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Detection of Salmonella typhimurium Grown Directly on Tomato Surface Using Phage-Based Magnetoelastic Biosensors

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Abstract

A phage-based magnetoelastic (ME) biosensor method is being developed for on-site pathogen detection in fresh fruits and vegetables. Salmonella typhimurium was directly grown with minimal nutrients on tomato surfaces in order to mimic natural environmental conditions. S. typhimurium was inoculated on the surface of fresh tomatoes, and ME biosensors were used to detect the bacteria. The populations of S. typhimurium after 24-h incubation time at 37°C and 100% relative humidity were 6.1 and 7.8 logCFU/cm2 after starting with initial inoculations of 3.0 and 5.0 logCFU/cm2, respectively. After evident growth, measurement sensors with E2 phage immobilized on their surfaces and control sensors devoid of E2 phage were placed on the inoculated tomato surfaces and the resonant frequency shifts were measured. As the population of S. typhimurium increased, the resonant frequency shifts of the measurement sensors significantly increased (P < 0.01), exhibiting 6,680 ± 665 and 9,384 ± 457 Hz for the populations of 6.1 and 7.8 logCFU/cm2, respectively. SEM images confirmed that the measurement sensor resonant frequency shifts were due to S. typhimurium binding with E2 phage. This study demonstrated that the ME biosensor method could detect S. typhimurium grown directly on tomato surfaces with limited sample preparation procedures. Therefore, the ME biosensor could be applied as a cost and time effective, relatively simple, practically suitable on-site detection method for S. typhimurium in fresh produce.

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References

  • Bakhrouf, A., Abdallah, F. B., & Lagha, R. (2008). Morphological changes of starved Salmonella enterica serovar Agona cells in soil after resuscitation. Annals of Microbiology, 58(3), 521–525.

    Article  Google Scholar 

  • Beuchat, L. R. (2002). Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes and Infection, 4, 413–423.

    Article  Google Scholar 

  • Beuchat, L. R., & Brackett, R. E. (1991). Behavior of Listeria monocytogenes inoculated into raw tomatoes and processed tomato products. Applied and Environmental Microbiology, 57, 1367–1371.

    CAS  Google Scholar 

  • Beuchat, L. R., & Ryu, J. H. (1997). Produce handling and processing practices. Emerging Infectious Diseases, 3, 439–465.

    Article  Google Scholar 

  • Bisha, B., & Brehm-Stecher, B. F. (2009). Simple adhesive-tape-based sampling of tomato surfaces combined with rapid fluorescence in situ hybridization for Salmonella detection. Applied and Environmental Microbiology, 75(5), 1450–1455.

    Article  CAS  Google Scholar 

  • Brackett, R. E. (1999). Incidence, contributing factors, and control of bacterial pathogens in produce. Postharvest Biology and Technology, 15, 305–311.

    Article  Google Scholar 

  • Dickson, J. S., Siragusa, G. R., & Wary, J. E. (1992). Predicting the growth of Salmonella typhimurium on beef by using the temperature function integration technique. Applied and Environmental Microbiology, 58(11), 3482–3487.

    CAS  Google Scholar 

  • Heaton, J. C., & Jones, K. (2008). Microbial contamination of fruit and vegetables and the behavior of enteropathogens in the phyllosphere: a review. Journal of Applied Microbiology, 104, 613–626.

    Article  CAS  Google Scholar 

  • Huang, S., Li, S. Q., Yang, H., Johnson, M. L., Wan, J., Chen, I., et al. (2008). Optimization of phage-based magnetoelastic biosensor performance. Special Issue of Sensors & Transducers Journal on Microsystems: Technology and Application, 3(12), 87–96.

    CAS  Google Scholar 

  • Huang, S., Yang, H., Lakshmanan, R. S., Johnson, M. L., Wan, J., Chen, I. H., et al. (2009). Sequential detection of Salmonella typhimurium and Bacillus anthracis spores using magnetoelastic biosensors. Biosensors and Bioelectronics, 24(6), 1730–1736.

    Article  CAS  Google Scholar 

  • Guntupalli, R., Lakshmanan, R. S., Hu, J., Huang, T. S., Barbaree, J. M., Vodyanoy, V., et al. (2007). Rapid and sensitive magnetoelastic biosensors for the detection of Salmonella typhimurium in a mixed microbial population. Journal of Microbiological Methods, 70(1), 112–118.

    Article  CAS  Google Scholar 

  • Guo, X., Chen, J., Brackett, R. E., & Beuchat, L. R. (2001). Survival of Salmonella on and in tomato plants from the time of inoculation at flowering and early stages of fruit development through fruit ripening. Applied and Environmental Microbiology, 67(10), 4760–4764.

    Article  CAS  Google Scholar 

  • Guo, X., Chen, J., Brackett, R. E., & Beuchat, L. R. (2002). Survival of Salmonella on tomatoes stored at high relative humidity, in soil, and on tomatoes in contact with soil. Journal of Food Protection, 65(2), 274–279.

    Google Scholar 

  • Gupta, S. D., Nalluswami, K., Snider, C., Perch, M., Balasegaram, M., Burmeister, D., Lockett, J., Sandt, C., Hoekstra, R.M., & Montgomery, S. (2007). Outbreak of Salmonella Braenderup infections associated with roma tomatoes, northeastern United States, 2004: a useful method for subtyping exposures in field investigations. Epidemiology and Infection, 135, 1165–1173.

    Article  CAS  Google Scholar 

  • Iturriaga, M. H., Tamplin, M. L., & Escartín, E. F. (2007). Colonization of tomatoes by Salmonella Montevideo is affected by relative humidity and storage temperature. Journal of Food Protection, 70(1), 30–34.

    Google Scholar 

  • Lakshmanan, R. S., Guntupalli, R., Hu, J., Petrenko, V. A., Barbaree, J. M., & Chin, B. A. (2007). Detection of Salmonella typhimurium in fat free milk using a phage immobilized magnetoelastic sensor. Sensors and Actuators B-Chemical, 126(2), 544–550.

    Article  Google Scholar 

  • Li, S., Li, Y., Chen, H., Horikawa, S., Shen, W., Simonian, A., et al. (2010). Direct detection of Salmonella typhimurium on fresh produce using phage-based magnetoelastic biosensors. Biosensors and Bioelectronics, 26, 1313–1319.

    Article  CAS  Google Scholar 

  • Lynch, M. F., Tauxe, R. V., & Hedberg, C. W. (2009). The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiology and Infection, 137, 307–315.

    Article  CAS  Google Scholar 

  • Matthews, K. R. (2006). Microorganisms associated with fruits and vegetables. In K. R. Matthews (Ed.), Microbiology of fresh produce (pp. 1–19). Washington, DC: ASM Press.

    Google Scholar 

  • Meng, J., & Doyle, M.P. (2002). Introduction. Microbiological food safety. Microbes and Infection, 4(4), 395–397.

  • Petrenko, V. A., & Sorokulova, I. B. (2004). Detection of biological threats. A challenge for directed molecular evolution. Journal of Microbiological Methods, 58(2), 147–168.

    Article  CAS  Google Scholar 

  • Shen, W., Lakshmanan, R. S., Mathison, L. C., Petrenko, V. A., & Chin, B. A. (2009). Phage coated magnetoelastic micro-biosensors for real-time detection of Bacillus anthracis spores. Sensors and Actuators B-Chemical, 137, 501–506.

    Article  Google Scholar 

  • Shi, X., Namvar, A., Kostrzynska, M., Hora, R., & Warriner, K. (2007). Persistence and growth of different Salmonella serovars on pre-and post-harvest tomatoes. Journal of Food Protection, 12, 2725–2731.

    Google Scholar 

  • Sivapalasingam, S., Friedman, C. R., Cohen, L., & Tauxe, R. V. (2004). Fresh produce: a growing cause of outbreaks of foodborne illnesses in the United States, 1973–1997. Journal of Food Protection, 7, 2342–2353.

    Google Scholar 

  • Sorokulova, I. B., Olsen, E. V., Chen, I. H., Fiebor, B., Barbaree, J. M., Vodyanoy, V. J., et al. (2005). Landscape phage probes for Salmonella typhimurium. Journal of Microbiological Methods, 63(1), 55–72.

    Article  CAS  Google Scholar 

  • Tauxe, R., Kruse, H., Hedberg, C., Potter, M., Madden, J., & Wachsmuth, K. (1997). Microbial hazards and emerging issues associated with produce: a preliminary report to the national advisory committee on microbiologic criteria for foods. Journal of Food Protection, 60, 1400–1408.

    Google Scholar 

  • Wei, C. I., Huang, T. S., Kim, J. M., Lin, W. F., Tamplin, M. L., & Bartz, J. A. (1995). Growth and survival of Salmonella montevideo on tomatoes and disinfection with chlorinated water. Journal of Food Protection, 58(8), 829–836.

    Google Scholar 

  • Zhuang, R. Y., Beuchat, L. R., & Angulo, F. J. (1995). Fate of Salmonella montevideo on and in raw tomatoes as affected by temperature and treatment with chlorine. Applied and Environmental Microbiology, 61(6), 2127–2131.

    CAS  Google Scholar 

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Acknowledgments

This research was supported by the Auburn University Detection and Food Safety (AUDFS) Center with funding from the USDA-CSREES grant (204327 130851 2000).

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  1. Materials Research and Education Center, Auburn University, 275 Wilmore Labs, Auburn, AL 36849, USA

    Mi-Kyung Park, Suiqiong Li & Bryan A. Chin

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  1. Mi-Kyung Park
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  2. Suiqiong Li
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  3. Bryan A. Chin
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Correspondence to Bryan A. Chin.

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This research was supported by the Auburn University Detection and Food Safety (AUDFS) Center with funding from the USDA-CSREES grant (204327 130851 2000).

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Park, MK., Li, S. & Chin, B.A. Detection of Salmonella typhimurium Grown Directly on Tomato Surface Using Phage-Based Magnetoelastic Biosensors. Food Bioprocess Technol 6, 682–689 (2013). https://doi.org/10.1007/s11947-011-0708-2

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