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Differential Bacteriophage Efficacy in Controlling Salmonella in Cattle Hide and Soil Models

Asymptomatic Salmonella carriage in beef cattle is a food safety concern and the beef feedlot environment and cattle hides are reservoirs of this pathogen. Bacteriophages present an attractive non-antibiotic strategy for control of Salmonella in beef. In this study, four diverse and genetically unre...

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Autores principales: Xie, Yicheng, Thompson, Tyler, O’Leary, Chandler, Crosby, Stephen, Nguyen, Quang X., Liu, Mei, Gill, Jason J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8273493/
https://www.ncbi.nlm.nih.gov/pubmed/34262535
http://dx.doi.org/10.3389/fmicb.2021.657524
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author Xie, Yicheng
Thompson, Tyler
O’Leary, Chandler
Crosby, Stephen
Nguyen, Quang X.
Liu, Mei
Gill, Jason J.
author_facet Xie, Yicheng
Thompson, Tyler
O’Leary, Chandler
Crosby, Stephen
Nguyen, Quang X.
Liu, Mei
Gill, Jason J.
author_sort Xie, Yicheng
collection PubMed
description Asymptomatic Salmonella carriage in beef cattle is a food safety concern and the beef feedlot environment and cattle hides are reservoirs of this pathogen. Bacteriophages present an attractive non-antibiotic strategy for control of Salmonella in beef. In this study, four diverse and genetically unrelated Salmonella phages, Sergei, Season12, Sw2, and Munch, were characterized and tested alone and in combination for their ability to control Salmonella in cattle hide and soil systems, which are relevant models for Salmonella control in beef production. Phage Sergei is a member of the genus Sashavirus, phage Season12 was identified as a member of the Chivirus genus, Sw2 was identified as a member of the T5-like Epseptimavirus genus, and Munch was found to be a novel “jumbo” myovirus. Observed pathogen reductions in the model systems ranged from 0.50 to 1.75 log(10) CFU/cm(2) in hides and from 0.53 to 1.38 log(10) CFU/g in soil, with phages Sergei and Sw2 producing greater reductions (∼1 log(10) CFU/cm(2) or CFU/g) than Season12 and Munch. These findings are in accordance with previous observations of phage virulence, suggesting the simple ability of a phage to form plaques on a bacterial strain is not a strong indicator of antimicrobial activity, but performance in liquid culture assays provides a better predictor. The antimicrobial efficacies of phage treatments were found to be phage-specific across model systems, implying that a phage capable of achieving bacterial reduction in one model is more likely to perform well in another. Phage combinations did not produce significantly greater efficacy than single phages even after 24 h in the soil model, and phage-insensitive colonies were not isolated from treated samples, suggesting that the emergence of phage resistance was not a major factor limiting efficacy in this system.
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spelling pubmed-82734932021-07-13 Differential Bacteriophage Efficacy in Controlling Salmonella in Cattle Hide and Soil Models Xie, Yicheng Thompson, Tyler O’Leary, Chandler Crosby, Stephen Nguyen, Quang X. Liu, Mei Gill, Jason J. Front Microbiol Microbiology Asymptomatic Salmonella carriage in beef cattle is a food safety concern and the beef feedlot environment and cattle hides are reservoirs of this pathogen. Bacteriophages present an attractive non-antibiotic strategy for control of Salmonella in beef. In this study, four diverse and genetically unrelated Salmonella phages, Sergei, Season12, Sw2, and Munch, were characterized and tested alone and in combination for their ability to control Salmonella in cattle hide and soil systems, which are relevant models for Salmonella control in beef production. Phage Sergei is a member of the genus Sashavirus, phage Season12 was identified as a member of the Chivirus genus, Sw2 was identified as a member of the T5-like Epseptimavirus genus, and Munch was found to be a novel “jumbo” myovirus. Observed pathogen reductions in the model systems ranged from 0.50 to 1.75 log(10) CFU/cm(2) in hides and from 0.53 to 1.38 log(10) CFU/g in soil, with phages Sergei and Sw2 producing greater reductions (∼1 log(10) CFU/cm(2) or CFU/g) than Season12 and Munch. These findings are in accordance with previous observations of phage virulence, suggesting the simple ability of a phage to form plaques on a bacterial strain is not a strong indicator of antimicrobial activity, but performance in liquid culture assays provides a better predictor. The antimicrobial efficacies of phage treatments were found to be phage-specific across model systems, implying that a phage capable of achieving bacterial reduction in one model is more likely to perform well in another. Phage combinations did not produce significantly greater efficacy than single phages even after 24 h in the soil model, and phage-insensitive colonies were not isolated from treated samples, suggesting that the emergence of phage resistance was not a major factor limiting efficacy in this system. Frontiers Media S.A. 2021-06-28 /pmc/articles/PMC8273493/ /pubmed/34262535 http://dx.doi.org/10.3389/fmicb.2021.657524 Text en Copyright © 2021 Xie, Thompson, O’Leary, Crosby, Nguyen, Liu and Gill. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Xie, Yicheng
Thompson, Tyler
O’Leary, Chandler
Crosby, Stephen
Nguyen, Quang X.
Liu, Mei
Gill, Jason J.
Differential Bacteriophage Efficacy in Controlling Salmonella in Cattle Hide and Soil Models
title Differential Bacteriophage Efficacy in Controlling Salmonella in Cattle Hide and Soil Models
title_full Differential Bacteriophage Efficacy in Controlling Salmonella in Cattle Hide and Soil Models
title_fullStr Differential Bacteriophage Efficacy in Controlling Salmonella in Cattle Hide and Soil Models
title_full_unstemmed Differential Bacteriophage Efficacy in Controlling Salmonella in Cattle Hide and Soil Models
title_short Differential Bacteriophage Efficacy in Controlling Salmonella in Cattle Hide and Soil Models
title_sort differential bacteriophage efficacy in controlling salmonella in cattle hide and soil models
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8273493/
https://www.ncbi.nlm.nih.gov/pubmed/34262535
http://dx.doi.org/10.3389/fmicb.2021.657524
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