Effect of spinach cultivar and bacterial adherence factors on survival of escherichia coli o157:H7 on spinach leaves

Journal of Food Protection

Volumn 76, Issue 11, 2013, Pages 1829-1837

  Macarisin, Dumitru ^a   Patel, Jitendra ^a   Bauchan, Gary ^a   Giron, Jorge A ^b   Ravishankar, Sadhana ^c  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL COUNT; BACTERIUM ADHERENCE; CLASSIFICATION; ESCHERICHIA COLI O157; FOOD CONTAMINATION; FOOD CONTROL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIOLOGY; PHYSIOLOGY; PLANT LEAF; SPINACH; TEMPERATURE;

BACTERIAL ADHESION; COLONY COUNT, MICROBIAL; ESCHERICHIA COLI O157; FOOD CONTAMINATION; FOOD MICROBIOLOGY; HUMANS; PLANT LEAVES; SPINACIA OLERACEA; TEMPERATURE;

EID: 84888400489     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X.JFP-12-556     Document Type: Article

References (44)

1. Barak, J. D, C. E. Jahn, D. L. Gibson, and A. O. Charkowski. 2007. The role of cellulose and O-antigen capsule in the colonization of plants by Salmonella enterica. Mol. Plant-Microbe Interact. 20: 1083-1091.
2. Bolin, H. R., and C. C. Huxsoll. 1991. Control of minimally processed carrot (Daucus carota) surface discoloration caused by abrasion peeling. J. Food Sci. 56:416-418.
3. Borges-Baldotto, L. E., and F. Lopes-Olivares. 2008. Phylloepiphytic interaction between bacteria and different plant species in a tropical agricultural system. Can. J. Microbiol. 54:918-931.
4. Boulange-Petermann, L., J. Rault, and M. N. Bellon-Fontaine. 1997. Adhesion of Streptococcus thermophilus to stainless steel with different surface topography and roughness. Biofouling 11:201-216.
5. Brandl, M. T. 2006. Fitness of human enteric pathogens on plants and implications for food safety. Annu. Rev. Phytopathol. 44:367-392.
6. Carder, P. A. 2010. Study of the microbial community of spinach at various stages of plant growth from seed to maturity. M.S. thesis. Virginia Polytechnic Institute and State University, Blacksburg.
7. Ercolani, G. L. 1991. Distribution of epiphytic bacteria on olive leaves and the influence of leaf age and sampling time. Microb. Ecol. 21:35-48.
8. Fett, W. F., and P. H. Cooke. 2003. Scanning electron microscopy of native biofilms on mung bean sprouts. Can. J. Microbiol. 49:45-50.
9. Hart, D. J., J. A. Wright, C. A. Wolfe, J. Dainty, L. R. Perkins, and P. M. Finglas. 2006. Production of intrinsically labelled spinach using stable isotopes (13C or 15N) for the study of folate absorption. Innov. Food Sci. Emerg. Technol. 7:147-151.
10. Hirano, S. S., L. S. Baker, and C. D. Upper. 1996. Raindrop momentum triggers growth of leaf-associated populations of Pseudomonas syringae on field-grown snap bean plants. Appl. Environ. Microbiol. 62:2560-2566.
11. Jacques, M., L. L. Kinkel, and C. E. Morris. 1995. Population sizes, immigration, and growth of epiphytic bacteria on leaves of different ages and positions of field-grown endive (Cichorium endivia var. latifolia). Appl. Environ. Microbiol. 61:899-906.
12. Jeter, C., and A. G. Matthysse. 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.
13. Kadivar, H., and A. E. Stapleton. 2003. Ultraviolet radiation alters maize phyllosphere bacterial diversity. Microb. Ecol. 45:353-361.
14. Kinkel, L. L., M. Wilson, and S. E. Lindow. 1996. Utility of microcosm studies for predicting phylloplane bacterium population sizes in the field. Appl. Environ. Microbiol. 62:3413-3423.
15. Kinkel, L. L., M. Wilson, and S. E. Lindow. 2000. Plant species and plant incubation conditions influence variability in epiphytic bacterial population size. Microb. Ecol. 39:1-11.
16. Klerks, M., E. Franz, G. Zijlstra, and A. Bruggen. 2007. Differential interaction of Salmonella enterica serovars with lettuce cultivars and plant-microbe factors influencing colonization efficiency. ISME J. 1: 620-631.
17. Krimm, U., D. Abanda-Nkpwatt, W. Schwab, and L. Schreiber. 2005. Epiphytic microorganisms on strawberry plants (Fragaria ananassa cv. Elsanta): identification of bacterial isolates and analysis of their interaction with leaf surfaces. FEMS Microbiol. Ecol. 53:483-492.
18. Kutter, S., A. Hartmann, and M. Schmid. 2006. Colonization of barley (Hordeum vulgare) with Salmonella enterica and Listeria spp. FEMS Microbiol. Ecol. 56:262-271.
19. Lee, H. Y., Y. Park, and K. Ko. 2000. Correlation between surface morphology and hydrophilic/hydrophobic conversion of MOCVDTiO2 films. Langmuir 16:7289-7293.
20. Lopez-Velasco, G., G. E. Welbaum, J. O. Falkinham III, and M. A. Ponder. 2011. Phyllopshere bacterial community structure of spinach (Spinacia oleracea) as affected by cultivar and environmental conditions at time of harvest. Diversity 3:721-738.
21. Lyytikainen, O., J. Koort, L. Ward, R. Schildt, P. Ruutu, E. Japisson, N. Timonen, and A. Siitonen. 2004. Molecular epidemiology of an outbreak caused by Salmonella enterica serovar Newport in Finland and the United Kingdom. Epidemiol. Infect. 124:185-192.
22. Macarisin, D., G. Bauchan, and R. Fayer. 2010. Spinacia oleracea L. leaf stomata harboring Cryptosporidium parvum oocysts: a potential threat for food safety. Appl. Environ. Microbiol. 76:555-559.
23. Macarisin, D., J. Patel, G. Bauchan, J. A. Giron, and V. K. Sharma. 2012. Role of curli and cellulose expression in adherence of Escherichia coli O157:H7 to spinach leaves. Foodborne Pathog. Dis. 9:160-167.
24. Macarisin, D., M. Santín, G. Bauchan, and R. Fayer. 2010. Infectivity of Cryptosporidium parvum oocysts after storage of experimentally contaminated apples. J. Food Prot. 73:1824-1829.
25. Matthysse, A. G., R. Deora, M. Mishra, and A. G. Torres. 2008. Polysaccharides cellulose, poly-β-1,6-N-acetyl-D-glucosamine, and colanic acid are required for optimal binding of Escherichia coli O157:H7 strains to alfalfa sprouts and K-12 strains to plastic but not for binding to epithelial cells. Appl. Environ. Microbiol. 74:2384-2390.
26. Mitra, R., E. Cuesta-Alonso, A. C. Wayadande, J. Talley, S. Gilliland, and J. Fletcher. 2009. 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. 72:1521-1530.
27. Monier, J. M., and S. E. Lindow. 2004. Frequency, size, and localization of bacterial aggregates on bean leaf surfaces. Appl. Environ. Microbiol. 70:346-355.
28. Morris, C. E., J. M. Monier, and M. A. Jacques. 1997. Methods for observing microbial biofilms directly on leaf surfaces and recovering them for isolation of culturable microorganisms. Appl. Environ. Microbiol. 63:1570-1576.
29. O'Brien, R. D., and S. E. Lindow. 1989. Effect of plant species and environmental conditions on epiphytic population size of Pseudomonas syringae and other bacteria. Phytopatology 79:619-627.
30. Patel, J., M. Sharma, and S. Ravishakar. 2011. Effect of curli expression and hydrophobicity of Escherichia coli O157:H7 on attachment to fresh produce surfaces. J. Appl. Microbiol. 110:737-745.
31. Rasche, F., R. Trondl, C. Naglreiter, T. G. Reichenauer, and A. Sessitsch. 2006. Chilling and cultivar type affect the diversity of bacterial endophytes colonizing sweet pepper (Capsicum anuum L.). Can. J. Microbiol. 52:1036-1045.
32. Ruppel, S., A. Krumbein, and M. Schreiner. 2008. Composition of the phyllospheric microbial populations on vegetable plants with different glucosinolate and carotenoid compositions. Microb. Ecol. 56:364-372.
33. Saldaña, Z., E. Sánchez, J. Xicohtencatl-Cortes, J. L. Puente, and J. A. Girón. 2011. Surface structures involved in plant stomata and leaf colonization by Shiga-toxigenic Escherichia coli O157:H7. Front. Microbiol. 2:119.
34. Saldaña, Z., J. Xicohtencatl-Cortes, F. Avelino, A. D. Phillips, J. B. Kaper, J. L. Puente, and J. A. Girón. 2009. Synergistic role of curli and cellulose in cell adherence and biofilm formation of attaching and effacing Escherichia coli and identification of Fis as a negative regulator of curli. Environ. Microbiol. 11:992-1006.
35. Solomon, E. B., S. Yaron, and K. R. Matthews. 2002. Transmission of Escherichia coli O157:H7 from contaminated manure and irrigation water to lettuce plant tissue and its subsequent internalization. Appl. Environ. Microbiol. 68:397-400.
36. Tatsumi, Y., A. E. Watada, and W. P. Wergin. 1991. Scanning electron microscopy of carrot stick surface to determine cause of white translucent appearance. J. Food Sci. 56:1357-1359.
37. Thompson, I. P., M. J. Bailey, J. S. Fenlon, T. R. Fermor, A. K. Lilley, J. M. Lynch, P. J. McCormack, M. P. McQuilken, and K. J. Purdy. 1993. Quantitative and qualitative seasonal changes in the microbial community from the phyllosphere of sugar beet. Plant Soil 150:177-191
38. Torres, A. G., C. Jeter, W. Langley, and A. G. Matthysse. 2005. Differential binding of Escherichia coli O157:H7 to alfalfa, human epithelial cells, and plastic is mediated by a variety of surface structures. Appl. Environ. Microbiol. 71:8008-8015.
39. Tydings, H., G. Lopez-Velasco, M. Ponder, and G. Welbaum. 2011. Alterations to the phylloepiphytic bacterial community of spinach with leaf age. Acta Hortic. 917:211-216.
40. Uhlich, G. A., P. H. Cooke, and E. B. Solomon. 2006. Analyses of the red-dry-rough phenotype of an Escherichia coli O157:H7 strain and its role in biofilm formation and resistance to antibacterial agents. Appl. Environ. Microbiol. 72:2564-2572.
41. U.S. Department of Agriculture, Agricultural Marketing Service, National Organic Program. 2011. NOP 1100. Available at: www.ams.usda.gov/AMSv1.0/nop. Accessed 20 August 2013.
42. Wang, H., H. Feng, W. Liang, Y. Luo, and V. Malyarchuk. 2009. Effect of surface roughness on retention and removal of Escherichia coli O157:H7 on surfaces of selected fruits. J. Food Sci. 74:E8-E15.
43. Xicohtencatl-Cortes, J., E. S. Chacó n, Z. Saldaña, E. Freer, and J. A. Giro'n. 2009. Interaction of Escherichia coli O157:H7 with leafy green produce. J. Food Prot.72:1531-1537.
44. Yadav, R. K. P., K. Karamanoli, and D. Vokou. 2005. Bacterial colonization of the phyllosphere of Mediterranean perennial species as influenced by leaf structural and chemical features. Microb. Ecol. 50:185-196.