Root development of vegetable crops, 1st ed. McGraw-Hill Book Company, Inc., New York, NY.
28. Ibekwe AM, Papiernik SK, Gan J, Yates SR, Yang CH, Crowley DE. 2001. Impact of fumigants on soil microbial communities. Appl. Environ. Microbiol. 67:3245-3257.
29. Haley BJ, Cole DJ, Lipp EK. 2009. Distribution, diversity, and seasonality of waterborne salmonellae in a rural watershed. Appl. Environ. Microbiol. 75:1248-1255.
30. Garcia R, Bælum J, Fredslund L, Santorum P, Jacobsen CS. 2010. Influence of temperature and predation on survival of Salmonella enterica serovar Typhimurium and expression of invA in soil and manure-amended soil. Appl. Environ. Microbiol. 76:5025-5031.
31. Howard MB, Hutcheson SW. 2003. Growth dynamics of Salmonella enterica strains on alfalfa sprouts and in waste seed irrigation water. Appl. Environ. Microbiol. 69:548-553.
32. Lenski RE, Mongold JA, Sniegowski PD, Travisano M, Vasi F, Gerrish PJ, Schmidt TM. 1998. Evolution of competitive fitness in experimental populations of E. coli: what makes one genotype a better competitor than another? Antonie Van Leeuwenhoek 73:35-47.
33. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJ, Relman DA. 2012. The application of ecological theory toward an understanding of the human microbiome. Science 336:1255-1262.
34. Anthon GE, LeStrange M, Barrett DM. 2011. Changes in pH, acids, sugars and other quality parameters during extended vine holding of ripe processing tomatoes. J. Sci. Food Agric. 91:1175-1181.
35. Chung KC, Goepfert JM. 1970. Growth of Salmonella at low pH. J. Food Sci. 35:326-328.