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References

  1. An derson M, Jaykus LA, Beaulieu S, Dennis S. 2011. Pathogen-produce pair attribution risk ranking tool to prioritize fresh produce commodity and pathogen combinations for further evaluation (P3ARRT). Food Control 22: 1865-1872.
  2. B erger CN, Sodha SV, Shaw RK, Grifiin PM, Pink D, Hand P, Frankel G. 2010. Fresh fruit and vegetables as vehicles for the transmission of human pathogen. Environ. Microbiol. 12:2385-2397.
    Pubmed CrossRef
  3. Beuchat LR. 2002. Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes Infect. 4: 413-423.
    CrossRef
  4. Beuchat LR. 2006. Vectors and conditions for preharvest contamination of fruits and vegetagles with pathogens capable of causing enteric diseases. Br. Food J. 108: 38-53.
    CrossRef
  5. By eon HM, Vodyanoy VJ, Oh JH, Kwon JH, Park MK. 2015. Lytic phage-based magnetoelastic biosensors for on-site detection of methicillin-resistant Staphylococcus aureus on spinach leaves. J. Electrochem. Soc. 162: B230-B235.
  6. CD C. 2009. Surveillance for foodborne disease outbreaks—United States, 2006. MMWR Morb. Mortal. Wkly Rep. 58: 609615.
  7. CD C. 2010. Surveillance for foodborne disease outbreaks—United States, 2007. MMWR Morb. Mortal. Wkly Rep. 59: 973579.
  8. Ch ang WW, Lee CH. 2014. Salmonella as an innovative therapeutic antitumor agent. Int. J. Mol. Sci. 15: 14546-14554.
  9. Doyle MP, Erickson MC. 2008. The problems with fresh produce: an overview. J. Appl. Microbiol. 105: 313-330.
  10. Ha rris LJ, Faber JN, Beuchat LR, Parish ME, Suslow TV, Garrett EH, Busta FF. 2003. Outbreaks associated with fresh produce: incidence, growth, and survival of pathogens in fresh and fresh cut produce. Compr. Rev. Food Sci. Food Saf. 2: 78-141.
  11. Herne TM, Tarlov MJ. 1997. Characterization of DNA probes immobilized on gold surfaces. J. Am. Chem. Soc. 119:8916-8920.
    CrossRef
  12. Hu ang S, Yang H, Lakshmanan RS, Johnson ML, Wan J, Chen IH, et al. 2009. Sequential detection of Salmonella typhimurium and Bacillus anthracis spores using magnetoelastic biosensors. Biosens. Bioelectron. 14: 1730-1736.
  13. I slam M, Morgan J, Doyle MP, Phatak SC, Millner P, Jiang XP. 2004. Fate of Salmonella enterica serovar Typhimurium on carrots and radishes grown in fields treated with contaminated manure composts or irrigation water. Appl. Environ. Microbiol. 70: 2497-2502.
  14. L akshmanan RS, Guntupalli R, Hu J, Petrenko VA, Barbaree JM, Chin BA. 2007. Detection of Salmonella typhimurium in fat free milk using a phage immobilized magnetoelastic sensor. Sens. Actuators B Chem. 126: 544-550.
  15. L i S, Li Y, Chen H, Horikawa S, Shen W, Simonian A, Chin BA. 2010. Direct detection of Salmonella typhimurium on fresh produce using phage-based magnetoelastic biosensors. Biosens. Bioelectron. 26: 1313-1319.
    Pubmed CrossRef
  16. L iu B, Huang PJJ, Zhang X, Wang F, Pautler R, Ip ACF, Liu J. 2013. Parts-per-million of polyethylene glycol as a noninterfering blocking agent for homogeneous biosensor development. Anal. Chem. 85: 10045-10050.
  17. P ark MK, Hirematha N, Weerakoon KA, Vglenov KA, Barbaree JM, Chin BA. 2013. Effects of surface morphologies of fresh produce on the performance of phage-based magnetoelastic biosensors. J. Electrochem. Soc. 160: B6-B12.
  18. Park M K, Li S, Chin BA. 2013. Detection of Salmonella typhimurium grown directly on tomato surface using phagebased magnetoelastic biosensors. Food Bioprocess Technol. 6: 682-689.
    CrossRef
  19. Park MK, O h JH. 2012. Rapid d etection of E. coli O157:H7 on turnip greens using a modified gold biosensor combined with light microscopic imaging system. J. Food Sci. 77:M127-M134.
    Pubmed CrossRef
  20. Park MK, Park JW, Wikle III HC, Chin BA. 2013. Evaluation of phage-based magnetoelastic biosensors for direct detection of Salmonella Typhimurium on spinach leaves. Sens. Actuators B Chem. 176: 1134-1140.
    CrossRef
  21. P ark MK, Weerakoon KA, Oh JH, Chin BA. 2013. The analytical comparison of phage-based magnetoelastic biosensor with TaqMan-based quantitative PCR method to detect Salmonella Typhimurium on cantaloupes. Food Control 33:330-336.
    CrossRef
  22. Petrenko VA, Sorokulova IB. 2004. Detection of biological threats. A challenge for directed molecular evolution. J. Microbiol. Methods 58: 147-168.
    Pubmed CrossRef
  23. Ri quelme MV, Zhao H, Srinivasaraghavan V, Pruden A. 2016. Optimizing blocking of nonspecific bacterial attachment to impedimetric biosensor. Sens Biosensing Res. 8: 47-54.
  24. S hen W, Li S, Park MK, Zhang Z, Cheng Z, Petrenko VA, Chin BA. 2012. Blocking agent optimization for nonspecific binding on phage based magnetoelastic biosensors. J. Electrochem. Soc. 159: B818-B823.
  25. Skogley EO, Dobermann A. 1996. Synthetic ion-exchange resins: soil and environmental studies. J. Environ. Qual. 25:13-24.
    CrossRef
  26. S orokulova IB, Olsen EV, Chen IH, Fiebor B, Barbaree JM, Vodyanoy VJ, et al. 2005. Landscape phage probes for Salmonella typhimurium. J. Microbiol. Methods 63: 55-72.
  27. Str awn LK, Grohn YT, Warchocki S, Worobo RW, Bihn EA, Wiedmann M. 2013. Risk factors associated with Salmonella and Listeria monocytogenes contamination of produce fields. Appl. Environ. Microbiol. 79: 7618-7627.
  28. Su L, Jia W, Hou C, Lei Y. 2011. Microbial biosensors: A review. Biosens. Bioelectron. 26: 1788-1799.
    Pubmed CrossRef
  29. Tovey ER, Bardo BA. 1989. Protein binding to nitrocellulose, nylon and PVDF membranes in immunoassays and electroblotting. J. Biochem. Biophys. Methods 19: 169-183.
    CrossRef
  30. V elusamy V, Arshak K, Korostynska O, Oliwa K, Adley C. 2010. An overview of foodborne pathogen: in the perspective of biosensors. Biotechnol. Adv. 28: 232-254.

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(12): 2051-2059

Published online December 28, 2016 https://doi.org/10.4014/jmb.1609.09062

Copyright © The Korean Society for Microbiology and Biotechnology.

Novel Approach of a Phage-Based Magnetoelastic Biosensor for the Detection of Salmonella enterica serovar Typhimurium in Soil

Mi-Kyung Park 1* and Bryan A. Chin 2

1School of Food Science and Biotechnology, Kyungpook National University, Daegu 41566, Republic of Korea, 2Materials Research and Education Center, Auburn University, Auburn, AL 36849, USA

Received: September 30, 2016; Accepted: October 11, 2016

Abstract

To date, there has been no employment of a magnetoelastic (ME) biosensor method to detect
Salmonella enterica serovar Typhimurium in soil. The ME biosensor method needs to be
investigated and modified for its successful performance. The filtration method, cationexchange
resin method, and combinations of both methods were employed for the extraction
of S. Typhimurium from soil. The number of S. Typhimurium and the resonant frequency shift
of the ME sensor were then compared using a brilliant green sulfa agar plate and an HP 8751A
network analyzer. A blocking study was performed using bovine serum albumin (BSA),
polyethylene glycol (PEG), and casein powder suspension. Finally, the modified ME biosensor
method was performed to detect S. Typhimurium in soil. The number of S. Typhimurium was
significantly decreased from 7.10 log CFU/soil to 4.45-4.72 log CFU/soil after introduction of
the cation-exchange resin method. The greatest resonant frequency shift of the measurement
sensor was found when employing centrifugation and filtration procedures. The resonant
frequency shift of the PEG-blocked measurement sensor was 3,219 ± 755 Hz, which was
significantly greater than those of the BSA- and casein-blocked ME sensor. The optimum
concentration of PEG was determined to be 1.0 mg/ml after considering the resonant shift and
economic issue. Finally, the modified ME biosensor method was able to detect S. Typhimurium in
soil in a dose-response manner. Although these modifications of the ME biosensor method
sacrificed some advantages, such as cost, time effectiveness, and operator friendliness, this
study demonstrated a novel approach of the ME biosensor method to detect S. Typhimurium
in soil.

Keywords: Soil, Phage-based magnetoelastic biosensor, Salmonella Typhimurium, Extraction, Blocking reagent

References

  1. An derson M, Jaykus LA, Beaulieu S, Dennis S. 2011. Pathogen-produce pair attribution risk ranking tool to prioritize fresh produce commodity and pathogen combinations for further evaluation (P3ARRT). Food Control 22: 1865-1872.
  2. B erger CN, Sodha SV, Shaw RK, Grifiin PM, Pink D, Hand P, Frankel G. 2010. Fresh fruit and vegetables as vehicles for the transmission of human pathogen. Environ. Microbiol. 12:2385-2397.
    Pubmed CrossRef
  3. Beuchat LR. 2002. Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes Infect. 4: 413-423.
    CrossRef
  4. Beuchat LR. 2006. Vectors and conditions for preharvest contamination of fruits and vegetagles with pathogens capable of causing enteric diseases. Br. Food J. 108: 38-53.
    CrossRef
  5. By eon HM, Vodyanoy VJ, Oh JH, Kwon JH, Park MK. 2015. Lytic phage-based magnetoelastic biosensors for on-site detection of methicillin-resistant Staphylococcus aureus on spinach leaves. J. Electrochem. Soc. 162: B230-B235.
  6. CD C. 2009. Surveillance for foodborne disease outbreaks—United States, 2006. MMWR Morb. Mortal. Wkly Rep. 58: 609615.
  7. CD C. 2010. Surveillance for foodborne disease outbreaks—United States, 2007. MMWR Morb. Mortal. Wkly Rep. 59: 973579.
  8. Ch ang WW, Lee CH. 2014. Salmonella as an innovative therapeutic antitumor agent. Int. J. Mol. Sci. 15: 14546-14554.
  9. Doyle MP, Erickson MC. 2008. The problems with fresh produce: an overview. J. Appl. Microbiol. 105: 313-330.
  10. Ha rris LJ, Faber JN, Beuchat LR, Parish ME, Suslow TV, Garrett EH, Busta FF. 2003. Outbreaks associated with fresh produce: incidence, growth, and survival of pathogens in fresh and fresh cut produce. Compr. Rev. Food Sci. Food Saf. 2: 78-141.
  11. Herne TM, Tarlov MJ. 1997. Characterization of DNA probes immobilized on gold surfaces. J. Am. Chem. Soc. 119:8916-8920.
    CrossRef
  12. Hu ang S, Yang H, Lakshmanan RS, Johnson ML, Wan J, Chen IH, et al. 2009. Sequential detection of Salmonella typhimurium and Bacillus anthracis spores using magnetoelastic biosensors. Biosens. Bioelectron. 14: 1730-1736.
  13. I slam M, Morgan J, Doyle MP, Phatak SC, Millner P, Jiang XP. 2004. Fate of Salmonella enterica serovar Typhimurium on carrots and radishes grown in fields treated with contaminated manure composts or irrigation water. Appl. Environ. Microbiol. 70: 2497-2502.
  14. L akshmanan RS, Guntupalli R, Hu J, Petrenko VA, Barbaree JM, Chin BA. 2007. Detection of Salmonella typhimurium in fat free milk using a phage immobilized magnetoelastic sensor. Sens. Actuators B Chem. 126: 544-550.
  15. L i S, Li Y, Chen H, Horikawa S, Shen W, Simonian A, Chin BA. 2010. Direct detection of Salmonella typhimurium on fresh produce using phage-based magnetoelastic biosensors. Biosens. Bioelectron. 26: 1313-1319.
    Pubmed CrossRef
  16. L iu B, Huang PJJ, Zhang X, Wang F, Pautler R, Ip ACF, Liu J. 2013. Parts-per-million of polyethylene glycol as a noninterfering blocking agent for homogeneous biosensor development. Anal. Chem. 85: 10045-10050.
  17. P ark MK, Hirematha N, Weerakoon KA, Vglenov KA, Barbaree JM, Chin BA. 2013. Effects of surface morphologies of fresh produce on the performance of phage-based magnetoelastic biosensors. J. Electrochem. Soc. 160: B6-B12.
  18. Park M K, Li S, Chin BA. 2013. Detection of Salmonella typhimurium grown directly on tomato surface using phagebased magnetoelastic biosensors. Food Bioprocess Technol. 6: 682-689.
    CrossRef
  19. Park MK, O h JH. 2012. Rapid d etection of E. coli O157:H7 on turnip greens using a modified gold biosensor combined with light microscopic imaging system. J. Food Sci. 77:M127-M134.
    Pubmed CrossRef
  20. Park MK, Park JW, Wikle III HC, Chin BA. 2013. Evaluation of phage-based magnetoelastic biosensors for direct detection of Salmonella Typhimurium on spinach leaves. Sens. Actuators B Chem. 176: 1134-1140.
    CrossRef
  21. P ark MK, Weerakoon KA, Oh JH, Chin BA. 2013. The analytical comparison of phage-based magnetoelastic biosensor with TaqMan-based quantitative PCR method to detect Salmonella Typhimurium on cantaloupes. Food Control 33:330-336.
    CrossRef
  22. Petrenko VA, Sorokulova IB. 2004. Detection of biological threats. A challenge for directed molecular evolution. J. Microbiol. Methods 58: 147-168.
    Pubmed CrossRef
  23. Ri quelme MV, Zhao H, Srinivasaraghavan V, Pruden A. 2016. Optimizing blocking of nonspecific bacterial attachment to impedimetric biosensor. Sens Biosensing Res. 8: 47-54.
  24. S hen W, Li S, Park MK, Zhang Z, Cheng Z, Petrenko VA, Chin BA. 2012. Blocking agent optimization for nonspecific binding on phage based magnetoelastic biosensors. J. Electrochem. Soc. 159: B818-B823.
  25. Skogley EO, Dobermann A. 1996. Synthetic ion-exchange resins: soil and environmental studies. J. Environ. Qual. 25:13-24.
    CrossRef
  26. S orokulova IB, Olsen EV, Chen IH, Fiebor B, Barbaree JM, Vodyanoy VJ, et al. 2005. Landscape phage probes for Salmonella typhimurium. J. Microbiol. Methods 63: 55-72.
  27. Str awn LK, Grohn YT, Warchocki S, Worobo RW, Bihn EA, Wiedmann M. 2013. Risk factors associated with Salmonella and Listeria monocytogenes contamination of produce fields. Appl. Environ. Microbiol. 79: 7618-7627.
  28. Su L, Jia W, Hou C, Lei Y. 2011. Microbial biosensors: A review. Biosens. Bioelectron. 26: 1788-1799.
    Pubmed CrossRef
  29. Tovey ER, Bardo BA. 1989. Protein binding to nitrocellulose, nylon and PVDF membranes in immunoassays and electroblotting. J. Biochem. Biophys. Methods 19: 169-183.
    CrossRef
  30. V elusamy V, Arshak K, Korostynska O, Oliwa K, Adley C. 2010. An overview of foodborne pathogen: in the perspective of biosensors. Biotechnol. Adv. 28: 232-254.