Loading next page...
/lp/elsevier/prophage-induction-reduces-shiga-toxin-producing-escherichia-coli-stec-wbIf0oTy6h
- Publisher
- Elsevier
- Copyright
- Copyright © 2018 Elsevier Ltd
- ISSN
- 0956-7135
- eISSN
- 1873-7129
- D.O.I.
- 10.1016/j.foodcont.2018.02.001
- Publisher site
- See Article on Publisher Site
Abstract
Fresh produce is increasingly implicated in foodborne outbreaks and most fresh produce is consumed raw, emphasizing the need to develop non-thermal methods to control foodborne pathogens. This study investigates bacterial cell lysis through induction of prophages as a novel approach to control foodborne bacterial pathogens on fresh produce. Shiga toxin producing Escherichia coli (STEC) and Salmonella enterica isolates were exposed to different prophage inducers (i.e. mitomycin C or streptonigrin) and growth of the cells was monitored by measuring the optical density (OD600) during incubation at 37 °C. Beginning at three hours after addition of the inducer, all concentrations (0.5, 1, 2 μg/mL) of mitomycin C, or 2 μg/mL streptonigrin significantly reduced the OD600 in broth cultures, in a concentration dependent manner, relative to cultures where no inducer was added. PCR confirmed bacterial release of induced bacteriophages and demonstrated that a single compound could successfully induce multiple types of prophages. The ability of mitomycin C to induce prophages in STEC O157:H7 and in S. enterica (serovars Typhimurium and Newport) on fresh produce was evaluated by inoculating red greenhouse tomatoes or spinach leaves with 5 × 107 and 5 × 108 colony forming units, respectively. After allowing time for the inoculum to dry on the fresh produce samples, 6 μg/mL mitomycin C was sprayed onto each sample, while control samples were sprayed with water. Following overnight incubation at 4 °C, the bacterial cells were recovered and plate counts were performed. A 3 log reduction in STEC O157:H7 cells was observed on tomatoes sprayed with mitomycin C compared to those sprayed with water, while a 1 log reduction was obtained on spinach. Similarly, spraying mitomycin C on tomatoes and spinach inoculated with S. enterica isolates resulted in a 1-1.5 log and 2 log reduction, respectively. These findings serve as a proof of concept that prophage induction can effectively control bacterial foodborne pathogens on fresh produce.
Journal
Food Control – Elsevier
Published: Jul 1, 2018
Recommended Articles
Loading...
References
-
Antibiotics in feed induce prophages in swine fecal microbiomesAllen, H.K.; Looft, T.; Bayles, D.O.; Humphrey, S.; Levine, U.Y.; Alt, D.
-
Serotype-converting bacteriophages and O-antigen modification in Shigella flexneriAllison, G.E.; Verma, N.K.
-
PHASTER: A better, faster version of the PHAST phage search toolArndt, D.; Grant, J.R.; Marcu, A.; Sajed, T.; Pon, A.; Liang, Y.
-
Comparative efficacy of Zataria multiflora Boiss., Origanum compactum and Eugenia caryophyllus essential oils against E. coli O157:H7, feline calicivirus and endogenous microbiota in commercial baby-leaf saladsAzizkhani, M.; Elizaquivel, P.; Sanchez, G.; Selma, M.V.; Aznar, R.
-
SOS, the formidable strategy of bacteria against aggressionsBaharoglu, Z.; Mazel, D.
-
Diversity of phage integrases in enterobacteriaceae: Development of markers for environmental analysis of temperate phagesBalding, C.; Bromley, S.A.; Pickup, R.W.; Saunders, J.R.
-
Combined efficacy of nisin and pediocin with sodium lactate, citric acid, phytic acid, and potassium sorbate and EDTA in reducing the Listeria monocytogenes population of inoculated fresh-cut produceBari, M.L.; Ukuku, D.O.; Kawasaki, T.; Inatsu, Y.; Isshiki, K.; Kawamoto, S.
-
Multistate foodborne disease outbreaks associated with raw tomatoes, United States, 1990-2010: A recurring public health problemBennett, S.D.; Littrell, K.W.; Hill, T.A.; Mahovic, M.; Behravesh, C.B.
-
Evolution of foodborne pathogens via temperate bacteriophage-mediated gene transferBrabban, A.D.; Hite, E.; Callaway, T.R.
-
Reported foodborne outbreaks due to fresh produce in the United States and European Union: Trends and causesCallejon, R.M.; Rodriguez-Naranjo, M.I.; Ubeda, C.; Hornedo-Ortega, R.; Garcia-Parrilla, M.C.; Troncoso, A.M.
-
Induction of the SOS response by bacteriophage lytic development in Salmonella entericaCampoy, S.; Hervas, A.; Busquets, N.; Erill, I.; Teixido, L.; Barbe, J.
-
Prophage genomicsCanchaya, C.; Proux, C.; Fournous, G.; Bruttin, A.; Brussow, H.
-
Elevated enterotoxin A expression and formation in Staphylococcus aureus and its association with prophage inductionCao, R.; Zeaki, N.; Wallin-Carlquist, N.; Skandamis, P.N.; Schelin, J.; Radstrom, P.
-
Multistate outbreak of listeriosis associated with Jensen Farms cantaloupe–United States, August-September 2011Centers for Disease Control & Prevention
-
Multistate outbreak of Salmonella Typhimurium and Salmonella Newport infections linked to cantaloupeCenters for Disease Control & Prevention
-
Outbreak of Escherichia coli O104:H4 infections associated with sprout consumption - Europe and North America, May-July 2011Centers for Disease Control & Prevention
-
Reports of selected Salmonella outbreak investigationsCenters for Disease Control & Prevention
-
The effects of streptonigrin on cultured human leukocytesCohen, M.M.; Shaw, M.W.; Craig, A.P.
-
In vivo transduction of an Stx-encoding phage in ruminantsCornick, N.A.; Helgerson, A.F.; Mai, V.; Ritchie, J.M.; Acheson, D.W.
-
Bacteriophages: An underestimated role in human and animal health?De Paepe, M.; Leclerc, M.; Tinsley, C.R.; Petit, M.A.
-
Outbreaks caused by sprouts, United States, 1998-2010: Lessons learned and solutions neededDechet, A.M.; Herman, K.M.; Chen Parker, C.; Taormina, P.; Johanson, J.; Tauxe, R.V.
-
Phages rarely encode antibiotic resistance genes: A cautionary tale for virome analysesEnault, F.; Briet, A.; Bouteille, L.; Roux, S.; Sullivan, M.B.; Petit, M.A.
-
Agricultural commodity markets past developments fruits and vegetables. An analysis of consumption, production and trade based on statistics from the Food and Agriculture Organization (FAO)European Commission
-
Scientific Opinion on the risk posed by pathogens in food of non-animal origin. Part 1 (outbreak data analysis and risk ranking of food/pathogen combinations)European Food Safety Authority, Panel on Biological Hazards
-
Scientific Opinion on the risk posed by pathogens in food of non-animal origin. Part 2 (Salmonella and Norovirus in berries)European Food Safety Authority, Panel on Biological Hazards
-
Diversity and host range of Shiga toxin-encoding phageGamage, S.D.; Patton, A.K.; Hanson, J.F.; Weiss, A.A.
-
Electrostatic spraying of food-grade organic and inorganic acids and plant extracts to decontaminate Escherichia coli O157:H7 on spinach and iceberg lettuceGanesh, V.; Hettiarachchy, N.S.; Griffis, C.L.; Martin, E.M.; Ricke, S.C.
-
A new Danish Listeria monocytogenes phage typing systemGerner-Smidt, P.; Rosdahl, V.T.; Frederiksen, W.
-
Complete genome sequence of PhiCP51, a temperate bacteriophage of Clostridium perfringensGervasi, T.; Curto, R.L.; Narbad, A.; Mayer, M.J.
-
Guidelines to validate control of cross-contamination during washing of fresh-cut leafy vegetablesGombas, D.; Luo, Y.; Brennan, J.; Shergill, G.; Petran, R.; Walsh, R.
-
The microbiological efficacy of decontamination methodologies for fresh produce: A reviewGoodburn, C.; Wallace, C.A.
-
Phage-based biocontrol strategies to reduce foodborne pathogens in foodsGoodridge, L.D.; Bisha, B.
-
Surveillance for foodborne disease outbreaks - United States, 1998-2008Gould, L.H.; Walsh, K.A.; Vieira, A.R.; Herman, K.; Williams, I.T.; Hall, A.J.
-
Reduction of Salmonella in ground chicken using a bacteriophageGrant, A.; Parveen, S.; Schwarz, J.; Hashem, F.; Vimini, B.
-
International outbreak of multiple Salmonella serotype infections linked to sprouted chia seed powder - USA and Canada, 2013-2014Harvey, R.R.; Heiman Marshall, K.E.; Burnworth, L.; Hamel, M.; Tataryn, J.; Cutler, J.
-
Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12Hayashi, T.; Makino, K.; Ohnishi, M.; Kurokawa, K.; Ishii, K.; Yokoyama, K.
-
Efficacy of disinfectants to reduce Listeria monocytogenes on precut iceberg lettuceHellstrom, S.; Kervinen, R.; Lyly, M.; Ahvenainen-Rantala, R.; Korkeala, H.
-
Outbreaks attributed to fresh leafy vegetables, United States, 1973-2012Herman, K.M.; Hall, A.J.; Gould, L.H.
-
Shiga toxin-encoding bacteriophages–genomes in motionHerold, S.; Karch, H.; Schmidt, H.
-
Genome analysis of the Clostridium difficile phage PhiCD6356, a temperate phage of the Siphoviridae familyHorgan, M.; O’Sullivan, O.; Coffey, A.; Fitzgerald, G.F.; van Sinderen, D.; McAuliffe, O.
-
A molecular mechanism of mitomycin action: Linking of complementary DNA strandsIyer, V.N.; Szybalski, W.
-
Mitomycins and porfiromycin: Chemical mechanism of activation and cross-linking of DNAIyer, V.N.; Szybalski, W.
-
Prophage genomics reveals patterns in phage genome organization and replicationKang, H.S.; McNair, K.; Cuevas, D.; Bailey, B.; Segall, A.; R.A., E
-
A novel restriction-modification system is responsible for temperature-dependent phage resistance in Listeria monocytogenes ECIIKim, J.W.; Dutta, V.; Elhanafi, D.; Lee, S.; Osborne, J.A.; Kathariou, S.
-
Evaluation of anti-SE bacteriophage as feed additives to prevent Salmonella Enteritidis (SE) in BroilerKim, K.H.; Lee, G.Y.; Jang, J.C.; Kim, J.E.; Kim, Y.Y.
-
Listeria phages: Genomes, evolution, and applicationKlumpp, J.; Loessner, M.J.
-
Foodborne outbreaks in Canada linked to produce: 2001 through 2009Kozak, G.K.; MacDonald, D.; Landry, L.; Farber, J.M.
-
Bacteriophage resistance mechanismsLabrie, S.J.; Samson, J.E.; Moineau, S.
-
Effectiveness of a novel spontaneous carvacrol nanoemulsion against Salmonella enterica Enteritidis and Escherichia coli O157:H7 on contaminated mung bean and alfalfa seedsLandry, K.S.; Chang, Y.; McClements, D.J.; McLandsborough, L.
-
Characterization of a new plasmid-like prophage in a pandemic Vibrio parahaemolyticus O3:K6 strainLan, S.F.; Huang, C.H.; Chang, C.H.; Liao, W.C.; Lin, I.H.; Jian, W.N.
-
Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocinLeverentz, B.; Conway, W.S.; Camp, M.J.; Janisiewicz, W.J.; Abuladze, T.; Yang, M.
-
The action of streptonigrin on bacterial DNA metabolism and on induction of phage production in lysogenic bacteriaLevine, M.; Borthwick, M.
-
Development of prototypes of bioactive packaging materials based on immobilized bacteriophages for control of growth of bacterial pathogens in foodsLone, A.; Anany, H.; Hakeem, M.; Aguis, L.; Avdjian, A.C.; Bouget, M.
-
Hydrogen peroxide-mediated induction of the Shiga toxin-converting lambdoid prophage ST2-8624 in Escherichia coli O157:H7Los, J.M.; Los, M.; Wegrzyn, A.; Wegrzyn, G.
-
Additive approach for inactivation of Escherichia coli O157:H7, Salmonella, and Shigella spp. on contaminated fresh fruits and vegetables using bacteriophage cocktail and produce washMagnone, J.P.; Marek, P.J.; Sulakvelidze, A.; Senecal, A.G.
-
Multistate outbreak of listeriosis associated with cantaloupeMcCollum, J.T.; Cronquist, A.B.; Silk, B.J.; Jackson, K.A.; O’Connor, K.A.; Cosgrove, S.
-
The use of hydrogen peroxide for disinfection and sterilization applicationsMcDonnell, G.
-
Mechanism of action of streptonigrin in leukemic cellsMiller, D.S.; Laszlo, J.; McCarty, K.S.; Guild, W.R.; Hochstein, P.
-
Temperate phages in Salmonella enterica serovar Typhimurium: Implications for epidemiologyMmolawa, P.T.; Willmore, R.; Thomas, C.J.; Heuzenroeder, M.W.
-
Genomic characterization provides new insight into Salmonella phage diversityMoreno Switt, A.I.; Orsi, R.H.; den Bakker, H.C.; Vongkamjan, K.; Altier, C.; Wiedmann, M.
-
Activity of mitomycin C, other antibiotics, and serum against lysogenic bacteriaMuschel, L.H.; Schmoker, K.
-
Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7O’Flynn, G.; Ross, R.P.; Fitzgerald, G.F.; Coffey, A.
-
Biopreservative methods to control the growth of foodborne pathogens on fresh-cut lettuceOliveira, M.; Abadias, M.; Colas-Meda, P.; Usall, J.; Vinas, I.
-
Switches in bacteriophage lambda developmentOppenheim, A.B.; Kobiler, O.; Stavans, J.; Court, D.L.; Adhya, S.
-
The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST)Overbeek, R.; Olson, R.; Pusch, G.D.; Olsen, G.J.; Davis, J.J.; Disz, T.
-
Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998-2008Painter, J.A.; Hoekstra, R.M.; Ayers, T.; Tauxe, R.V.; Braden, C.R.; Angulo, F.J.
-
Use of organic acids to inactivate Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria monocytogenes on organic fresh apples and lettucePark, S.H.; Choi, M.R.; Park, J.W.; Park, K.H.; Chung, M.S.; Ryu, S.
-
Concentration of enteric viruses from tap water using an anion exchange resin-based methodPerez-Mendez, A.; Chandler, J.C.; Bisha, B.; Goodridge, L.D.
-
Vibrio vulnificus phage PV94 is closely related to temperate phages of V. cholerae and other Vibrio speciesPryshliak, M.; Hammerl, J.A.; Reetz, J.; Strauch, E.; Hertwig, S.
-
Antibiotic resistance genes in the bacteriophage DNA fraction of human fecal samplesQuiros, P.; Colomer-Lluch, M.; Martinez-Castillo, A.; Miro, E.; Argente, M.; Jofre, J.
-
Proteolytic cleavage of bacteriophage lambda repressor in inductionRoberts, J.W.; Roberts, C.W.
-
Nature of the SOS-inducing signal in Escherichia coli. The involvement of DNA replicationSassanfar, M.; Roberts, J.W.
-
Cleavage of the lambda and P22 repressors by recA proteinSauer, R.T.; Ross, M.J.; Ptashne, M.
-
Developing and optimizing bacteriophage treatment to control enterohemorrhagic Escherichia coli on fresh produceSnyder, A.B.; Perry, J.J.; Yousef, A.E.
-
Using lytic bacteriophages to eliminate or significantly reduce contamination of food by foodborne bacterial pathogensSulakvelidze, A.
-
The mitomycin bioreductive antitumor agents: Cross-linking and alkylation of DNA as the molecular basis of their activityTomasz, M.; Palom, Y.
-
An integrated pipeline for de novo assembly of microbial genomesTritt, A.; Eisen, J.A.; Facciotti, M.T.; Darling, A.E.
-
Hurdles in bacteriophage therapy: Deconstructing the parametersTsonos, J.; Vandenheuvel, D.; Briers, Y.; De Greve, H.; Hernalsteens, J.P.; Lavigne, R.
-
Bacteriophage control of bacterial virulenceWagner, P.L.; Waldor, M.K.
-
Lysogenic conversion by a filamentous phage encoding cholera toxinWaldor, M.K.; Mekalanos, J.J.
-
Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coliWalker, G.C.
-
Acetic acid increases the phage-encoded enterotoxin A expression in Staphylococcus aureusWallin-Carlquist, N.; Cao, R.; Marta, D.; da Silva, A.S.; Schelin, J.; Radstrom, P.
-
Bacteriophages lytic for Salmonella rapidly reduce Salmonella contamination on glass and stainless steel surfacesWoolston, J.; Parks, A.R.; Abuladze, T.; Anderson, B.; Li, M.; Carter, C.
-
Deoxyribonuclease activity in Escherichia coli K12 (lambda) after bacteriophage induction with ultraviolet irradiationWormser, E.H.; Pardee, A.B.
-
Mitomycin-induced synthesis of a Shiga-like toxin from enteropathogenic Escherichia coli H.I.8Yee, A.J.; De Grandis, S.; Gyles, C.L.
-
Transduction of bla(CMY-2), tet(A), and tet(B) from Salmonella enterica subspecies enterica serovar Heidelberg to S. TyphimuriumZhang, Y.; LeJeune, J.T.
-
Quinolone antibiotics induce Shiga toxin-encoding bacteriophages, toxin production, and death in miceZhang, X.; McDaniel, A.D.; Wolf, L.E.; Keusch, G.T.; Waldor, M.K.; Acheson, D.W.
@Phil_Robichaud
@deepthiw
@JoseServera